Cardiac gene therapy with SERCA2a: From bench to bedside

Journal of Molecular and Cellular Cardiology

Volumn 50, Issue 5, 2011, Pages 803-812

  Gwathmey, Judith K ^a   Yerevanian, Alexan I ^b,c   Hajjar, Roger J ^c  

^a Gwathmey Inc   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Heart failure; Sarcoplasmic reticulum; SERCA2a

Indexed keywords

ADENOVIRUS VECTOR; CALCIUM ION; GAMMA INTERFERON; LENTIVIRUS VECTOR; NEUTRALIZING ANTIBODY; PARVOVIRUS VECTOR; PLACEBO; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; UNCLASSIFIED DRUG;

ANTIBODY TITER; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CARDIOVASCULAR RESPONSE; CONGESTIVE HEART FAILURE; CYTOKINE RELEASE; DRUG EFFICACY; DRUG SAFETY; GENE FUNCTION; GENE OVEREXPRESSION; GENE TARGETING; GENE THERAPY; GENE TRANSFER; GENETIC TRANSDUCTION; HEART ARRHYTHMIA; HUMAN; IMMUNE RESPONSE; LOW DRUG DOSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TREATMENT RESPONSE; VIRAL GENE DELIVERY SYSTEM;

ANIMALS; GENE THERAPY; HEART FAILURE; HUMANS; MODELS, BIOLOGICAL; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 79953692977     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.11.011     Document Type: Review

References (107)

1. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010 Feb 23;121(7):948-54.
2. Gwathmey J.K., Slawsky M.T., Hajjar R.J., Briggs G.M., Morgan J.P. Role of intracellular calcium handling in force-interval relationships of human ventricular myocardium. J Clin Invest 1990, 85(5):1599-1613.
3. Hasenfuss G., Pieske B. Calcium cycling in congestive heart failure. J Mol Cell Cardiol 2002, 34(8):951-969.
4. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003 Jul, 4(7):517-529.
5. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002 Jan 10, 415(6868):198-205.
6. Blinks J.R., Wier W.G., Hess P., Prendergast F.G. Measurement of Ca2+ concentrations in living cells. Prog Biophys Mol Biol 1982, 40(1-2):1-114.
7. Gwathmey J.K., Copelas L., MacKinnon R., Schoen F.J., Feldman M.D., Grossman W., et al. Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 1987, 61(1):70-76.
8. Gwathmey J.K., Morgan J.P. Altered calcium handling in experimental pressure-overload hypertrophy in the ferret. Circ Res 1985, 57(6):836-843.
9. Gwathmey J.K., Morgan J.P. The effects of milrinone and piroximone on intracellular calcium handling in working myocardium from the ferret. Br J Pharmacol 1985, 85(1):97-108.
10. Gwathmey J.K., Copelas L., MacKinnon R., Schoen F.J., Feldman M.D., Grossman W., et al. Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 1987, 61(1):70-76.
11. Beuckelmann D.J., Nabauer M., Erdmann E. Intracellular calcium handling in isolated ventricular myocytes from patients with terminal heart failure. Circulation 1992, 85(3):1046-1055.
12. Akar F.G., Tomaselli G.F. Ion channels as novel therapeutic targets in heart failure. Ann Med 2005, 37(1):44-54.
13. Morgan J.P., Erny R.E., Allen P.D., Grossman W., Gwathmey J.K. Abnormal intracellular calcium handling, a major cause of systolic and diastolic dysfunction in ventricular myocardium from patients with heart failure. Circulation 1990, 81(2 Suppl):III21-III32.
14. Vangheluwe P., Louch W.E., Ver Heyen M., Sipido K., Raeymaekers L., Wuytack F. Ca2+ transport ATPase isoforms SERCA2a and SERCA2b are targeted to the same sites in the murine heart. Cell Calcium 2003 Dec, 34(6):457-464.
15. He H., Giordano F.J., Hilal-Dandan R., Choi D.J., Rockman H.A., McDonough P.M., et al. Overexpression of the rat sarcoplasmic reticulum Ca2+ ATPase gene in the heart of transgenic mice accelerates calcium transients and cardiac relaxation. J Clin Invest 1997, 100(2):380-389.
16. Baker D.L., Hashimoto K., Grupp I.L., Ji Y., Reed T., Loukianov E., et al. Targeted overexpression of the sarcoplasmic reticulum Ca2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ Res 1998, 83(12):1205-1214.
17. Bavendiek U., Brixius K., Munch G., Zobel C., Muller-Ehmsen J., Schwinger R.H. Effect of inotropic interventions on the force-frequency relation in the human heart. Basic Res Cardiol 1998, 93(Suppl 1):76-85.
18. Arai M., Alpert N.R., MacLennan D.H., Barton P., Periasamy M. Alterations in sarcoplasmic reticulum gene expression in human heart failure. A possible mechanism for alterations in systolic and diastolic properties of the failing myocardium. Circ Res 1993 Feb, 72(2):463-469.
19. Schwinger R.H., Munch G., Bolck B., Karczewski P., Krause E.G., Erdmann E. Reduced Ca(2+)-sensitivity of SERCA 2a in failing human myocardium due to reduced serin-16 phospholamban phosphorylation. J Mol Cell Cardiol 1999, 31(3):479-491.
20. Haghighi K., Gregory K.N., Kranias E.G. Sarcoplasmic reticulum Ca-ATPase-phospholamban interactions and dilated cardiomyopathy. Biochem Biophys Res Commun 2004, 322(4):1214-1222.
21. Rodriguez P., Mitton B., Nicolaou P., Chen G., Kranias E.G. Phosphorylation of human inhibitor-1 at Ser67 and/or Thr75 attenuates stimulatory effects of protein kinase A signaling in cardiac myocytes. Am J Physiol Heart Circ Physiol 2007, 293(1):H762-H769.
22. Chopra N., Kannankeril P.J., Yang T., Hlaing T., Holinstat I., Ettensohn K., et al. Modest reductions of cardiac calsequestrin increase sarcoplasmic reticulum Ca2+ leak independent of luminal Ca2+ and trigger ventricular arrhythmias in mice. Circ Res 2007, 101(6):617-626.
