Free fatty acid receptor 2 explained

Free fatty acid receptor 2 (FFAR2), also termed G-protein coupled receptor 43 (GPR43), is a rhodopsin-like G-protein coupled receptor (also termed GPR or GPCR). It is coded (i.e., its synthesis is directed) by the FFAR2 gene.[1] (FFAR2 and Ffar2 are used respectively to designate the human and animal genes for FFAR2.) In humans, the FFAR2 gene is located on the long (i.e., "q") arm of chromosome 19 at position 13.12 (location notated as 19q13.12).[2] Like other GPCRs, FFAR2s reside on the surface membrane of cells and when bond to one of their activating ligands regulate the function of their parent cells.[3] FFAR2 is a member of a small family of structurally and functionally related GPRs termed free fatty acid receptors (FFARs). This family includes three other receptors which, like FFAR2, are activated by certain fatty acids: FFAR1 (also termed GPR40), FFAR3 (GPR41), and FFAR4 (GPR120). FFAR2 and FFAR3 are activated by short-chain fatty acids[4] whereas FFAR1 and FFAR4 are activated by long-chain fatty acids.[5]

Short-chain fatty acids (i.e., SCFAs) are made by intestinal bacteria (intestinal and intestine are used here to mean the small intestine plus the large intestine's longest portion, the colon). These SCFAs are excreted from the bacteria, enter the hosts tissues, and stimulate cells in these tissues. This stimulation regulates many normal body functions but may result in the inhibition or promotion of various diseases and disorders.[6] The types of bacteria in the intestines can be modified to increase the number of bacteria that make SCFAs by using foods that stimulate the growth of these bacteria (i.e., prebiotics), preparations of SCFA-producing bacteria (i.e., probiotics), or both methods (i.e., synbiotics).[7] Individuals with diseases or disorders that are associated with low levels of the SCFA-producing intestinal bacteria may show improvements in their conditions when treated with prebiotics, probiotics, or synbiotics while individuals with diseases or disorders associated with high levels of SCFAs may show improvements in their conditions when treated with methods, e.g., antibiotics, that reduce the intestinal levels of these bacteria.[6] [5] It is now known that FFAR2 is activated by SCFAs and therefore may function not only in regulating normal body functions but also in inhibiting or promoting many diseases and disorders. Consequently, drugs are being tested for their ability to act more usefully, potently, and effectively than SCFAs to stimulate or inhibit FFAR2 for treating the conditions that appear inhibited or stimulated, respectively, by SCFAs.[8]

Studies have suggested that SCFA-activated FFAR2 regulates blood insulin and glucose levels, inflammation, the development of fat tissues, blood levels of fatty acids, the growth of certain cancerous and non-cancerous cells, and the infectiveness and severity of certain bacteria and viruses. As a result of these actions, FFAR2 may promote or inhibit the development and/or progression of diabetes, inflammatory reactions, obesity, ketoacidosis (i.e., life-threatening increases in blood acidity due to diabetes, starvation, excessive alcohol intake, certain medications, or certain toxins), some types of cancer, maturation of microglia (i.e., immune) cells in the brain and spinal cord,[5] certain neurological diseases,[9] [10] and certain bacterial and viral infections.[11] [12] Here, we review studies on the functions of FFAR2 in health as well as these diseases and disorders.

Activators and inhibitors of FFAR2

FFAR2 and FFR3 are activated primarily by short-chain fatty acids (SCFAs) that are 2 to 6 carbons in length (see length of fatty acids). In humans, acetic acid, which has 2 carbon atoms, is a strong activator of FFAR2 but very weak activator of FFAR3;[13] propionic and butyric acids, which have 3 and 4 carbons, respectively, are strong activators of both FFAR2 and FFAR3;[14] pentanoic acid, which has 5 carbon atoms, is a weak activator of FFAR2 but strong activator of FFAR3;[15] and hexanoic acid, which has 6 carbon atoms, is a weak activator of FFAR3[5] but its effect on FFAR2 has not been reported.[13] More recently, the ketone body fatty acid, acetoacetic acid, while not classified as a SCFA, has been shown to activate FFAR2 with a potency similar to acetic and propionic acids.[16]

Many drugs have been developed that bind to and regulate FFAR2's activity. 1) MOMBA, Sorbate,[14] and Compound 1[17] are orthostatic agonists, i.e., they bind to the same site as SCFAs to activate FFAR2. 2) Compound 58 and AZ1729 are positive allosteric agonists, i.e., they bind to FFAR2 at a site different than the orthostatic binding site and do not by themselves alter FFAR2 activity but enhance the ability of SCFAs and other FFAR2 orthostatic agonists to activate FFAR2.[17] 3) CATPB and BTI-A-404 are reverse agonists, i.e., they bind to the same site as SCFAs but induce a response opposite to that induced by SCFAs.[18] 4) 4-CMTB[14] and TUG-1375[8] [19] are classified as FFAR2 agonists but studies are needed to define their binding sites on FFAR2. And 5) GLPG0974 is an allosteric antagonist, i.e., it inhibits human FFAR2 by binding to a site different than the SCFAs' binding site. GLPGO908 does not bind to or inhibit rodent FFAR2[19] but nonetheless GLPG0974 does have effects in rodents. Off-target actions such as these need to be but often are not considered in studies on the actions of SCFAs and FFAR2 drugs.[14] Furthermore, SCFAs have many actions that do not involve FFAR2, e.g., they activate FFAR3, GPR109A (now termed hydroxycarboxylic acid receptor 2 or HCA2), and two other GPRs, Olfr78 and Olfr558.[6] Most of the studies reported here include experiments in which the actions of SCFAs and FFAR2-regulating drugs in cells and animals are further tested in the cells and animals that have been made to express relatively little or no FFAR2 using gene knockdown or gene knockout methods, respectively. The effects of SCFAs and the drugs should be reduced or absent in cells and animals that under-express or lack FFAR2.

Cells and tissues expressing FFAR2

Studies have detected FFAR2 protein and/or its messenger RNA (an indicator of FFAR2 protein expression) in the following cell types, cell lines, and tissues: 1) human and rodent enteroendocrine K cells, i.e., cells located in the epithelium of the small intestine; 2) human and rodent enteroendocrine L cells, i.e., cells located in the epithelium of the small intestine and colon;[20] [21] [22] [23] 3) human and rodent fat tissue and/or cultured fat cells;[20] 4) cells in human and rodent pancreatic islets (these islets contain the beta cells and alpha cells that synthesize and secrete insulin and glucagon, respectively, into the blood);[24] 5) cells in and/or derived from cells in the human or mouse spleen, lymph nodes, bone marrow, and blood (e.g., monocytes, lymphocytes,[22] and neutrophils[25]); 6) mouse[26] and, based on indirect studies, human[27] dendritic cells; 7) cells in or derived from cells in human and/or rodent kidneys, hearts, brains (e.g., hypothalamus), fetal membranes, and placentas;[22] [28] 8) cells in the taste buds' lingual papillae of human tongues;[22] 9) mouse renal arteries, aortas, and iliac arteries;[29] 10) various human cell lines including SW480, SW620, HT-29, and T84 colon cancer cells, NCI-H716 colon cancer cells that have a lymphoblast morphology, Caco-2 colorectal cancer cells, Hutu-80 duodenal cancer cells, SW872 liposarcoma cells, MDA-MB-231, MDA-MB-436, and MCF7 breast cancer cells, Huh7 and JHH-4 liver cancer cells, THP-1 acute myeloid leukemia cells, U937 acute promyelocytic leukemia cells, and K562 myelogenous leukemia cells;[22] and 11) the various mouse and rat cell lines discussed below. FFAR2 is also expressed in a wide range of tissues in other animals such as cows, pigs, sheep, cats, and dogs.[22]

