Adeno-associated virus vector-mediated gene delivery to the vasculature and kidney.
Languages of publication
Relatively successful elsewhere, gene delivery aimed at the vasculature and kidney has made very little progress. In the kidney, the hurdles are related to the unique structure–function relationships of this organ and in the blood vessels to a variety of, mostly endothelial, factors making the delivery of transgenes very difficult. Among gene-therapeutic approaches, most viral gene delivery systems utilized to date have shown significant practical and safety-related limitations due to the level and duration of recombinant transgene expression as well as their induction of a significant host immune response to vector proteins. Recombinant adeno-associated virus (rAAV) vectors appear to offer a vehicle for safe, long-term transgene expression. rAAV-based vectors are characterized by a relative non-immunogenicity and the absence of viral coding sequences. Furthermore, they allow for establishment of long-term latency without deleterious effects on the host cell. This brief review addresses problems related to transgene-delivery to kidney and vasculature with particular attention given to rAAV vectors. The potential for gene therapy as a strategy for selected renal and vascular diseases is also discussed.
- Afione SA, Conrad CK, Kearns WG, Chunduru S, Adams R, Reynolds TC, Guggino WB, Cutting GR, Carter BJ, Flotte TR (1996) In vivo model of adeno-associated virus vector persistence and rescue. J Virol 70: 3235-3241.
- Alisky JM, Hughes SM, Sauter SL, Jolly D, Dubensky TW Jr, Staber PD, Chiorini JA, Davidson BL (2000) Transduction of murine cerebellar neurons with recombinant FIV and AAV5 vectors. Neuroreport 11: 2669-2673.
- Anderson WF (1998) Human gene therapy. Nature 392: 25-30.
- Atkinson MA, Maclaren NK (1994) The pathogenesis of insulin-dependent diabetes mellitus. N Engl J Med 331: 1428-1436.
- Auricchio A, O’Connor E, Weiner D, Gao GP, Hildinger M, Wang L, Calcedo R, Wilson JM (2002) Noninvasive gene transfer to the lung for systemic delivery of therapeutic proteins. J Clin Invest 110: 499-504.
- Berns KI, Linden RM (1995) The cryptic life style of adeno-associated virus. Bioessays 17: 237-245.
- Brown D, Weyer P, Orci L (1987) Nonclathrin-coated vesicles are involved in endocytosis in kidney collecting duct intercalated cells. Anat Rec 218: 237-242.
- Chao H, Liu Y, Rabinowitz J, Li C, Samulski RJ, Walsh CE (2000) Several log increase in therapeutic transgene delivery by distinct adeno-associated viral serotype vectors. Mol Ther 2: 619-623.
- Chen S, Agarwal A, Glushakova OY, Jorgensen MS, Salgar SK, Poirier A, Flotte TR, Croker BP, Madsen KM, Atkinson MA, Hauswirth WW, Berns KI, Tisher CC (2003) Gene delivery in renal tubular epithelial cells using recombinant adeno-associated viral vectors. J Am Soc Nephrol 14: 947-958.
- Chen S, Kapturczak M, Loiler SA, Zolotukhin S, Glushakova OY, Madsen KM, Samulski RJ, Hauswirth WW, Campbell-Thompson M, Berns KI, Flotte TR, Atkinson MA, Tisher CC, Agarwal A (2005) Efficient transduction of vascular endothelial cells with recombinant adeno-associated virus serotype 1 and 5. Hum Gene Ther 16: 235-247.
- Chiorini JA, Kim F, Yang L, Kotin RM (1999) Cloning and characterization of adeno-associated virus type 5. J Virol 73: 1309-1319.
- Conrad CK, Allen SS, Afione SA, Reynolds TC, Beck SE, Fee-Maki M, Barrazza-Ortiz X, Adams R, Askin FB, Carter BJ, Guggino WB, Flotte TR (1996) Safety of single-dose administration of an adeno-associated virus (AAV)-CFTR vector in the primate lung. Gene Ther 3: 658-668.
- Crook MF, Akyurek LM (2003) Gene transfer strategies to inhibit neointima formation. Trends Cardiovasc Med 13: 102-106.
- Davidson BL, Stein CS, Heth JA, Martins I, Kotin RM, Derksen TA, Zabner J, Ghodsi A, Chiorini JA (2000) Recombinant adeno-associated virus type 2, 4, and 5 vectors: transduction of variant cell types and regions in the mammalian central nervous system. Proc Natl Acad Sci USA 97: 3428-3432.
- Dishart KL, Denby L, George SJ, Nicklin SA, Yendluri S, Tuerk MJ, Kelley MP, Donahue BA, Newby AC, Harding T, Baker AH (2003) Third-generation lentivirus vectors efficiently transduce and phenotypically modify vascular cells: implications for gene therapy. J Mol Cell Cardiol 35: 739-748.