23. Arvanitis D.A., Vafiadaki E., Fan G.C., Mitton B.A., Gregory K.N., Del Monte F., et al. Histidine-rich Ca-binding protein interacts with sarcoplasmic reticulum Ca-ATPase. Am J Physiol Heart Circ Physiol 293(3):H1581-H1589.
24. Gyorke S., Terentyev D. Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res 2008, 77(2):245-255.
25. Guo T., Cornea R.L., Huke S., Camors E., Yang Y., Picht E., et al. Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca sparks. Circ Res 2010, 106(11):1743-1752.
26. Chelu M.G., Sarma S., Sood S., Wang S., van Oort R.J., Skapura D.G., et al. Calmodulin kinase II-mediated sarcoplasmic reticulum Ca2+ leak promotes atrial fibrillation in mice. J Clin Invest 2009, 119(7):1940-1951.
27. Pleger S.T., Most P., Boucher M., Soltys S., Chuprun J.K., Pleger W., et al. Stable myocardial-specific AAV6-S100A1 gene therapy results in chronic functional heart failure rescue. Circulation 2007, 115(19):2506-2515.
28. Most P., Pleger S.T., Volkers M., Heidt B., Boerries M., Weichenhan D., et al. Cardiac adenoviral S100A1 gene delivery rescues failing myocardium. J Clin Invest 2004, 114(11):1550-1563.
29. Loukianov E., Ji Y., Grupp I.L., Kirkpatrick D.L., Baker D.L., Loukianova T., et al. Enhanced myocardial contractility and increased Ca2+ transport function in transgenic hearts expressing the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+-ATPase. Circ Res 1998, 83(9):889-897.
30. Mork H.K., Sjaastad I., Sande J.B., Periasamy M., Sejersted O.M., Louch W.E. Increased cardiomyocyte function and Ca2+ transients in mice during early congestive heart failure. J Mol Cell Cardiol 2007, 43(2):177-186.
31. Periasamy M., Reed T.D., Liu L.H., Ji Y., Loukianov E., Paul R.J., et al. Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 (SERCA2) gene. J Biol Chem 1999, 274(4):2556-2562.
32. Schultz Jel J., Glascock B.J., Witt S.A., Nieman M.L., Nattamai K.J., Liu L.H., et al. Accelerated onset of heart failure in mice during pressure overload with chronically decreased SERCA2 calcium pump activity. Am J Physiol Heart Circ Physiol 2004, 286(3):H1146-H1153.
33. Sakata S., Lebeche D., Sakata N., Sakata Y., Chemaly E.R., Liang L.F., et al. Restoration of mechanical and energetic function in failing aortic-banded rat hearts by gene transfer of calcium cycling proteins. J Mol Cell Cardiol 2007, 42(4):852-861.
34. Kawase Y., Ly H.Q., Prunier F., Lebeche D., Shi Y., Jin H., et al. Reversal of cardiac dysfunction after long-term expression of SERCA2a by gene transfer in a pre-clinical model of heart failure. J Am Coll Cardiol 2008, 51(11):1112-1119.
35. Byrne M.J., Power J.M., Preovolos A., Mariani J.A., Hajjar R.J., Kaye D.M. Recirculating cardiac delivery of AAV2/1SERCA2a improves myocardial function in an experimental model of heart failure in large animals. Gene Ther 2008, 15(23):1550-1557.
36. Davia K., Bernobich E., Ranu H.K., del Monte F., Terracciano C.M., MacLeod K.T., et al. SERCA2A overexpression decreases the incidence of aftercontractions in adult rabbit ventricular myocytes. J Mol Cell Cardiol 2001, 33(5):1005-1015.
37. del Monte F., Lebeche D., Guerrero J.L., Tsuji T., Doye A.A., Gwathmey J.K., et al. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci USA 2004, 101(15):5622-5627.
38. Prunier F., Kawase Y., Gianni D., Scapin C., Danik S.B., Ellinor P.T., et al. Prevention of ventricular arrhythmias with sarcoplasmic reticulum Ca2+ ATPase pump overexpression in a porcine model of ischemia reperfusion. Circulation 2008, 118(6):614-624.
39. Cutler M.J., Wan X., Laurita K.R., Hajjar R.J., Rosenbaum D.S. Targeted SERCA2a gene expression identifies molecular mechanism and therapeutic target for arrhythmogenic cardiac alternans. Circ Arrhythm Electrophysiol 2009, 2(6):686-694.
40. Del Monte F., Dalal R., Tabchy A., Couget J., Bloch K.D., Peterson R., et al. Transcriptional changes following restoration of SERCA2a levels in failing rat hearts. FASEB J 2004, 18(12):1474-1476.
41. Kay M.A., Glorioso J.C., Naldini L. Viral vectors for gene therapy: the art of turning infectious agents into vehicles of therapeutics. Nat Med 2001, 7(1):33-40.