Formation of SCFAs

The oral administration of glucose elicits a much greater rise in blood insulin levels and a much lower rise in blood glucose levels than those elicited by intravenous glucose infusions. This difference, termed the incretin effect, is due to the activation of FFAR2-bearing intestinal cells by the SCFAs that intestinal bacteria excrete.[30] The microbiotas inside the small intestine and colon of animals and humans consist of a wide range of microorganisms and viruses. The microorganisms ingest the food their hosts consume including soluble dietary fibers, e.g., resistant starch, xanthan gum, and inulin, all three of which are resistant to the hosts' digestive enzymes.[31] Certain microorganisms (e.g., anaerobic bacteria[32]), ferment[20] these dietary fibers to form and then excrete SCFAs (primarily acetic, propionic, and butyric acids[33]).[34] The relative levels of these three SCFAs in the intestines of humans are about 60:20:20, respectively.[11] Intestinal SCFAs activate FFAR2-bearing cells in the nearby intestinal walls and also enter the blood circulation to activate FFAR2-bearing cells in distant tissues.[6] SCFAs may also be made and released by the bacteria and/or host cells in tissue that contain bacterial infections.[11]

FFAR2 functions and actions

Diabetes

Type 2 diabetes

The SCFAs excreted by the soluble dietary fiber-consuming bacteria in the intestine activate FFAR2 on nearby intestinal L-cells. This stimules these cells to secrete GLP-1 (i.e., glucagon-like peptide-1) and PYY (i.e., peptide YY) into the blood. GLP-1 stimulates pancreatic beta cells to secrete insulin into the blood and inhibits pancreatic alpha cells from secreting glucagon into the blood. Since insulin causes cells to take up blood glucose and glucagon causes the liver to release glucose into the blood, FFAR2 activation of L cells lowers blood glucose levels. In addition, PYY[35] and GLP-1[7] reduce appetite and food consumption. The excreted SCFAs also activate FFAR2 on nearby intestinal K cells to simulate their secretion of GIP (i.e., glucose-dependent insulinotropic polypeptide). GIP stimulates insulin secretion but, perhaps paradoxically, also stimulates glucagon secretion; however, the net effect of GIP is to reduce blood glucose levels. GIP also slows gastric motility.[13] [36] In addition, both GLP-1 and GIP protect pancreatic beta cells from dying by apoptosis (see programmed cell death).[13] The SCFAs excreted by the gut microorganisms also pass through the intestinal epithelium to enter the blood stream[33] and activate FFAR2 on cells located in distant tissues such as pancreas beta cells[35] and adipose tissue fat cells.[33]

Individuals with type 2 diabetes, particularly in advanced cases, have nearly completely lost the incretin effect.[37] A study treated non-diabetic, healthy men with the GLP-1 receptor antagonist (i.e., blocker of receptor activation) exendin(9-39)NH2a (also termed avexitide[38]), the GIP receptor antagonist GIP(3-30)NH2,[39] or both antagonists and challenged them with an oral glucose tolerance test. Men treated with either agent responded to the tolerance test with modest decreases in blood insulin levels and modest increases in blood glucose levels. However, men treated with both antagonists responded with very low insulin and very high glucose blood levels: their responses were similar to those in individuals with type 2 diabetes.[37] [40] This study shows that 1) the stimulation of the FFAR2 on K and L cells by SCFAs underlies the differences between oral and intravenous glucose challenges defined by the incretin effect and 2) FFAR2 functions to regulate blood insulin and glucose levels. This does not prove that type 2 diabetes is a FFAR2-incretin disease: post-feeding secretion of the incretins (i.e.,GLP-1 and GIP) is impaired in type 2 diabetes, but the impairment appears to result primarily from decreases in the responsiveness of pancreas alpha cells to GLP-1. This conclusion is supported by studies showing that type 2 diabetic individuals who are treated with large amounts of GLP-1 and challenged with intravenous glucose show changes in blood insulin and glucose levels that are similar to those in non-diabetic individuals.[37] Indeed, GLP-1 agonists, e.g., Dulaglutide,[41] and a first-in-kind GLP-1 and GIP agonist, Tirzepatide,[42] are used to treat type 2 diabetes.

Type 1 diabetes

Ffar2 gene knockout mice (i.e., mice that have had their Ffar2 genes removed or inactivated) have decreased pancreatic beta cell masses at birth and throughout adulthood but do not develop diabetes.[43] However, they do develop defective insulin secretion, glucose intolerance (a prediabetic condition in humans manifested by elevated blood glucose levels),[44] and obesity.[22] This mouse model has some but not all of the features found in human type 1 diabetes. In particular, human type 1 diabetes is at least partly a genetically predisposed autoimmune disease in which an individual's immune system causes inflammation in their pancreatic islets that injures their beta, alpha, and other cells.[13] Non-obese Diabetic mice, i.e., NOD mice, may be a more appropriate model of the human disease. These mice are genetically predisposed to develop tissue-damaging inflammation in their pancreatic islets, insulin insufficiency, and overt diabetes. NOD mice fed a HAMSA or HAMSB diet (i.e., prebiotic diets which cause high intestinal levels of acetic acid or butyric acid, respectively), were partially protected and mice fed a combination of the two diets were fully protected from developing diabetes. Notably, Ffar2 gene knockout NOD mice had far more pancreatic islet inflammation and far less protection from becoming diabetic by either of these diets.[45] Finally, a study of children with pre-type 1 diabetes (base on their having antibodies against multiple pancreatic islet antigens) found that children who had low levels of SCFA-producing intestinal bacteria had a higher risk of progressing to type 1 diabetes than those with higher intestinal levels of these bacteria.[46] These results suggest that the activation of FFAR2 by intestinal SCFAs suppresses the development of type 1 diabetes in mice and humans and may do so by reducing the inflammation with injures pancreatic islet cells.[5] [45] [46] [47]

Inflammation

FFAR2 is expressed in various cells involved in the development of inflammatory responses such as neutrophils, monocytes, macrophages, dendritic cells, regulatory T cells, and T helper cells. FFAR2 often appears to be involved in suppressing these cells' pro-inflammatory actions and thereby the development of inflammation. For example: 1) compared to control mice, Ffar2 gene knockout mice developed more severe and unresolving inflammation in colitis, arthritis, peritonitis, and asthma models of inflammation; 2) germ-free mice, which lack intestinal SCFAs, likewise had severer disease in these colitis, arthritis, and asthma models; 3) in a dextran sulphate sodium-induced model of colitis, Ffar2 gene knockout mice developed more severe disease than control mice;[5] [48] 4) two studies found that normal mice but not Ffar2 gene knockout mice fed a prebiotic diet that produces higher intestinal levels of SCFAs were protected from developing allergic responses to food;[5] [49] 5) the latter study also showed that the prebiotic diet was fully protective in Ffar3 gene knockout mice[49] (allergic responses are a subtype of the inflammatory reactions[50]); and 6) studies in mice and humans suggest that FFAR2 is involved in suppressing the pancreatic islet inflammation underlying the development of type 1 diabetes (see previous section). Other studies, however, have reported that FFAR2 promotes inflammation.[51] Two studies found that FFAR2 gene knockdown mice had less severe disease in a dextran sulphate sodium-induce colitis model compared to control mice.[5] And, another study reported that the level of FFAR2 messenger RNA in circulating blood monocytes was elevated in humans with gout compared to those who did not have gout and rose further during flare-ups of their disease; the study suggested that FFAR2 is involved in triggering gout flare-ups.[52] Notably, a study based on the premise that FFAR2 promotes inflammation examined the effect of GLPG0974, a potent allosteric antagonist inhibitor of FFAR2,[14] [53] on patients with the inflammatory disease ulcerative colitis. The study progressed through phase I and II clinical studies that found the drug to be safe (i.e., non-toxic) but ineffective in reducing mild to moderate ulcerative colitis (further development of GLPG609 was terminated[54]).[14] While most studies suggest that FFAR2 suppresses human and mouse inflammation, further studies are needed to determine if and why FFAR2 promotes some types of inflammation.[5] [22] [51]

