Prostasomes Explained

Prostasomes are extracellular vesicles (40-500 nm in diameter) secreted by the prostate gland epithelial cells into seminal fluid.[1] They possess an unusual lipid composition and a tight and highly ordered structure of their lipid bilayer membrane, resembling that of lipid raft domains. Prostasomes appear to improve sperm motility and protect against attacks from the female immune defense during the passage to the egg.[2]

The name prostasomes was coined in the early 1980s by combining the terms "prosta"=prostate and "soma" (Greek for "body"). Around this time, the first functional studies of prostasomes were also performed.[3] [4] [5] [6] [7]

Cancerous prostate cells and prostate cells with low differentiation continue to produce and secrete prostasomes.[8] Possibly, the high incidence of prostate cancer in elderly men could be due to the immunomodulatory properties of prostasomes, protecting the cancer from attack by the immune system.

Fusion of prostasomes with the sperm plasma membrane is required for regulation of different aspects of sperm function, such as motility and capacitation.[9] Prostasomes have also been implicated in the interaction between prostatic cancer cells and their microenvironment.[10]

Immune regulating proteins found in prostasomes include: amino-peptidase N (CD13); dipeptidyl-peptidase IV (CD26); enkephalinase (neutral endopeptidase, CD10); angiotensin converting enzyme (ACE, CD143); tissue factor TF (CD142, thromboplastin); decay accelerating factor (CD55); protectin (CD59, inhibitor of MAC) and complement regulatory membrane cofactor protein (CD46).[11] [12] [13] Prostasomes also contain high levels of the divalent cations: Zn2+, Ca2+ and Mg2+.

Historical background of prostasome research

Year
1977-78 An ATPase activity in seminal plasma indicated an occurrence of membrane-surrounded extracellular vesicles [14] [15] [16]
1981The first association between prostasomes and fertility was reported [17]
1983The first electron microscopic pictures of prostasomes inside storage vesicles (multivesicular bodies) in cytoplasm of prostate epithelial cells and their extracellular release into lumen of the prostate [18] [19]
1984The role of prostasomes in infertility and prostate cancer was investigated [20]
1986-89Studies on ATPases on the prostasomal surface [21] [22] [23] [24]
1989The prostasomal membrane was found to have a much higher cholesterol/phospholipid ratio than ordinary cellular membranes [25]
1990Nucleic acid was found to be associated with prostasomes.[26] An interaction between prostasomes and sperm was shown [27]
1991-94Prostasomes and their role in immunosuppression were investigated in several articles.[28] [29] [30] Granulophysin (CD63) was suggested as a marker for prostasomes[31]
1995-2001Monoclonal antibodies against prostasomes were produced and several studies involving these antibodies were performed [32] [33] [34] as well as prostasome-sperm interaction studies.[35] [36] [37] [38] [39] [40] Prostasomes were discovered in prostatic fluid of other species.[41] [42] Prostatic cancer cell lines were found to produce prostasomes.[43] [44] Prostasomes displayed anti-bacterial activity[45]
2001Autoantibodies against prostasomes were evaluated as biomarkers for prostate cancer [46]
2003The first comprehensive shotgun proteomics of the prostasome proteome [47] and it has been followed by two others [48] [49]
2005Haemostasis coupled to prostasomes and the prostasomal membrane in fertility and in cancer [50] [51] [52]
2009-Investigation of prostasomal DNA.[53] [54] [55] DNA was found in both non-malignant prostasomes as well as in prostate cancer (PC3) cell derived prostasomes/exosomes
2009-Prostasomes as a serum biomarker of prostate cancer [56]
2015Lipid rafts purified from prostasome membranes [57]