- Duan D, Yue Y, Yan Z, Yang J, Engelhardt JF (2000) Endosomal processing limits gene transfer to polarized airway epithelia by adeno-associated virus. J Clin Invest 105: 1573-1587.
- Ferrari FK, Xiao X, Mccarty D, Samulski RJ (1997) New developments in the generation of Ad-free high-titer rAAV gene therapy vectors. Nat Med 3: 1295-1297.
- Fisher KJ, Jooss K, Alston J, Yang Y, Haecker SE, High K, Pathak R, Raper SE, Wilson JM (1997) Recombinant adeno-associated virus for muscle directed gene therapy. Nat Med 3: 306-312.
- Flotte TR, Afione SA, Conrad C, Mcgrath SA, Solow R, Oka H, Zeitlin PL, Guggino WB, Carter BJ (1993) Stable in vivo expression of the cystic fibrosis transmembrane conductance regulator with an adeno-associated virus vector. Proc Natl Acad Sci USA 90: 10613-10617.
- Flotte T, Agarwal A, Wang J, Song S, Fenjves ES, Inverardi L, Chesnut K, Afione S, Loiler S, Wasserfall C, Kapturczak M, Ellis T, Nick H, Atkinson M (2001) Efficient ex vivo transduction of pancreatic islet cells with recombinant adeno-associated virus vectors. Diabetes 50: 515-520.
- Flotte TR, Zeitlin PL, Reynolds TC, Heald AE, Pedersen P, Beck S, Conrad CK, Brass-Ernst L, Humphries M, Sullivan K, Wetzel R, Taylor G, Carter BJ, Guggino WB (2003) Phase I trial of intranasal and endobronchial administration of a recombinant adeno-associated virus serotype 2 (rAAV2)-CFTR vector in adult cystic fibrosis patients: a two-part clinical study. Hum Gene Ther 14: 1079-1088.
- Flotte TR, Brantly ML, Spencer LT, Byrne BJ, Spencer CT, Baker DJ, Humphries M (2004) Phase I trial of intramuscular injection of a recombinant adeno-associated virus alpha 1-antitrypsin (rAAV2-CB-hAAT) gene vector to AAT-deficient adults. Hum Gene Ther 15: 93-128.
- Gao GP, Alvira MR, Wang L, Calcedo R, Johnston J, Wilson JM (2002) Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci USA 99: 11854-11859.
- Gao G, Vandenberghe LH, Alvira MR, Lu Y, Calcedo R, Zhou X, Wilson JM (2004) Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 78: 6381-6388.
- Giraud C, Winocour E, Berns KI (1994) Site-specific integration by adeno-associated virus is directed by a cellular DNA sequence. Proc Natl Acad Sci USA 91: 10039-10043.
- Gnatenko D, Arnold TE, Zolotukhin S, Nuovo GJ, Muzyczka N, Bahou WF (1997) Characterization of recombinant adeno-associated virus-2 as a vehicle for gene delivery and expression into vascular cells. J Investig Med 45: 87-98.
- Gonzalez MA, Selwyn AP (2003) Endothelial function inflammation prognosis in cardiovascular disease. Am J Med 115 Suppl 8A: 99S-106S.
- Gruchala M, Bhardwaj S, Pajusola K, Roy H, Rissanen TT, Kokina I, Kholova I, Markkanen JE, Rutanen J, Heikura T, Alitalo K, Bueler H, Yla-Herttuala S (2004) Gene transfer into rabbit arteries with adeno-associated virus and adenovirus vectors. J Gene Med 6: 545-554.
- Hauck B, Xiao W (2003) Characterization of tissue tropism determinants of adeno-associated virus type 1. J Virol 77: 2768-2774.
- Hermonat PL, Muzyczka N (1984) Use of adeno-associated virus as a mammalian DNA cloning vector: transduction of neomycin resistance into mammalian tissue culture cells. Proc Natl Acad Sci USA 81: 6466-6470.
- Jooss K, Yang Y, Fisher KJ, Wilson JM (1998) Transduction of dendritic cells by DNA viral vectors directs the immune response to transgene products in muscle fibers. J Virol 72: 4212-4223.
- Kaludov N, Brown KE, Walters RW, Zabner J, Chiorini JA (2001) Adeno-associated virus serotype 4 (AAV4) and AAV5 both require sialic acid binding for hemagglutination and efficient transduction but differ in sialic acid linkage specificity. J Virol 75: 6884-6893.
- Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, O’malley KL, During MJ (1994) Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8: 148-154.