Adipogenesis, obesity, lipolysis, and ketogenesis

Angiogenesis and obesity

Studies have disagreed about the effects of FFAR2 on adipogenesis (i.e., formation of fat cells and fat tissue from precursor cells) as well as on the development of obesity.[5] [20] The inconsistencies reported by different research groups need to be resolved through further research in order to develop a clear picture of the actions that FFAR2 has on adipogenesis and obesity.[20] [51]

Lipolysis

Numerous studies have shown that SCFAs and FFAR2-activating drugs inhibit the lipolysis (i.e., enzymatic hydrolytic breakdown of cellular triglycerides into their component fatty acids and glycerol) in mice and their cultured fat cells.[20] For example: acetic and propionic acids inhibited lipolysis in mice (as defined by reducing their fatty acid blood levels) as well as their isolated cultured fat cells but did not do so in Ffar2 gene knockout mice or their isolated fat cells.[20] [55] There have been very few studies on FFAR2 and lipolysis in humans. Two studies reported that acetic acid suppressed fatty acid blood levels in humans but did not determine if this effect involved FFAR2.[55] [56] [57] Note that in a mouse model of severe stress, i.e., starvation, FFAR2 activation stimulated lipolysis (see next section on Ketogenesis and ketoacidosis).[16] FFAR2 appears to have very different effects on lipolysis in mice depending on their energy conditions and nutritional status.[5] While SCFAs and FFAR2 have been suggested to stimulate lipolysis in humans on low glucose diets (study described in section on Ketogenesis and ketoacidosis), the role of FFAR2 in this stimulation is unclear and requires further study.

Ketogenesis and ketoacidosis

Ketogenesis is a condition in which the liver releases ketone bodies, i.e., acetoacetic acid, beta-hydroxybutyric acid, and acetone, into the blood. This occurs when blood glucose levels are moderately low such as during sleep, fasting, dieting,[58] pregnancy, and the first 28 days after birth (i.e., the neonatal period); this form of ketogenesis is associated with modest elevations in the blood levels of the ketone bodies and, due to their increased release from adipose tissue, fatty acids.[59] The circulating ketone bodies and fatty acids serve as nutrients to sustain the functioning of critical organs such as muscle, heart, kidney and brain when blood glucose levels are too low to do so.[59] During serious stress conditions such as diabetic ketoacidosis and non-diabetic ketoacidosis due to excessive alcohol intake, medications, toxins, or starvation (see ketogenesis sections on each of these conditions), blood glucose levels are very low, blood ketone bodies and fatty acid levels are very high, and (due to the high blood levels of the ketone bodies and fatty acids) the blood is extremely acidic. This condition, a form of acidosis termed ketoacidosis, is life-threatening.[18] In addition to serving as a tissue nutrient and blood acidifier, one of the circulating ketone bodies appears to have another function: acetoacetic acid activates FFAR2. In a mouse model of starvation-induced ketogenesis: 1) the plasma concentration of acetoacetate was markedly increased in wild-type as well as Ffar2 gene knockout mice while at the same time plasma levels of acetic, propionic, and butyric acids were, as a consequence of starvation, far below those that would activate FFAR2; 2) plasma free fatty acid levels were elevated in wild type but not Ffar2 gene knockout mice; 3) fat tissue weight was significantly higher in Ffar2 gene knockout than wild-type mice; and 4) the lean body masses in the two groups of mice were comparable.[16] These results suggest that in mice the acetoacetic acid-induced activation of FFAR2 on fat cells stimulates lipolysis and thereby the rises in plasma fatty acid levels that occur in mild and severe ketoacidosis. Thus, FFAR2 appears to have a physiological role in mild but a pathological role in severe ketogenesis in mice.[16] [59] The acetoacetic acid-FFAR2-lipolysis linkage may occur in humans. Ketogenic diets i.e., low-carbohydrate diets, have been used to treat various neurological diseases. Individuals on these diets develop a mild form of ketogenesis consisting of moderately high blood levels of the ketone bodies and fatty acids. The increased fatty acid levels of individuals on these diets may be due to the stimulation of lipolysis by acetoacetic acid-induced activation of FFAR2 on their fat cells. High blood levels of beta-hydroxybutyric acid may activate hydroxycarboxylic acid receptor 2 on fat cells to similarly cause elevated fatty acid blood levels. Further studies are needed to support this role for FFAR2 in elevating fatty acid blood levels in humans on the ketogenic diet.[59]

Blood pressure regulation and vascular disease

The infusion of a FFAR2-activating SCFA, i.e. acetic, propionic, or butyric acid, into mice causes short-term falls in their blood pressure.[60] Similarly, patients undergoing hemodialysis that uses a hemodialysis solution containing acetic acid have an increased risk of becoming hypotensive compared to patients dialyzed with an acetic acid-free solution.[61] Furthermore, FFAR2 gene knockout mice developed perivascular fibrosis (which is an indicator of blood vessel disease[62]), higher end-diastolic blood pressures, and higher pulse pressures.[63] Finally, in the angiotensin II–infusion model of hypertension, mice had reduced levels of FFAR2 in their kidney tissues compared to control mice[60] and a study in humans reported that the levels of FFAR2 in the circulating white blood cells of hypertensive individuals was significantly lower than that in individuals with normal blood pressures.[64] These findings suggest that FFAR2 functions to reduce blood pressure as well as hypertension induced vascular disease in mice and humans and support further studies to examine these relationships.[60]

Cancer

Preliminary studies suggest that FFAR2 may be involved in some types of cancer.[65] 1) One study found that FFAR2 levels were elevated in human stomach and colorectal cancers although another study reported that FFAR2 levels were markedly deceased in human colorectal cancer. These results suggest that FFAR2 may promote the development and/or progression of human stomach cancer but its impact on human colorectal cancer requires further study.[18] 2) In a dextran sulfate sodium-induced model of inflammation-associated colon cancer, FFAR2 knockdown mice developed larger and more tumors than control mice.[66] This study suggests that FFAR2 inhibits the development and/or progression of inflammation-associated colon carcinoma in mice; its role in human inflammation-associated colorectal cancer (e.g., colorectal cancer developing in ulcerative colitis) has not been clarified.[5] 3) Compared to their normal lung tissues, the lung cancer tissues of 42 patients had lower levels of FFAR2 but not FFAR1, FFAR3, or FFAR4.[67] 4) Butyric acid inhibited the proliferation of and triggered apoptosis in cultured human A549 lung cancer cells;[68] further studies in A549 as well as H1299 human lung cancer cells found that propionic acid inhibited their stimulated migration, invasiveness, and colony growth in cell culture assays but did not do so in FFAR2 gene knockout A549 or H1299 cells.[67] These results suggest that FFAR2 may inhibit the development and/or progression of human lung cancer.[67] [68] (Studies have also reported that SCFAs inhibit the proliferation and caused apoptosis in cultured human breast cancer MCF-7[69] and human bladder cancer NaB cells[70] but neither study determined if their actions involved FFAR2.) Further studies are needed to confirm and broaden these preliminary findings and extend them to other types of cancer.[5] [65]