42. Nishikawa M., Huang L. Nonviral vectors in the new millennium: delivery barriers in gene transfer. Hum Gene Ther 2001, 12(8):861-870.
43. Felgner P.L. Nonviral strategies for gene therapy. Sci Am 1997, 276(6):102-106.
44. Agha-Mohammadi S., Lotze M.T. Regulatable systems: applications in gene therapy and replicating viruses. J Clin Invest 2000, 105(9):1177-1183.
45. Agha-Mohammadi S., Lotze M.T. Immunomodulation of cancer: potential use of selectively replicating agents. J Clin Invest 2000, 105(9):1173-1176.
46. Isner J.M. Myocardial gene therapy. Nature 2002, 415(6868):234-239.
47. Guzman R.J., Lemarchand P., Crystal R.G., Epstein S.E., Finkel T. Efficient and selective adenovirus-mediated gene transfer into vascular neointima. Circulation 1993, 88(6):2838-2848.
48. Barr E., Carroll J., Kalynych A.M., Tripathy S.K., Kozarsky K., Wilson J.M., et al. Efficient catheter-mediated gene transfer into the heart using replication-defective adenovirus. Gene Ther 1994, 1(1):51-58.
49. Hajjar R.J., Schmidt U., Matsui T., Guerrero J.L., Lee K.H., Gwathmey J.K., et al. Modulation of ventricular function through gene transfer in vivo. Proc Natl Acad Sci USA 1998, 95(9):5251-5256.
50. Shohet R.V., Chen S., Zhou Y.T., Wang Z., Meidell R.S., Unger R.H., et al. Echocardiographic destruction of albumin microbubbles directs gene delivery to the myocardium. Circulation 2000, 101(22):2554-2556.
51. Beeri R., Guerrero J.L., Supple G., Sullivan S., Levine R.A., Hajjar R.J. New efficient catheter-based system for myocardial gene delivery. Circulation 2002, 106(14):1756-1759.
52. Donahue J.K., Kikkawa K., Johns D.C., Marban E., Lawrence J.H. Ultrarapid, highly efficient viral gene transfer to the heart. Proc Natl Acad Sci USA 1997, 94(9):4664-4668.
53. Donahue J.K., Kikkawa K., Thomas A.D., Marban E., Lawrence J.H. Acceleration of widespread adenoviral gene transfer to intact rabbit hearts by coronary perfusion with low calcium and serotonin. Gene Ther 1998, 5(5):630-634.
54. Nagata K., Marban E., Lawrence J.H., Donahue J.K. Phosphodiesterase inhibitor-mediated potentiation of adenovirus delivery to myocardium. J Mol Cell Cardiol 2001, 33(3):575-580.
55. Klages N., Zufferey R., Trono D. A stable system for the high-titer production of multiply attenuated lentiviral vectors. Mol Ther 2000, 2(2):170-176.
56. Galimi F., Noll M., Kanazawa Y., Lax T., Chen C., Grompe M., et al. Gene therapy of Fanconi anemia: preclinical efficacy using lentiviral vectors. Blood 2002 Oct, 100(8):2732-2736.
57. Galimi F., Verma I.M. Opportunities for the use of lentiviral vectors in human gene therapy. Curr Top Microbiol Immunol 2002, 261:245-254.
58. Sirven A., Pflumio F., Zennou V., Titeux M., Vainchenker W., Coulombel L., et al. The human immunodeficiency virus type-1 central DNA flap is a crucial determinant for lentiviral vector nuclear import and gene transduction of human hematopoietic stem cells. Blood 2000, 96(13):4103-4110.
59. Bonci D., Cittadini A., Latronico M.V., Borello U., Aycock J.K., Drusco A., et al. 'Advanced' generation lentiviruses as efficient vectors for cardiomyocyte gene transduction in vitro and in vivo. Gene Ther 2003, 10(8):630-636.
60. Monahan P.E., Samulski R.J. AAV vectors: is clinical success on the horizon?. Gene Ther 2000, 7(1):24-30.
61. Monahan P.E., Samulski R.J., Tazelaar J., Xiao X., Nichols T.C., Bellinger D.A., et al. Direct intramuscular injection with recombinant AAV vectors results in sustained expression in a dog model of hemophilia. Gene Ther 1998, 5(1):40-49.
62. Flotte T.R., Carter B.J. Adeno-associated virus vectors for gene therapy. Gene Ther 1995, 2(6):357-362.
63. Schnepp B.C., Jensen R.L., Chen C.L., Johnson P.R., Clark K.R. Characterization of adeno-associated virus genomes isolated from human tissues. J Virol 2005, 79(23):14793-14803.
64. Monahan P.E., Jooss K., Sands M.S. Safety of adeno-associated virus gene therapy vectors: a current evaluation. Expert Opin Drug Saf 2002, 1(1):79-91.
65. Dutheil N., Shi F., Dupressoir T., Linden R.M. Adeno-associated virus site-specifically integrates into a muscle-specific DNA region. Proc Natl Acad Sci USA 2000, 97(9):4862-4866.