See also

Notes and References

  1. Ronquist G, Brody I . The prostasome: its secretion and function in man . Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes . 822 . 2 . 203–18 . September 1985 . 2992593 . 10.1016/0304-4157(85)90008-5 .
  2. Burden HP, Holmes CH, Persad R, Whittington K . Prostasomes--their effects on human male reproduction and fertility . Human Reproduction Update . 12 . 3 . 283–92 . 2006 . 16373403 . 10.1093/humupd/dmi052 . free .
  3. Stegmayr B, Brody I, Ronquist G . A biochemical and ultrastructural study on the endogenous protein kinase activity of secretory granule membranes of prostatic origin in human seminal plasma . Journal of Ultrastructure Research . 78 . 2 . 206–14 . February 1982 . 6283103 . 10.1016/s0022-5320(82)80024-5 .
  4. Stegmayr B, Ronquist G . Stimulation of sperm progressive motility by organelles in human seminal plasma . Scandinavian Journal of Urology and Nephrology . 16 . 2 . 85–90 . 1982 . 7123173 . 10.3109/00365598209179734 . 8 .
  5. Stegmayr B, Ronquist G . Distribution of cyclic AMP in human seminal plasma and its relation to sperm progressive motility . Scandinavian Journal of Urology and Nephrology . 16 . 2 . 91–5 . 1982 . 6289426 . 10.3109/00365598209179735 . 9 .
  6. Stegmayr B, Ronquist G . Promotive effect on human sperm progressive motility by prostasomes . Urological Research . 10 . 5 . 253–7 . 1982 . 6219486 . 10.1007/bf00255932 . 26574697 . 10 .
  7. Stegmayr B, Berggren PO, Ronquist G, Hellman B . Calcium, magnesium, and zinc contents in organelles of prostatic origin in human seminal plasma . Scandinavian Journal of Urology and Nephrology . 16 . 3 . 199–203 . 1982 . 6219456 . 10.3109/00365598209179753 . 11 .
  8. Ronquist G, Nilsson BO . The Janus-faced nature of prostasomes: their pluripotency favours the normal reproductive process and malignant prostate growth . Prostate Cancer and Prostatic Diseases . 7 . 1 . 21–31 . 2004 . 14999234 . 10.1038/sj.pcan.4500684 .
  9. Aalberts. Marian. Stout. Tom A E. Stoorvogel. Willem. January 2014. Prostasomes: extracellular vesicles from the prostate. Reproduction. 147. 1. R1–R14. 10.1530/REP-13-0358. 24149515. 1470-1626. free.
  10. Carlsson. L.. Lennartsson. L.. Nilsson. B.O.. Nilsson. S.. Ronquist. G.. 2000. Growth - Inhibitory Effect of Prostasomes on Prostatic Cancer Cell Lines in Culture. European Urology. 38. 4. 468–474. 10.1159/000020326. 11025388. 46871454.
  11. Book: Ronquist G, Jin M, Schrimpf S, Nilsson BO . Motta PM . 1997 . Prostasomes and human reproduction . Microscopy of Reproduction and Development: A Dynamic Approach . 213–219 . Antonio Delfino Editore . Rome .
  12. Book: Ronquist G, Carlsson L, Larsson A, Nilsson BO . Prostasomes . 1–9 . Nilsson BO, Ronquist G . Prostasomes: proceedings from a symposium held at the Wenner-Gren Centre, Stockholm, in June 2001 . 2002 . Portland . London . 978-1-85578-151-1 .
  13. Stewart AB, Anderson W, Delves G, Lwaleed BA, Birch B, Cooper A . Prostasomes: a role in prostatic disease? . BJU International . 94 . 7 . 985–9 . November 2004 . 15541114 . 10.1111/j.1464-410X.2004.05091.x . 19310896 .
  14. Ronquist G, Hedström M . Restoration of detergent-inactivated adenosine triphosphatase activity of human prostatic fluid with concanavalin A . Biochimica et Biophysica Acta (BBA) - Enzymology . 483 . 2 . 483–6 . August 1977 . 142513 . 10.1016/0005-2744(77)90078-x . 2 .
  15. Ronquist G, Brody I, Gottfries A, Stegmayr B . An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid: part I . Andrologia . 10 . 4 . 261–72 . 1978 . 152589 . 10.1111/j.1439-0272.1978.tb03030.x . 27340699 . 9 . free .