Nervous system

Microglia are the resident immune cells of the central nervous system (i.e., brain and spinal cord). They are key contributors to the development and maintenance of neural tissues[71] and mediate inflammatory responses to, e.g., bacterial invasion as well as the pathological inflammations which underlie many neurological diseases.[9] [10] Studies have reported that compared to control mice, germ-free mice (which lack SCFAs in their gastrointestinal tracts) have increased levels of immature microglia throughout their brains; SCFA supplementation normalized the microglial cell maturity. Furthermore, Ffar2 gene knockout mice likewise had increased levels of immature microglia throughout their brains. These studies suggest that FFAR2 is required for the maturation, and therefore functionality, of the microglia in mice.[5] [6] Since mouse microglial cells do not express FFAR2, the FFAR2-bearing cells responsible for the maturation and thereby functionality of the mouse's microglia are unclear.[5]

Studies have suggested that promoting the intestinal microbiota's production of SCFAs may suppress the development and/or progression of various human neurological diseases, particularly Parkinson's disease, Alzheimer's disease, neuromyelitis optica, and multiple sclerosis. This linkage is thought to involve at least in part SCFA-induced suppression of the inflammation associated with these diseases.[9] [72] With somewhat less evidence, other studies have suggested that SCFRs may suppress the development and/or progression of human autism, schizophrenia, vascular dementia, strokes, pathological anxiety and depression disorders,[9] [10] behavioral and social communication disorders,[73] and postoperative cognitive dysfunction.[74] Some of these studies mention the possibility that SCFA-induced activation of FFAR2 suppresses these diseases and disorders but give no evidence to support this. The studies often do suggest that the SCFAs act by various other mechanisms to achieve their neurological effects.[75] Furthermore, the role of SCFAs in humans with these diseases may be unclear. For example, two extensive reviews found that studies on the role of intestinal SCFAs in multiple sclerosis patients were inconclusive.[76] [77] There is a need to define the precise roles of SCFAs, FFAR2, and the other proposed causal factors in these neurological diseases and disorders.[9] [72]

Infections

Bacterial infections

Studies have shown that bacterial infections of the human urinary tract, vagina (i.e., bacterial vaginosis), gums (i.e., periodentitis), and abscesses in various tissues are associated with high concentrations of SCFAs, especially acetic acid, at the infection sites or, in urinary tract infections, the urine. These SCFAs may be made and released by the bacteria and/or host cells in the infected areas.[11] Several studies have suggested that SCFAs act through FFAR2 to suppress these infections. 1) Compared to control mice, Ffar2 gene knockout mice had more severe infections in models of Citrobacter rodentium, Klebsiella pneumoniae, Clostridioides difficile,[11] and Streptococcus pneumoniae bacterial infections.[78] 2) Injection of acetic acid into the peritoneum 1/2 hour before or 6 hours after injection of Staphylococcus aureus bacteria into the bloodstream of mice reduced signs of severe disease, the amount of body weight lost, and the numbers of bacteria recovered from the liver, spleen, and kidneys; these reductions did not occur in Fffar2 gene knockdown mice.[79] And, 3) higher circulating blood cell levels of FFAR2 messenger RNA were associated with higher survival rates in patients with sepsis, i.e., disseminated bacterial infections, compared to patients with lower levels of blood cell FFAR2 messenger RNA.[80] These studies suggest that FFAR2 reduces the severity of the cited bacterial infections in humans and mice and recommend further studies on the roles of FFAR2 in these and other bacterial infections.[11]

Viral infections

Mice pretreated for 4 weeks with diets that raised their intestinal SCFAs levels had reduced viral levels and pulmonary inflammation during the course of respiratory syncytial virus infection; these reductions did not occur in Ffar2 gene knockout mice or mice pretreated with antibiotics to reduce their intestines' SCFAs levels. Thus, SCFA activated FFAR2 appeared to reduce the severity of this viruses infection in mice.[11] Different results were found in a study examining influenza A virus's ability to enter and thereby infect human A549 lung cancer cells and mouse 264RAW .7 macrophages. Reduction of FFAR2 using gene knockdown methods reduced the virus's ability to enter into both cell types. Treating A549 cells with FFAR2 agonists, either 4-CMTB or compound 58, also inhibited the virus's entry into these cells. Analysis of this inhibition revealed that Influenza A virus entered these cells by binding to their surface membrane sialic acid receptors; this binding triggered endocytosis, i.e., internalization, of these cells' sialic acid receptors along with their attached viruses. A portion of the sialic acid receptor-bound virus also binds to and activates FFAR 2; this activation increased the endocytosis triggered by the virus's binding to the sialic acid receptors.[12] 4-CMTB and Compound 58 acted to block the ability of the sialic acid-bound virus to enhance endocytosis.[12] [14]

FFAR2-FFAR3 receptor heteromer

The FFAR2-FFAR3 protein dimer, also termed FFAR2-FFAR3 receptor heteromer, consists of single FFAR2 and FFAR3 proteins joined together. This dimer has been detected in monocytes isolated from human blood and macrophages that were differentiated from these monocytes (see monocyte differentiation into macrophages). Like other protein dimers, the FFAR2-FFAR3 protein dimer had activities that differed from each of its FFAR monomer proteins. However, FFAR2-FFAR3 dimers have not yet been associated with specific functions, clinical disorders, or clinical diseases.[81]