- Kapturczak MH, Flotte T, Atkinson MA (2001) Adeno-associated virus (AAV) as a vehicle for therapeutic gene delivery: improvements in vector design and viral production enhance potential to prolong graft survival in pancreatic islet cell transplantation for the reversal of type 1 diabetes. Curr Mol Med 1: 245-258.
- Kapturczak M, Zolotukhin S, Cross J, Pileggi A, Molano RD, Jorgensen M, Byrne B, Flotte TR, Ellis T, Inverardi L, Ricordi C, Nick H, Atkinson M, Agarwal A (2002) Transduction of human and mouse pancreatic islet cells using a bicistronic recombinant adeno-associated viral vector. Mol Ther 5: 154-160.
- Katusic ZS (2002) Therapeutic angiogenesis: new indication for endothelial NO synthase gene transfer. Arterioscler Thromb Vasc Biol 22: 1254-1255.
- Kay MA, Manno CS, Ragni MV, Larson PJ, Couto LB, Mcclelland A, Glader B, Chew AJ, Tai SJ, Herzog RW, Arruda V, Johnson F, Scallan C, Skarsgard E, Flake AW, High KA (2000) Evidence for gene transfer and expression of factor IX in haemophilia B patients treated with an AAV vector. Nat Genet 24: 257-261.
- Kessler PD, Podsakoff GM, Chen X, Mcquiston SA, Colosi PC, Matelis LA, Kurtzman GJ, Byrne BJ (1996) Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc Natl Acad Sci USA 93: 14082-14087.
- Lieberthal W, Nigam SK (1998) Acute renal failure I relative importance of proximal vs distal tubular injury. Am J Physiol 275: F623-631.
- Lipkowitz MS, Hanss B, Tulchin N, Wilson PD, Langer JC, Ross MD, Kurtzman GJ, Klotman PE, Klotman ME (1999) Transduction of renal cells in vitro and in vivo by adeno-associated virus gene therapy vectors. J Am Soc Nephrol 10: 1908-1915.
- Liu Q, Muruve DA (2003) Molecular basis of the inflammatory response to adenovirus vectors. Gene Ther 10: 935-940.
- Loiler SA, Conlon TJ, Song S, Tang Q, Warrington KH, Agarwal A, Kapturczak M, Li C, Ricordi C, Atkinson MA, Muzyczka N, Flotte TR (2003) Targeting recombinant adeno-associated virus vectors to enhance gene transfer to pancreatic islets and liver. Gene Ther 10: 1551-1558.
- Maeda Y, Ikeda U, Ogasawara Y, Urabe M, Takizawa T, Saito T, Colosi P, Kurtzman G, Shimada K, Ozawa K (1997) Gene transfer into vascular cells using adeno-associated virus (AAV) vectors. Cardiovasc Res 35: 514-521.
- McCown TJ, Xiao X, Li J, Breese GR, Samulski RJ (1996) Differential and persistent expression patterns of CNS gene transfer by an adeno-associated virus (AAV) vector. Brain Res 713: 99-107.
- Mori S, Wang L, Takeuchi T, Kanda T (2004) Two novel adeno-associated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 330: 375-383.
- Muller OJ, Kaul F, Weitzman MD, Pasqualini R, Arap W, Kleinschmidt JA, Trepel M (2003) Random peptide libraries displayed on adeno-associated virus to select for targeted gene therapy vectors. Nat Biotechnol 21: 1040-1046.
- Nicklin SA, Buening H, Dishart KL, De Alwis M, Girod A, Hacker U, Thrasher AJ, Ali RR, Hallek M, Baker AH (2001) Efficient and selective AAV2-mediated gene transfer directed to human vascular endothelial cells. Mol Ther 4: 174-181.
- Pajusola K, Gruchala M, Joch H, Luscher TF, Yla-Herttuala S, Bueler H (2002) Cell-type-specific characteristics modulate the transduction efficiency of adeno-associated virus type 2 and restrain infection of endothelial cells. J Virol 76: 11530-11540.
- Pascariu M, Bendayan M, Ghitescu L (2004) Correlated endothelial caveolin overexpression and increased transcytosis in experimental diabetes. J Histochem Cytochem 52: 65-76.
- Ponnazhagan S, Erikson D, Kearns WG, Zhou SZ, Nahreini P, Wang XS, Srivastava A (1997) Lack of site-specific integration of the recombinant adeno-associated virus 2 genomes in human cells. Hum Gene Ther 8: 275-284.
- Qing K, Mah C, Hansen J, Zhou S, Dwarki V, Srivastava A (1999) Human fibroblast growth factor receptor 1 is a co-receptor for infection by adeno-associated virus 2. Nat Med 5: 71-77.
- Rabinowitz JE, Rolling F, Li C, Conrath H, Xiao W, Xiao X, Samulski RJ (2002) Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 76: 791-801.