  16. Ronquist G, Brody I, Gottfries A, Stegmayr B . An Mg2+ and Ca2+-stimulated adenosine triphosphatase in human prostatic fluid--part II . Andrologia . 10 . 6 . 427–33 . 1978 . 153718 . 10.1111/j.1439-0272.1978.tb03064.x . 46519228 . 8 . free .
  17. Brody I, Ronquist G, Gottfries A, Stegmayr B . Abnormal deficiency of both Mg2+ and Ca2+-dependent adenosine triphosphatase and secretory granules and vesicles in human seminal plasma . Scandinavian Journal of Urology and Nephrology . 15 . 2 . 85–90 . 1981 . 6120566 . 10.3109/00365598109179581 . 6 .
  18. Ronquist G, Stegmayr B, Brody I, Gottfries A . [Prostasomes--a newly discovered organelle that increases sperm motility] . Läkartidningen . 80 . 9 . 810–3 . March 1983 . 6865591 . 5 .
  19. Brody I, Ronquist G, Gottfries A . Ultrastructural localization of the prostasome - an organelle in human seminal plasma . Upsala Journal of Medical Sciences . 88 . 2 . 63–80 . 1983 . 6649193 . 10.3109/03009738309178440 . 3 . free .
  20. Ronquist G, Stegmayr B . Prostatic origin of fucosyl transferase in human seminal plasma--a study on healthy controls and on men with infertility or with prostatic cancer . Urological Research . 12 . 5 . 243–7 . 1984 . 6240149 . 10.1007/bf00256148 . 37354859 . 4 .
  21. Ronquist G, Frithz GG . Prostasomes in human semen contain ADP and GDP . Acta Europaea Fertilitatis . 17 . 4 . 273–6 . 1986 . 3577591 . 16 .
  22. Ronquist G . Effect of modulators on prostasome membrane-bound ATPase in human seminal plasma . European Journal of Clinical Investigation . 17 . 3 . 231–6 . June 1987 . 2957209 . 10.1111/j.1365-2362.1987.tb01241.x . 5983398 . 2 .
  23. Ronquist G . Zinc ion stimulation of ATP cleavage by prostasomes from human seminal plasma . Urologia Internationalis . 43 . 6 . 334–40 . 1988 . 2977004 . 10.1159/000281386 . 3 .
  24. Ronquist G, Frithz G, Jansson A . Prostasome membrane associated enzyme activities and semen parameters in men attending an infertility clinic . Urologia Internationalis . 43 . 3 . 133–8 . 1988 . 2902707 . 10.1159/000281325 . 4 .
  25. Arvidson G, Ronquist G, Wikander G, Ojteg AC . Human prostasome membranes exhibit very high cholesterol/phospholipid ratios yielding high molecular ordering . Biochimica et Biophysica Acta (BBA) - Biomembranes . 984 . 2 . 167–73 . September 1989 . 2548623 . 10.1016/0005-2736(89)90212-5 . 1 .
  26. Olsson I, Ronquist G . Nucleic acid association to human prostasomes . Archives of Andrology . 24 . 1 . 1–10 . 1990 . 1691619 . 10.3109/01485019008986852 . 4 .
  27. Ronquist G, Nilsson BO, Hjertën S . Interaction between prostasomes and spermatozoa from human semen . Archives of Andrology . 24 . 2 . 147–57 . 1990 . 2327824 . 10.3109/01485019008986874 . 2 .
  28. Kelly RW, Holland P, Skibinski G, Harrison C, McMillan L, Hargreave T, James K . Extracellular organelles (prostasomes) are immunosuppressive components of human semen . Clinical and Experimental Immunology . 86 . 3 . 550–6 . December 1991 . 1747961 . 1554200 . 10.1111/j.1365-2249.1991.tb02968.x . 2 .
  29. Skibinski G, Kelly RW, Harkiss D, James K . Immunosuppression by human seminal plasma--extracellular organelles (prostasomes) modulate activity of phagocytic cells . American Journal of Reproductive Immunology . 28 . 2 . 97–103 . September 1992 . 1337434 . 10.1111/j.1600-0897.1992.tb00767.x . 23564256 . 4 .
  30. Rooney IA, Atkinson JP, Krul ES, Schonfeld G, Polakoski K, Saffitz JE, Morgan BP . Physiologic relevance of the membrane attack complex inhibitory protein CD59 in human seminal plasma: CD59 is present on extracellular organelles (prostasomes), binds cell membranes, and inhibits complement-mediated lysis . The Journal of Experimental Medicine . 177 . 5 . 1409–20 . May 1993 . 7683035 . 2191001 . 10.1084/jem.177.5.1409 . 1 .