See also

Further reading

Notes and References

  1. Web site: Entrez Gene: FFAR1 free fatty acid receptor 1.
  2. Kalis M, Levéen P, Lyssenko V, Almgren P, Groop L, Cilio CM . Variants in the FFAR1 gene are associated with beta cell function . PLOS ONE . 2 . 11 . e1090 . November 2007 . 17987108 . 2042513 . 10.1371/journal.pone.0001090 . 2007PLoSO...2.1090K . free .
  3. Weis WI, Kobilka BK . The Molecular Basis of G Protein-Coupled Receptor Activation . Annual Review of Biochemistry . 87 . 897–919 . June 2018 . 29925258 . 6535337 . 10.1146/annurev-biochem-060614-033910 .
  4. Karmokar PF, Moniri NH . Oncogenic signaling of the free-fatty acid receptors FFA1 and FFA4 in human breast carcinoma cells . Biochemical Pharmacology . 206 . 115328 . December 2022 . 36309079 . 10.1016/j.bcp.2022.115328 . 253174629 .
  5. Kimura I, Ichimura A, Ohue-Kitano R, Igarashi M . Free Fatty Acid Receptors in Health and Disease . Physiological Reviews . 100 . 1 . 171–210 . January 2020 . 31487233 . 10.1152/physrev.00041.2018 . free .
  6. Ikeda T, Nishida A, Yamano M, Kimura I . Short-chain fatty acid receptors and gut microbiota as therapeutic targets in metabolic, immune, and neurological diseases . Pharmacology & Therapeutics . 239 . 108273 . November 2022 . 36057320 . 10.1016/j.pharmthera.2022.108273 . 251992642 . free .
  7. Kim YA, Keogh JB, Clifton PM . Probiotics, prebiotics, synbiotics and insulin sensitivity . Nutrition Research Reviews . 31 . 1 . 35–51 . June 2018 . 29037268 . 10.1017/S095442241700018X . free .
  8. Loona DP, Das B, Kaur R, Kumar R, Yadav AK . Free Fatty Acid Receptors (FFARs): Emerging Therapeutic Targets for the Management of Diabetes Mellitus . Current Medicinal Chemistry . 30 . 30 . 3404–3440 . 2023 . 36173072 . 10.2174/0929867329666220927113614 . 252598831 .
  9. Castillo-Álvarez F, Marzo-Sola ME . Role of the gut microbiota in the development of various neurological diseases . Neurologia . 37 . 6 . 492–498 . 2022 . 35779869 . 10.1016/j.nrleng.2019.03.026 . free .
  10. Mirzaei R, Bouzari B, Hosseini-Fard SR, Mazaheri M, Ahmadyousefi Y, Abdi M, Jalalifar S, Karimitabar Z, Teimoori A, Keyvani H, Zamani F, Yousefimashouf R, Karampoor S . Role of microbiota-derived short-chain fatty acids in nervous system disorders . Biomedicine & Pharmacotherapy . 139 . 111661 . July 2021 . 34243604 . 10.1016/j.biopha.2021.111661 . free .
  11. Schlatterer K, Peschel A, Kretschmer D . Short-Chain Fatty Acid and FFAR2 Activation - A New Option for Treating Infections? . Frontiers in Cellular and Infection Microbiology . 11 . 785833 . 2021 . 34926327 . 8674814 . 10.3389/fcimb.2021.785833 . free .
  12. Wang G, Jiang L, Wang J, Zhang J, Kong F, Li Q, Yan Y, Huang S, Zhao Y, Liang L, Li J, Sun N, Hu Y, Shi W, Deng G, Chen P, Liu L, Zeng X, Tian G, Bu Z, Chen H, Li C . The G Protein-Coupled Receptor FFAR2 Promotes Internalization during Influenza A Virus Entry . Journal of Virology . 94 . 2 . January 2020 . 31694949 . 6955252 . 10.1128/JVI.01707-19 .
  13. Priyadarshini M, Lednovich K, Xu K, Gough S, Wicksteed B, Layden BT . FFAR from the Gut Microbiome Crowd: SCFA Receptors in T1D Pathology . Metabolites . 11 . 5 . May 2021 . 302 . 34064625 . 8151283 . 10.3390/metabo11050302 . free .
  14. Milligan G, Barki N, Tobin AB . Chemogenetic Approaches to Explore the Functions of Free Fatty Acid Receptor 2 . Trends in Pharmacological Sciences . 42 . 3 . 191–202 . March 2021 . 33495026 . 10.1016/j.tips.2020.12.003 . 231712546 .
  15. Brown AJ, Goldsworthy SM, Barnes AA, Eilert MM, Tcheang L, Daniels D, Muir AI, Wigglesworth MJ, Kinghorn I, Fraser NJ, Pike NB, Strum JC, Steplewski KM, Murdock PR, Holder JC, Marshall FH, Szekeres PG, Wilson S, Ignar DM, Foord SM, Wise A, Dowell SJ . The Orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids . The Journal of Biological Chemistry . 278 . 13 . 11312–9 . March 2003 . 12496283 . 10.1074/jbc.M211609200 . free .
  16. Miyamoto J, Ohue-Kitano R, Mukouyama H, Nishida A, Watanabe K, Igarashi M, Irie J, Tsujimoto G, Satoh-Asahara N, Itoh H, Kimura I . Ketone body receptor GPR43 regulates lipid metabolism under ketogenic conditions . Proceedings of the National Academy of Sciences of the United States of America . 116 . 47 . 23813–23821 . November 2019 . 31685604 . 6876247 . 10.1073/pnas.1912573116 . 2019PNAS..11623813M . free .
  17. Lind S, Holdfeldt A, Mårtensson J, Granberg KL, Forsman H, Dahlgren C . Multiple ligand recognition sites in free fatty acid receptor 2 (FFA2R) direct distinct neutrophil activation patterns . Biochemical Pharmacology . 193 . 114762 . November 2021 . 34499871 . 10.1016/j.bcp.2021.114762 . 237471881 . free .
  18. Carretta MD, Quiroga J, López R, Hidalgo MA, Burgos RA . Participation of Short-Chain Fatty Acids and Their Receptors in Gut Inflammation and Colon Cancer . Frontiers in Physiology . 12 . 662739 . 2021 . 33897470 . 8060628 . 10.3389/fphys.2021.662739 . free .
  19. Hansen AH, Sergeev E, Bolognini D, Sprenger RR, Ekberg JH, Ejsing CS, McKenzie CJ, Rexen Ulven E, Milligan G, Ulven T . Discovery of a Potent Thiazolidine Free Fatty Acid Receptor 2 Agonist with Favorable Pharmacokinetic Properties . Journal of Medicinal Chemistry . 61 . 21 . 9534–9550 . November 2018 . 30247908 . 10.1021/acs.jmedchem.8b00855 . free .
  20. Al Mahri S, Malik SS, Al Ibrahim M, Haji E, Dairi G, Mohammad S . Free Fatty Acid Receptors (FFARs) in Adipose: Physiological Role and Therapeutic Outlook . Cells . 11 . 4 . February 2022 . 750 . 35203397 . 8870169 . 10.3390/cells11040750 . free .
  21. Iwasaki K, Harada N, Sasaki K, Yamane S, Iida K, Suzuki K, Hamasaki A, Nasteska D, Shibue K, Joo E, Harada T, Hashimoto T, Asakawa Y, Hirasawa A, Inagaki N . Free fatty acid receptor GPR120 is highly expressed in enteroendocrine K cells of the upper small intestine and has a critical role in GIP secretion after fat ingestion . Endocrinology . 156 . 3 . 837–46 . March 2015 . 25535828 . 10.1210/en.2014-1653 . 2433/215430 . free .
  22. Mishra SP, Karunakar P, Taraphder S, Yadav H . Free Fatty Acid Receptors 2 and 3 as Microbial Metabolite Sensors to Shape Host Health: Pharmacophysiological View . Biomedicines . 8 . 6 . June 2020 . 154 . 32521775 . 7344995 . 10.3390/biomedicines8060154 . free .