- Richter M, Iwata A, Nyhuis J, Nitta Y, Miller AD, Halbert CL, Allen MD (2000) Adeno-associated virus vector transduction of vascular smooth muscle cells in vivo. Physiol Genomics 2: 117-127.
- Song S, Morgan M, Ellis T, Poirier A, Chesnut K, Wang J, Brantly M, Muzyczka N, Byrne BJ, Atkinson M, Flotte TR (1998) Sustained secretion of human alpha-1-antitrypsin from murine muscle transduced with adeno-associated virus vectors. Proc Natl Acad Sci USA 95: 14384-14388.
- Summerford C, Samulski RJ (1998) Membrane-associated heparan sulfate proteoglycan is a receptor for adeno-associated virus type 2 virions. J Virol 72: 1438-1445.
- Summerford C, Bartlett JS, Samulski RJ (1999) AlphaVbeta5 integrin: a co-receptor for adeno-associated virus type 2 infection. Nat Med 5: 78-82.
- Takeda S, Takahashi M, Mizukami H, Kobayashi E, Takeuchi K, Hakamata Y, Kaneko T, Yamamoto H, Ito C, Ozawa K, Ishibashi K, Matsuzaki T, Takata K, Asano Y, Kusano E (2004) Successful gene transfer using adeno-associated virus vectors into the kidney: comparison among adeno-associated virus serotype 1-5 vectors in vitro and in vivo. Nephron Exp Nephrol 96: e119-126.
- Tratschin JD, West MH, Sandbank T, Carter BJ (1984) A human parvovirus adeno-associated virus as a eucaryotic vector: transient expression and encapsidation of the procaryotic gene for chloramphenicol acetyltransferase. Mol Cell Biol 4: 2072-2081.
- Vassalli G, Bueler H, Dudler J, Von Segesser LK, Kappenberger L (2003) Adeno-associated virus (AAV) vectors achieve prolonged transgene expression in mouse myocardium and arteries in vivo: a comparative study with adenovirus vectors. Int J Cardiol 90: 229-238.
- Wagner JA, Reynolds T, Moran ML, Moss RB, Wine JJ, Flotte TR, Gardner P (1998) Efficient and persistent gene transfer of AAV-CFTR in maxillary sinus. Lancet 351: 1702-1703.
- Wagner JA, Messner AH, Moran ML, Daifuku R, Kouyama K, Desch JK, Manley S, Norbash AM, Conrad CK, Friborg S, Reynolds T, Guggino WB, Moss RB, Carter BJ, Wine JJ, Flotte TR, Gardner P (1999) Safety and biological efficacy of an adeno-associated virus vector-cystic fibrosis transmembrane regulator (AAV-CFTR) in the cystic fibrosis maxillary sinus. Laryngoscope 109: 266-274.
- Walters RW, Yi SM, Keshavjee S, Brown KE, Welsh MJ, Chiorini JA, Zabner J (2001) Binding of adeno-associated virus type 5 to 23-linked sialic acid is required for gene transfer. J Biol Chem 276: 20610-20616.
- White SJ, Nicklin SA, Buning H, Brosnan MJ, Leike K, Papadakis ED, Hallek M, Baker AH (2004) Targeted gene delivery to vascular tissue in vivo by tropism-modified adeno-associated virus vectors. Circulation 109: 513-519.
- Work LM, Nicklin SA, Baker AH (2003) Targeting gene therapy vectors to the vascular endothelium. Curr Atheroscler Rep 5: 163-170.
- Work LM, Nicklin SA, Brain NJ, Dishart KL, Von Seggern DJ, Hallek M, Buning H, Baker AH (2004) Development of efficient viral vectors selective for vascular smooth muscle cells. Mol Ther 9: 198-208.
- Xiao X, Li J, Samulski RJ (1996) Efficient long-term gene transfer into muscle tissue of immunocompetent mice by adeno-associated virus vector. J Virol 70: 8098-8108.
- Zabner J, Seiler M, Walters R, Kotin RM, Fulgeras W, Davidson BL, Chiorini JA (2000) Adeno-associated virus type 5 (AAV5) but not AAV2 binds to the apical surfaces of airway epithelia and facilitates gene transfer. J Virol 74: 3852-3858.
- Zhang YC, Powers M, Wasserfall C, Brusko T, Song S, Flotte T, Snyder RO, Potter M, Scott-Jorgensen M, Campbell-Thompson M, Crawford JM, Nick HS, Agarwal A, Ellis TM, Atkinson MA (2004) Immunity to adeno-associated virus serotype 2 delivered transgenes imparted by genetic predisposition to autoimmunity. Gene Ther 11: 233-240.
Publication order reference