Self-complementary adeno-associated virus explained

Self-complementary adeno-associated virus (scAAV) is a viral vector engineered from the naturally occurring adeno-associated virus (AAV) to be used as a tool for gene therapy.[1] Use of recombinant AAV (rAAV) has been successful in clinical trials addressing a variety of diseases.[2] This lab-made progeny of rAAV is termed "self-complementary" because the coding region has been designed to form an intra-molecular double-stranded DNA template. A rate-limiting step for the standard AAV genome involves the second-strand synthesis since the typical AAV genome is a single-stranded DNA template.[3] [4] However, this is not the case for scAAV genomes. Upon infection, rather than waiting for cell mediated synthesis of the second strand, the two complementary halves of scAAV will associate to form one double stranded DNA (dsDNA) unit that is ready for immediate replication and transcription. The caveat of this construct is that instead of the full coding capacity found in rAAV (4.7–6kb)[5] scAAV can only hold about half of that amount (≈2.4kb).[6]

In gene therapy application utilizing rAAV, the virus transduces the cell with a single stranded DNA (ssDNA) flanked by two inverted terminal repeats (ITRs). These ITRs form hairpins at the end of the sequence to serve as primers to initiate synthesis of the second strand before subsequent steps of infection can begin. The second strand synthesis is considered to be one of several blocks to efficient infection.[7] Additional advantages of scAAV include increased and prolonged transgene expression in vitro and in vivo, as well as "higher in vivo DNA stability and more effective circularization."[8]

In gene therapy

scAAV is an attractive vector for use in gene therapy for many reasons. Its parent vector, AAV, is already being used in clinical trials.[9] Due to a variety of scAAV serotypes available, scientists can choose a serotype which has properties desirable for their therapy. Selecting only a subset of cells improves specificity and lowers the risk of being inhibited by the immune system. Different scAAV and AAV serotypes can efficiently transfect a variety of cellular targets.[10] [11] Like all vector-based approaches to gene therapy, one obstacle in translating therapies from pre-clinical trials into a human clinical application will be the production of large quantities of highly concentrated virus.[12] One disadvantage that scAAV faces is that due to robust gene expression, transgene products delivered via scAAV elicit a stronger immune response than those same transgenes delivered via a single-stranded AAV vector.[13]

Virus classification

Like AAV, scAAV is a member of the family Parvoviridae, commonly known as parvoviruses. These viruses are nonenveloped, single-strand DNA (ssDNA) viruses. Within Parvoviridae, scAAV further belongs to the Dependovirus genus, characteristically defined by an inability to replicate on their own. In nature, these viruses depend on another virus to provide replication machinery; adeno-associated virus can only replicate during an active infection of adenovirus or some types of herpesvirus. In lab use, this obstacle is overcome by addition of the helper plasmids, which exogenously expresses replication genes which AAV itself lacks.

Viral replication

As a dependovirus, scAAV remains in a latent state within the cell until the cell experiences certain permissive conditions. These can include presence of a helper virus infection (such as adenovirus) or other toxic events such as exposure to UV light or carcinogens.[14] Because the endogenous rep ORF has been replaced with transgene, exogenously provided rep genes encode the proteins required for genome replication and other viral life cycle components. The ITRs located 5' and 3' of the viral genome serve as the origin of replication.[15]

Viral packaging

Like the rep ORF, scAAV's cap ORF has been replaced by transgene and therefore is provided exogenously in a lab environment. The genes encoded in this ORF build capsid proteins and are responsible (along with intracellular processing) for conveying target specificity. Rep proteins participate in the integration of the genome into preformed capsids. Despite the fact that scAAV is designed to form dsDNA upon infection, the two complementary strands are not packaged in a double stranded manner. Parvoviruses package their viral genome such that the ssDNA bases come in contact with the amino acids on the inside of the viral capsid. Thus the sequence of scAAV is likely unwound by a virally encoded DNA helicase before being packaged into viral protein capsid.