  23. Jorsal T, Rhee NA, Pedersen J, Wahlgren CD, Mortensen B, Jepsen SL, Jelsing J, Dalbøge LS, Vilmann P, Hassan H, Hendel JW, Poulsen SS, Holst JJ, Vilsbøll T, Knop FK . Enteroendocrine K and L cells in healthy and type 2 diabetic individuals . Diabetologia . 61 . 2 . 284–294 . February 2018 . 28956082 . 10.1007/s00125-017-4450-9 . free .
  24. Lorza-Gil E, Kaiser G, Rexen Ulven E, König GM, Gerst F, Oquendo MB, Birkenfeld AL, Häring HU, Kostenis E, Ulven T, Ullrich S . FFA2-, but not FFA3-agonists inhibit GSIS of human pseudoislets: a comparative study with mouse islets and rat INS-1E cells . Scientific Reports . 10 . 1 . 16497 . October 2020 . 33020504 . 7536384 . 10.1038/s41598-020-73467-5 .
  25. Lind S, Holdfeldt A, Mårtensson J, Sundqvist M, Kenakin TP, Björkman L, Forsman H, Dahlgren C . Interdependent allosteric free fatty acid receptor 2 modulators synergistically induce functional selective activation and desensitization in neutrophils . Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 1867 . 6 . 118689 . June 2020 . 32092308 . 10.1016/j.bbamcr.2020.118689 . free .
  26. Lavoie S, Chun E, Bae S, Brennan CA, Gallini Comeau CA, Lang JK, Michaud M, Hoveyda HR, Fraser GL, Fuller MH, Layden BT, Glickman JN, Garrett WS . Expression of Free Fatty Acid Receptor 2 by Dendritic Cells Prevents Their Expression of Interleukin 27 and Is Required for Maintenance of Mucosal Barrier and Immune Response Against Colorectal Tumors in Mice . Gastroenterology . 158 . 5 . 1359–1372.e9 . April 2020 . 31917258 . 7291292 . 10.1053/j.gastro.2019.12.027 .
  27. Xiu W, Chen Q, Wang Z, Wang J, Zhou Z . Microbiota-derived short chain fatty acid promotion of Amphiregulin expression by dendritic cells is regulated by GPR43 and Blimp-1 . Biochemical and Biophysical Research Communications . 533 . 3 . 282–288 . December 2020 . 32958255 . 10.1016/j.bbrc.2020.09.027 . 221843901 .
  28. Nilsson NE, Kotarsky K, Owman C, Olde B . Identification of a free fatty acid receptor, FFA2R, expressed on leukocytes and activated by short-chain fatty acids . Biochemical and Biophysical Research Communications . 303 . 4 . 1047–52 . April 2003 . 12684041 . 10.1016/S0006-291X(03)00488-1 .
  29. Pluznick JL, Protzko RJ, Gevorgyan H, Peterlin Z, Sipos A, Han J, Brunet I, Wan LX, Rey F, Wang T, Firestein SJ, Yanagisawa M, Gordon JI, Eichmann A, Peti-Peterdi J, Caplan MJ . Olfactory receptor responding to gut microbiota-derived signals plays a role in renin secretion and blood pressure regulation . Proceedings of the National Academy of Sciences of the United States of America . 110 . 11 . 4410–5 . March 2013 . 23401498 . 3600440 . 10.1073/pnas.1215927110 . 2013PNAS..110.4410P . free .
  30. Nauck MA, Meier JJ . Incretin hormones: Their role in health and disease . Diabetes, Obesity & Metabolism . 20 . Suppl 1. 5–21 . February 2018 . 29364588 . 10.1111/dom.13129 . free .
  31. de Vos WM, Tilg H, Van Hul M, Cani PD . Gut microbiome and health: mechanistic insights . Gut . 71 . 5 . 1020–1032 . May 2022 . 35105664 . 8995832 . 10.1136/gutjnl-2021-326789 .
  32. Mazhar M, Zhu Y, Qin L . The Interplay of Dietary Fibers and Intestinal Microbiota Affects Type 2 Diabetes by Generating Short-Chain Fatty Acids . Foods . 12 . 5 . February 2023 . 1023 . 36900540 . 10001013 . 10.3390/foods12051023 . free .
  33. Kasarello K, Cudnoch-Jedrzejewska A, Czarzasta K . Communication of gut microbiota and brain via immune and neuroendocrine signaling . Frontiers in Microbiology . 14 . 1118529 . 2023 . 36760508 . 9907780 . 10.3389/fmicb.2023.1118529 . free .
  34. Bermudez LE, Young LS . Phagocytosis and intracellular killing of Mycobacterium avium complex by human and murine macrophages . Brazilian Journal of Medical and Biological Research = Revista Brasileira de Pesquisas Medicas e Biologicas . 20 . 2 . 191–201 . 1987 . 3690054 .
  35. Ghislain J, Poitout V . Targeting lipid GPCRs to treat type 2 diabetes mellitus - progress and challenges . Nature Reviews. Endocrinology . 17 . 3 . 162–175 . March 2021 . 33495605 . 10.1038/s41574-020-00459-w . 231695737 .
  36. Müller TD, Finan B, Bloom SR, D'Alessio D, Drucker DJ, Flatt PR, Fritsche A, Gribble F, Grill HJ, Habener JF, Holst JJ, Langhans W, Meier JJ, Nauck MA, Perez-Tilve D, Pocai A, Reimann F, Sandoval DA, Schwartz TW, Seeley RJ, Stemmer K, Tang-Christensen M, Woods SC, DiMarchi RD, Tschöp MH . Glucagon-like peptide 1 (GLP-1) . Molecular Metabolism . 30 . 72–130 . December 2019 . 31767182 . 6812410 . 10.1016/j.molmet.2019.09.010 .
  37. Holst JJ, Gasbjerg LS, Rosenkilde MM . The Role of Incretins on Insulin Function and Glucose Homeostasis . Endocrinology . 162 . 7 . July 2021 . 33782700 . 8168943 . 10.1210/endocr/bqab065 .
  38. Tan M, Lamendola C, Luong R, McLaughlin T, Craig C . Safety, efficacy and pharmacokinetics of repeat subcutaneous dosing of avexitide (exendin 9-39) for treatment of post-bariatric hypoglycaemia . Diabetes, Obesity & Metabolism . 22 . 8 . 1406–1416 . August 2020 . 32250530 . 10.1111/dom.14048 . 214809891 .
  39. Lynggaard MB, Gasbjerg LS, Christensen MB, Knop FK . GIP(3-30)NH2 - a tool for the study of GIP physiology . Current Opinion in Pharmacology . 55 . 31–40 . December 2020 . 33053504 . 10.1016/j.coph.2020.08.011 . 222420789 .
  40. Gasbjerg LS, Helsted MM, Hartmann B, Jensen MH, Gabe BN, Sparre-Ulrich AH, Veedfald S, Stensen S, Lanng AR, Bergmann NC, Christensen MB, Vilsbøll T, Holst JJ, Rosenkilde MM, Knop FK . Separate and Combined Glucometabolic Effects of Endogenous Glucose-Dependent Insulinotropic Polypeptide and Glucagon-like Peptide 1 in Healthy Individuals . Diabetes . 68 . 5 . 906–917 . May 2019 . 30626611 . 10.2337/db18-1123 . free .
  41. Scott LJ . Dulaglutide: A Review in Type 2 Diabetes . Drugs . 80 . 2 . 197–208 . February 2020 . 32002850 . 10.1007/s40265-020-01260-9 . 210954338 .
  42. Bradley CL, McMillin SM, Hwang AY, Sherrill CH . Tirzepatide, the Newest Medication for Type 2 Diabetes: A Review of the Literature and Implications for Clinical Practice . The Annals of Pharmacotherapy . 57 . 7 . 822–836 . July 2023 . 36367094 . 10.1177/10600280221134127 . 253457679 .