  31. Skibinski G, Kelly RW, James K . Expression of a common secretory granule specific protein as a marker for the extracellular organelles (prostasomes) in human semen . Fertility and Sterility . 61 . 4 . 755–9 . April 1994 . 8150122 . 10.1016/s0015-0282(16)56658-8 . 2 .
  32. Ronquist G, Fabiani R, Jin M, Nilsson BO, Elenbring K, Hjerten S . Adherence of human prostasomes to mouse spermatozoa and their displacement by monoclonal antibodies as revealed by free zone electrophoresis . Archives of Andrology . 36 . 2 . 101–7 . 1996 . 8907670 . 10.3109/01485019608987085 . 2 .
  33. Nilsson BO, Jin M, Ronquist G . Immunolocalization of prostasomes in the human prostate . Upsala Journal of Medical Sciences . 101 . 2 . 149–57 . 1996 . 8897705 . 10.3109/03009739609178919 . 5 . free .
  34. Nilsson BO, Jin M, Einarsson B, Persson BE, Ronquist G . Monoclonal antibodies against human prostasomes . The Prostate . 35 . 3 . 178–84 . May 1998 . 9582086 . 10.1002/(SICI)1097-0045(19980515)35:3<178::AID-PROS3>3.0.CO;2-D . 2 .
  35. Arienti G, Carlini E, Verdacchi R, Cosmi EV, Palmerini CA . Prostasome to sperm transfer of CD13/aminopeptidase N (EC 3.4.11.2) . Biochimica et Biophysica Acta (BBA) - General Subjects . 1336 . 3 . 533–8 . October 1997 . 9367181 . 10.1016/s0304-4165(97)00071-8 . 17 .
  36. Arienti G, Carlini E, Verdacchi R, Palmerini CA . Transfer of aminopeptidase activity from prostasomes to sperm . Biochimica et Biophysica Acta (BBA) - General Subjects . 1336 . 2 . 269–74 . August 1997 . 9305799 . 10.1016/S0304-4165(97)00036-6 . 18 .
  37. Carlini E, Palmerini CA, Cosmi EV, Arienti G . Fusion of sperm with prostasomes: effects on membrane fluidity . Archives of Biochemistry and Biophysics . 343 . 1 . 6–12 . July 1997 . 9210640 . 10.1006/abbi.1997.9999 . 19 .
  38. Arienti G, Polci A, Carlini E, Palmerini CA . Transfer of CD26/dipeptidyl peptidase IV (E.C. 3.5.4.4) from prostasomes to sperm . FEBS Letters . 410 . 2–3 . 343–6 . June 1997 . 9237659 . 10.1016/S0014-5793(97)00655-8 . 36256822 . 20 .
  39. Arienti G, Carlini E, Palmerini CA . Fusion of human sperm to prostasomes at acidic pH . The Journal of Membrane Biology . 155 . 1 . 89–94 . January 1997 . 9002427 . 10.1007/s002329900160 . 33729362 . 21 .
  40. Renneberg H, Konrad L, Dammshäuser I, Seitz J, Aumüller G . Immunohistochemistry of prostasomes from human semen . The Prostate . 30 . 2 . 98–106 . February 1997 . 9051148 . 10.1002/(SICI)1097-0045(19970201)30:2<98::AID-PROS5>3.0.CO;2-G . 12 .
  41. Arienti G, Carlini E, De Cosmo AM, Di Profio P, Palmerini CA . Prostasome-like particles in stallion semen . Biology of Reproduction . 59 . 2 . 309–13 . August 1998 . 9687300 . 10.1095/biolreprod59.2.309 . 16 . free .
  42. Minelli A, Moroni M, Martínez E, Mezzasoma I, Ronquist G . Occurrence of prostasome-like membrane vesicles in equine seminal plasma . Journal of Reproduction and Fertility . 114 . 2 . 237–43 . November 1998 . 10070353 . 10.1530/jrf.0.1140237 . 5 . free .
  43. Nilsson BO, Lennartsson L, Carlsson L, Nilsson S, Ronquist G . Expression of prostasome-like granules by the prostate cancer cell lines PC3, Du145 and LnCaP grown in monolayer . Upsala Journal of Medical Sciences . 104 . 3 . 199–206 . 1999 . 10680953 . 10.3109/03009739909178963 . 14 . free .
  44. Nilsson BO, Egevad L, Jin M, Ronquist G, Busch C . Distribution of prostasomes in neoplastic epithelial prostate cells . The Prostate . 39 . 1 . 36–40 . April 1999 . 10221264 . 10.1002/(SICI)1097-0045(19990401)39:1<36::AID-PROS6>3.0.CO;2-6 . 1 .