Notes and References

  1. 10.1038/sj.gt.3301514 . Self-complementary recombinant adeno-associated virus (scAAV) vectors promote efficient transduction independently of DNA synthesis . 2001 . McCarty . D M . Monahan . P E . Samulski . R J . Gene Therapy . 8 . 16 . 1248–54 . 11509958. free .
  2. Web site: Gene Therapy Clinical Trials Worldwide.
  3. 8627803 . 1996 . Ferrari . FK . Samulski . T . Shenk . T . Samulski . RJ . Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors . 70 . 5 . 3227–34 . 190186 . Journal of Virology. 10.1128/JVI.70.5.3227-3234.1996 .
  4. 8523565 . 1996 . Fisher . KJ . Gao . GP . Weitzman . MD . Dematteo . R . Burda . JF . Wilson . JM . Transduction with recombinant adeno-associated virus for gene therapy is limited by leading-strand synthesis . 70 . 1 . 520–32 . 189840 . Journal of Virology. 10.1128/JVI.70.1.520-532.1996 .
  5. 10.1128/JVI.79.15.9933-9944.2005 . Packaging Capacity of Adeno-Associated Virus Serotypes: Impact of Larger Genomes on Infectivity and Postentry Steps . 2005 . Grieger . J. C. . Samulski . R. J. . Journal of Virology . 79 . 15 . 9933–44 . 16014954 . 1181570.
  6. Wu. J. Zhao. W. Zhong. L. Han. Z. Li. B. Ms. W. Weigel-Kelley. KA. Warrington. KH. Srivastava. A. Self-complementary recombinant adeno-associated viral vectors: packaging capacity and the role of rep proteins in vector purity. Human Gene Therapy. Feb 2007. 18. 2. 171–82. 10.1089/hum.2006.088. 17328683.
  7. 10.1038/mt.2008.171 . Self-complementary AAV Vectors; Advances and Applications . 2008 . McCarty . Douglas M . Molecular Therapy . 16 . 10 . 1648–56 . 18682697. free .
  8. 10.1038/sj.gt.3302133 . Rapid and highly efficient transduction by double-stranded adeno-associated virus vectors in vitro and in vivo . 2003 . Wang . Z . Ma . H-I . Li . J . Sun . L . Zhang . J . Xiao . X . Gene Therapy . 10 . 26 . 2105–11 . 14625564. free .
  9. 10.3410/M3-17 . 21941595 . 3169911 . Advancements in adeno-associated viral gene therapy approaches: Exploring a new horizon . 2011 . Aalbers . Caroline J. . Tak . Paul P. . Vervoordeldonk . Margriet J. . F1000 Medicine Reports . 3. 17 . free .
  10. Hillestad . ML . Guenzel . AJ . Nath . KA . Barry . MA . Oct 2012 . A vector-host system to fingerprint virus tropism . Hum Gene Ther. . 23 . 10. 1116–26 . 10.1089/hum.2011.116 . 22834781 . 3472556.
  11. Zincarelli . C . Soltys . S . Rengo . G . Rabinowitz . JE . Jun 2008 . Analysis of AAV serotypes 1–9 mediated gene expression and tropism in mice after systemic injection . Mol. Ther. . 16 . 6. 1073–80 . 10.1038/mt.2008.76 . 18414476 . free .
  12. Clément . N . Knop . DR . Byrne . BJ . Aug 2009 . Large-scale adeno-associated viral vector production using a herpesvirus-based system enables manufacturing for clinical studies . Hum Gene Ther. . 20 . 8. 796–806 . 10.1089/hum.2009.094 . 19569968 . 2861951.
  13. Wu . T . Töpfer . K . Lin . SW . Li . H . Bian . A . Zhou . XY . High . KA . Ertl . HC . Mar 2012 . Self-complementary AAVs induce more potent transgene product-specific immune responses compared to a single-stranded genome . Mol. Ther. . 20 . 3. 572–9 . 10.1038/mt.2011.280 . 22186792 . 3293612.
  14. Berns . KI . Sep 1990 . Parvovirus replication . Microbiol. Rev. . 54 . 3. 316–29 . 2215424 . 372780 . 10.1128/mmbr.54.3.316-329.1990.
  15. Büning . H . Perabo . L . Coutelle . O . Quadt-Humme . S . Hallek . M . Jul 2008 . Recent developments in adeno-associated virus vector technology . J. Gene Med. . 10 . 7. 717–33 . 10.1002/jgm.1205 . 18452237 . 41510186 .