  43. Villa SR, Priyadarshini M, Fuller MH, Bhardwaj T, Brodsky MR, Angueira AR, Mosser RE, Carboneau BA, Tersey SA, Mancebo H, Gilchrist A, Mirmira RG, Gannon M, Layden BT . Loss of Free Fatty Acid Receptor 2 leads to impaired islet mass and beta cell survival . Scientific Reports . 6 . 28159 . June 2016 . 27324831 . 4914960 . 10.1038/srep28159 . 2016NatSR...628159V .
  44. McNelis JC, Lee YS, Mayoral R, van der Kant R, Johnson AM, Wollam J, Olefsky JM . GPR43 Potentiates β-Cell Function in Obesity . Diabetes . 64 . 9 . 3203–17 . September 2015 . 26023106 . 4542437 . 10.2337/db14-1938 .
  45. Mariño E, Richards JL, McLeod KH, Stanley D, Yap YA, Knight J, McKenzie C, Kranich J, Oliveira AC, Rossello FJ, Krishnamurthy B, Nefzger CM, Macia L, Thorburn A, Baxter AG, Morahan G, Wong LH, Polo JM, Moore RJ, Lockett TJ, Clarke JM, Topping DL, Harrison LC, Mackay CR . Gut microbial metabolites limit the frequency of autoimmune T cells and protect against type 1 diabetes . Nature Immunology . 18 . 5 . 552–562 . May 2017 . 28346408 . 10.1038/ni.3713 . 30078908 .
  46. Harbison JE, Roth-Schulze AJ, Giles LC, Tran CD, Ngui KM, Penno MA, Thomson RL, Wentworth JM, Colman PG, Craig ME, Morahan G, Papenfuss AT, Barry SC, Harrison LC, Couper JJ . Gut microbiome dysbiosis and increased intestinal permeability in children with islet autoimmunity and type 1 diabetes: A prospective cohort study . Pediatric Diabetes . 20 . 5 . 574–583 . August 2019 . 31081243 . 10.1111/pedi.12865 . 11343/285878 . 153308576 . free .
  47. Simon MC, Reinbeck AL, Wessel C, Heindirk J, Jelenik T, Kaul K, Arreguin-Cano J, Strom A, Blaut M, Bäckhed F, Burkart V, Roden M . Distinct alterations of gut morphology and microbiota characterize accelerated diabetes onset in nonobese diabetic mice . The Journal of Biological Chemistry . 295 . 4 . 969–980 . January 2020 . 31822562 . 6983849 . 10.1074/jbc.RA119.010816 . free .
  48. Maslowski KM, Vieira AT, Ng A, Kranich J, Sierro F, Yu D, Schilter HC, Rolph MS, Mackay F, Artis D, Xavier RJ, Teixeira MM, Mackay CR . Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43 . Nature . 461 . 7268 . 1282–6 . October 2009 . 19865172 . 3256734 . 10.1038/nature08530 . 2009Natur.461.1282M .
  49. Tan J, McKenzie C, Vuillermin PJ, Goverse G, Vinuesa CG, Mebius RE, Macia L, Mackay CR . Dietary Fiber and Bacterial SCFA Enhance Oral Tolerance and Protect against Food Allergy through Diverse Cellular Pathways . Cell Reports . 15 . 12 . 2809–24 . June 2016 . 27332875 . 10.1016/j.celrep.2016.05.047 . 1885/153817 . free .
  50. Han X, Krempski JW, Nadeau K . Advances and novel developments in mechanisms of allergic inflammation . Allergy . 75 . 12 . 3100–3111 . December 2020 . 33068299 . 10.1111/all.14632 . free .
  51. Ang Z, Ding JL . GPR41 and GPR43 in Obesity and Inflammation - Protective or Causative? . Frontiers in Immunology . 7 . 28 . 2016 . 26870043 . 4734206 . 10.3389/fimmu.2016.00028 . free .
  52. Orji OC, López-Domínguez MB, Sandoval-Plata G, Guetta-Baranes T, Valdes AM, Doherty M, Morgan K, Abhishek A . Upregulated expression of FFAR2 and SOC3 genes is associated with gout . Rheumatology . 62 . 2 . 977–983 . February 2023 . 35731142 . 9891400 . 10.1093/rheumatology/keac360 .
  53. Namour F, Galien R, Van Kaem T, Van der Aa A, Vanhoutte F, Beetens J, Van't Klooster G . Safety, pharmacokinetics and pharmacodynamics of GLPG0974, a potent and selective FFA2 antagonist, in healthy male subjects . British Journal of Clinical Pharmacology . 82 . 1 . 139–48 . July 2016 . 26852904 . 4917808 . 10.1111/bcp.12900 .
  54. Sergeev E, Hansen AH, Bolognini D, Kawakami K, Kishi T, Aoki J, Ulven T, Inoue A, Hudson BD, Milligan G . A single extracellular amino acid in Free Fatty Acid Receptor 2 defines antagonist species selectivity and G protein selection bias . Scientific Reports . 7 . 1 . 13741 . October 2017 . 29061999 . 5653858 . 10.1038/s41598-017-14096-3 . 2017NatSR...713741S .
  55. Ge H, Li X, Weiszmann J, Wang P, Baribault H, Chen JL, Tian H, Li Y . Activation of G protein-coupled receptor 43 in adipocytes leads to inhibition of lipolysis and suppression of plasma free fatty acids . Endocrinology . 149 . 9 . 4519–26 . September 2008 . 18499755 . 10.1210/en.2008-0059 . free .
  56. Suokas A, Kupari M, Heikkilä J, Lindros K, Ylikahri R . Acute cardiovascular and metabolic effects of acetate in men . Alcoholism: Clinical and Experimental Research . 12 . 1 . 52–8 . February 1988 . 3279860 . 10.1111/j.1530-0277.1988.tb00132.x .
  57. Laurent C, Simoneau C, Marks L, Braschi S, Champ M, Charbonnel B, Krempf M . Effect of acetate and propionate on fasting hepatic glucose production in humans . European Journal of Clinical Nutrition . 49 . 7 . 484–91 . July 1995 . 7588498 .
  58. Aalling . Nadia Nielsen . Nedergaard . Maiken . DiNuzzo . Mauro . Cerebral Metabolic Changes During Sleep. . Current Neurology and Neuroscience Reports . July 16, 2018 . 18 . 9 . 57 . 10.1007/s11910-018-0868-9 . 30014344 . 6688614 .
  59. Spigoni V, Cinquegrani G, Iannozzi NT, Frigeri G, Maggiolo G, Maggi M, Parello V, Dei Cas A . Activation of G protein-coupled receptors by ketone bodies: Clinical implication of the ketogenic diet in metabolic disorders . Frontiers in Endocrinology . 13 . 972890 . 2022 . 36339405 . 9631778 . 10.3389/fendo.2022.972890 . free .
  60. Xu J, Moore BN, Pluznick JL . Short-Chain Fatty Acid Receptors and Blood Pressure Regulation: Council on Hypertension Mid-Career Award for Research Excellence 2021 . Hypertension . 79 . 10 . 2127–2137 . October 2022 . 35912645 . 10.1161/HYPERTENSIONAHA.122.18558 . 9458621 . 251222823 .
  61. de Sequera P, Pérez-García R, Molina M, Álvarez-Fernández G, Muñoz-González RI, Mérida E, Camba MJ, Blázquez LA, Alcaide MP, Echarri R . Advantages of the use of citrate over acetate as a stabilizer in hemodialysis fluid: A randomized ABC-treat study . Nefrologia . 42 . 3 . 327–337 . 2022 . 36210622 . 10.1016/j.nefroe.2021.12.003 . free .