  45. Carlsson L, Påhlson C, Bergquist M, Ronquist G, Stridsberg M . Antibacterial activity of human prostasomes . The Prostate . 44 . 4 . 279–86 . September 2000 . 10951492 . 10.1002/1097-0045(20000901)44:4<279::AID-PROS4>3.0.CO;2-2 . 2 .
  46. Nilsson BO, Carlsson L, Larsson A, Ronquist G . Autoantibodies to prostasomes as new markers for prostate cancer . Upsala Journal of Medical Sciences . 106 . 1 . 43–9 . 2001 . 11817562 . 10.3109/2000-1967-171 . 10 . free .
  47. Utleg AG, Yi EC, Xie T, Shannon P, White JT, Goodlett DR, Hood L, Lin B . Proteomic analysis of human prostasomes . The Prostate . 56 . 2 . 150–61 . July 2003 . 12746840 . 10.1002/pros.10255 . 24396813 . 2 .
  48. Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA . Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen . The Prostate . 69 . 2 . 159–67 . February 2009 . 18819103 . 10.1002/pros.20860 . 18120312 . 1 .
  49. Ronquist KG, Ek B, Morrell J, Stavreus-Evers A, Ström Holst B, Humblot P, Ronquist G, Larsson A . Prostasomes from four different species are able to produce extracellular adenosine triphosphate (ATP) . Biochimica et Biophysica Acta (BBA) - General Subjects . 1830 . 10 . 4604–10 . October 2013 . 23707955 . 10.1016/j.bbagen.2013.05.019 . 2 . free .
  50. Lwaleed BA, Greenfield RS, Birch BR, Cooper AJ . Does human semen contain a functional haemostatic system? A possible role for Tissue Factor Pathway Inhibitor in fertility through semen liquefaction . Thrombosis and Haemostasis . 93 . 5 . 847–52 . May 2005 . 15886798 . 10.1160/TH04-09-0600 . 5 .
  51. Babiker AA, Ekdahl KN, Nilsson B, Ronquist G . Prothrombotic effects of prostasomes isolated from prostatic cancer cell lines and seminal plasma . Seminars in Thrombosis and Hemostasis . 33 . 1 . 80–6 . February 2007 . 17253194 . 10.1055/s-2006-958466 . 2 .
  52. Babiker AA, Hamad OA, Sanchez J, Ronquist G, Nilsson B, Ekdahl KN . Prothrombotic effect of prostasomes of metastatic cell and seminal origin . The Prostate . 67 . 4 . 378–88 . March 2007 . 17219380 . 10.1002/pros.20497 . 31977978 . 3 .
  53. Ronquist KG, Ronquist G, Carlsson L, Larsson A . Human prostasomes contain chromosomal DNA . The Prostate . 69 . 7 . 737–43 . May 2009 . 19143024 . 10.1002/pros.20921 . 22808455 . 5 .
  54. Ronquist GK, Larsson A, Stavreus-Evers A, Ronquist G . Prostasomes are heterogeneous regarding size and appearance but affiliated to one DNA-containing exosome family . The Prostate . 72 . 16 . 1736–45 . December 2012 . 22539202 . 10.1002/pros.22526 . 42538544 . 3 .
  55. Ronquist GK, Larsson A, Ronquist G, Isaksson A, Hreinsson J, Carlsson L, Stavreus-Evers A . Prostasomal DNA characterization and transfer into human sperm . Molecular Reproduction and Development . 78 . 7 . 467–76 . July 2011 . 21638509 . 10.1002/mrd.21327 . 22864833 . 4 .
  56. Tavoosidana G, Ronquist G, Darmanis S, Yan J, Carlsson L, Wu D, Conze T, Ek P, Semjonow A, Eltze E, Larsson A, Landegren UD, Kamali-Moghaddam M . Multiple recognition assay reveals prostasomes as promising plasma biomarkers for prostate cancer . Proceedings of the National Academy of Sciences of the United States of America . 108 . 21 . 8809–14 . May 2011 . 21555566 . 3102389 . 10.1073/pnas.1019330108 . 2011PNAS..108.8809T . 1 . free .
  57. Dubois L, Ronquist KK, Ek B, Ronquist G, Larsson A . Proteomic Profiling of Detergent Resistant Membranes (Lipid Rafts) of Prostasomes . Molecular & Cellular Proteomics . 14 . 11 . 3015–22 . November 2015 . 26272980 . 4638043 . 10.1074/mcp.M114.047530 . free .

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