  62. Zhuang R, Chen J, Cheng HS, Assa C, Jamaiyar A, Pandey AK, Pérez-Cremades D, Zhang B, Tzani A, Khyrul Wara A, Plutzky J, Barrera V, Bhetariya P, Mitchell RN, Liu Z, Feinberg MW . Perivascular Fibrosis Is Mediated by a KLF10-IL-9 Signaling Axis in CD4+ T Cells . Circulation Research . 130 . 11 . 1662–1681 . May 2022 . 35440172 . 9149118 . 10.1161/CIRCRESAHA.121.320420 .
  63. Kaye DM, Shihata WA, Jama HA, Tsyganov K, Ziemann M, Kiriazis H, Horlock D, Vijay A, Giam B, Vinh A, Johnson C, Fiedler A, Donner D, Snelson M, Coughlan MT, Phillips S, Du XJ, El-Osta A, Drummond G, Lambert GW, Spector TD, Valdes AM, Mackay CR, Marques FZ . Deficiency of Prebiotic Fiber and Insufficient Signaling Through Gut Metabolite-Sensing Receptors Leads to Cardiovascular Disease . Circulation . 141 . 17 . 1393–1403 . April 2020 . 32093510 . 10.1161/CIRCULATIONAHA.119.043081 . 211476145 . free . 10536/DRO/DU:30135388 . free .
  64. Nakai M, Ribeiro RV, Stevens BR, Gill P, Muralitharan RR, Yiallourou S, Muir J, Carrington M, Head GA, Kaye DM, Marques FZ . Essential Hypertension Is Associated With Changes in Gut Microbial Metabolic Pathways: A Multisite Analysis of Ambulatory Blood Pressure . Hypertension . 78 . 3 . 804–815 . September 2021 . 34333988 . 10.1161/HYPERTENSIONAHA.121.17288 . free .
  65. Mirzaei R, Afaghi A, Babakhani S, Sohrabi MR, Hosseini-Fard SR, Babolhavaeji K, Khani Ali Akbari S, Yousefimashouf R, Karampoor S . Role of microbiota-derived short-chain fatty acids in cancer development and prevention . Biomedicine & Pharmacotherapy . 139 . 111619 . July 2021 . 33906079 . 10.1016/j.biopha.2021.111619 . free .
  66. Pan P, Oshima K, Huang YW, Agle KA, Drobyski WR, Chen X, Zhang J, Yearsley MM, Yu J, Wang LS . Loss of FFAR2 promotes colon cancer by epigenetic dysregulation of inflammation suppressors . International Journal of Cancer . 143 . 4 . 886–896 . August 2018 . 29524208 . 6041131 . 10.1002/ijc.31366 .
  67. Kim MJ, Kim JY, Shin JH, Kang Y, Lee JS, Son J, Jeong SK, Kim D, Kim DH, Chun E, Lee KY . FFAR2 antagonizes TLR2- and TLR3-induced lung cancer progression via the inhibition of AMPK-TAK1 signaling axis for the activation of NF-κB . Cell & Bioscience . 13 . 1 . 102 . June 2023 . 37287005 . 10249240 . 10.1186/s13578-023-01038-y . free .
  68. Xiao X, Xu Y, Chen H . Sodium butyrate-activated TRAF6-TXNIP pathway affects A549 cells proliferation and migration . Cancer Medicine . 9 . 10 . 3477–3488 . May 2020 . 31578830 . 7221305 . 10.1002/cam4.2564 .
  69. Semaan J, El-Hakim S, Ibrahim JN, Safi R, Elnar AA, El Boustany C . Comparative effect of sodium butyrate and sodium propionate on proliferation, cell cycle and apoptosis in human breast cancer cells MCF-7 . Breast Cancer (Tokyo, Japan) . 27 . 4 . 696–705 . July 2020 . 32095987 . 10.1007/s12282-020-01063-6 . 211265423 .
  70. Wang F, Wu H, Fan M, Yu R, Zhang Y, Liu J, Zhou X, Cai Y, Huang S, Hu Z, Jin X . Sodium butyrate inhibits migration and induces AMPK-mTOR pathway-dependent autophagy and ROS-mediated apoptosis via the miR-139-5p/Bmi-1 axis in human bladder cancer cells . FASEB Journal . 34 . 3 . 4266–4282 . March 2020 . 31957111 . 10.1096/fj.201902626R . free . 210832147 .
  71. Borst K, Dumas AA, Prinz M . Microglia: Immune and non-immune functions . Immunity . 54 . 10 . 2194–2208 . October 2021 . 34644556 . 10.1016/j.immuni.2021.09.014 . 238858388 .
  72. Sun Y, Zhang H, Zhang X, Wang W, Chen Y, Cai Z, Wang Q, Wang J, Shi Y . Promotion of astrocyte-neuron glutamate-glutamine shuttle by SCFA contributes to the alleviation of Alzheimer's disease . Redox Biology . 62 . 102690 . June 2023 . 37018970 . 10122027 . 10.1016/j.redox.2023.102690 .
  73. Stilling RM, van de Wouw M, Clarke G, Stanton C, Dinan TG, Cryan JF . The neuropharmacology of butyrate: The bread and butter of the microbiota-gut-brain axis? . Neurochemistry International . 99 . 110–132 . October 2016 . 27346602 . 10.1016/j.neuint.2016.06.011 . 207124576 .
  74. Luo A, Li S, Wang X, Xie Z, Li S, Hua D . Cefazolin Improves Anesthesia and Surgery-Induced Cognitive Impairments by Modulating Blood-Brain Barrier Function, Gut Bacteria and Short Chain Fatty Acids . Frontiers in Aging Neuroscience . 13 . 748637 . 2021 . 34720997 . 8548472 . 10.3389/fnagi.2021.748637 . free .
  75. Eicher TP, Mohajeri MH . Overlapping Mechanisms of Action of Brain-Active Bacteria and Bacterial Metabolites in the Pathogenesis of Common Brain Diseases . Nutrients . 14 . 13 . June 2022 . 2661 . 35807841 . 9267981 . 10.3390/nu14132661 . free .
  76. Valburg C, Sonti A, Stern JN, Najjar S, Harel A . Dietary factors in experimental autoimmune encephalomyelitis and multiple sclerosis: A comprehensive review . Multiple Sclerosis (Houndmills, Basingstoke, England) . 27 . 4 . 494–502 . April 2021 . 32406797 . 10.1177/1352458520923955 . 218633615 .
  77. Ghezzi L, Cantoni C, Pinget GV, Zhou Y, Piccio L . Targeting the gut to treat multiple sclerosis . The Journal of Clinical Investigation . 131 . 13 . July 2021 . 34196310 . 8245171 . 10.1172/JCI143774 .
  78. Galvão I, Tavares LP, Corrêa RO, Fachi JL, Rocha VM, Rungue M, Garcia CC, Cassali G, Ferreira CM, Martins FS, Oliveira SC, Mackay CR, Teixeira MM, Vinolo MA, Vieira AT . The Metabolic Sensor GPR43 Receptor Plays a Role in the Control of Klebsiella pneumoniae Infection in the Lung . Frontiers in Immunology . 9 . 142 . 2018 . 29515566 . 5826235 . 10.3389/fimmu.2018.00142 . free .
  79. Schlatterer K, Beck C, Schoppmeier U, Peschel A, Kretschmer D . Acetate sensing by GPR43 alarms neutrophils and protects from severe sepsis . Communications Biology . 4 . 1 . 928 . July 2021 . 34330996 . 8324776 . 10.1038/s42003-021-02427-0 .
  80. Carr ZJ, Van De Louw A, Fehr G, Li JD, Kunselman A, Ruiz-Velasco V . Increased whole blood FFA2/GPR43 receptor expression is associated with increased 30-day survival in patients with sepsis . BMC Research Notes . 11 . 1 . 41 . January 2018 . 29338778 . 5771199 . 10.1186/s13104-018-3165-4 . free .
  81. Ang Z, Xiong D, Wu M, Ding JL . FFAR2-FFAR3 receptor heteromerization modulates short-chain fatty acid sensing . FASEB Journal . 32 . 1 . 289–303 . January 2018 . 28883043 . 5731126 . 10.1096/fj.201700252RR . free .