66. Young S.M., Samulski R.J. Adeno-associated virus (AAV) site-specific recombination does not require a Rep-dependent origin of replication within the AAV terminal repeat. Proc Natl Acad Sci USA 2001, 98(24):13525-13530.
67. Carter P.J., Samulski R.J. Adeno-associated viral vectors as gene delivery vehicles. Int J Mol Med 2000, 6(1):17-27.
68. Inagaki K., Fuess S., Storm T.A., Gibson G.A., McTiernan C.F., Kay M.A., et al. Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 2006, 14(1):45-53.
69. Pacak C.A., Mah C.S., Thattaliyath B.D., Conlon T.J., Lewis M.A., Cloutier D.E., et al. Recombinant adeno-associated virus serotype 9 leads to preferential cardiac transduction in vivo. Circ Res 2006, 99(4):e3-e9.
70. Wang Z., Zhu T., Qiao C., Zhou L., Wang B., Zhang J., et al. Adeno-associated virus serotype 8 efficiently delivers genes to muscle and heart. Nat Biotechnol 2005, 23(3):321-328.
71. Zhu T., Zhou L., Mori S., Wang Z., McTiernan C.F., Qiao C., et al. Sustained whole-body functional rescue in congestive heart failure and muscular dystrophy hamsters by systemic gene transfer. Circulation 2005, 112(17):2650-2659.
72. Tratschin J.D., Miller I.L., Smith M.G., Carter B.J. Adeno-associated virus vector for high-frequency integration, expression, and rescue of genes in mammalian cells. Mol Cell Biol 1985, 5(11):3251-3260.
73. Carter B.J. Adeno-associated virus vectors in clinical trials. Hum Gene Ther 2005, 16(5):541-550.
74. Flotte T.R. Adeno-associated virus-based gene therapy for inherited disorders. Pediatr Res 2005, 58(6):1143-1147.
75. Monahan P.E., Samulski R.J. Adeno-associated virus vectors for gene therapy: more pros than cons?. Mol Med Today 2000, 6(11):433-440.
76. Schnepp B.C., Clark K.R., Klemanski D.L., Pacak C.A., Johnson P.R. Genetic fate of recombinant adeno-associated virus vector genomes in muscle. J Virol 2003, 77(6):3495-3504.
77. Snyder R.O., Miao C., Meuse L., Tubb J., Donahue B.A., Lin H.F., et al. Correction of hemophilia B in canine and murine models using recombinant adeno-associated viral vectors. Nat Med 1999, 5(1):64-70.
78. Kessler P.D., Podsakoff G.M., Chen X., McQuiston S.A., Colosi P.C., Matelis L.A., et al. Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. Proc Natl Acad Sci USA 1996, 93(24):14082-14087.
79. Rabinowitz J.E., Rolling F., Li C., Conrath H., Xiao W., Xiao X., et al. Cross-packaging of a single adeno-associated virus (AAV) type 2 vector genome into multiple AAV serotypes enables transduction with broad specificity. J Virol 2002, 76(2):791-801.
80. Ferrari F.K., Samulski T., Shenk T., Samulski R.J. Second-strand synthesis is a rate-limiting step for efficient transduction by recombinant adeno-associated virus vectors. J Virol 1996, 70(5):3227-3234.
81. Malik A.K., Monahan P.E., Allen D.L., Chen B.G., Samulski R.J., Kurachi K. Kinetics of recombinant adeno-associated virus-mediated gene transfer. J Virol 2000, 74(8):3555-3565.
82. Nakai H., Storm T.A., Kay M.A. Recruitment of single-stranded recombinant adeno-associated virus vector genomes and intermolecular recombination are responsible for stable transduction of liver in vivo. J Virol 2000, 74(20):9451-9463.
83. Maurice J.P., Hata J.A., Shah A.S., White D.C., McDonald P.H., Dolber P.C., et al. Enhancement of cardiac function after adenoviral-mediated in vivo intracoronary beta2-adrenergic receptor gene delivery. J Clin Invest 1999, 104(1):21-29.
84. Zincarelli C., Soltys S., Rengo G., Rabinowitz J.E. Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 2008, 16(6):1073-1080.
85. Fromes Y., Salmon A., Wang X., Collin H., Rouche A., Hagege A., et al. Gene delivery to the myocardium by intrapericardial injection. Gene Ther 1999, 6(4):683-688.
86. Preovolos A.C., Mennen M.T., Bilney A., Mariani J., Kaye D.M., Power J.M. Development of a novel perfusion technique to allow targeted delivery of gene therapy-the V-Focus system. J Extra-Corpor Technol 2006, 38(1):51-52.
87. Bridges C.R., Burkman J.M., Malekan R., Konig S.M., Chen H., Yarnall C.B., et al. Global cardiac-specific transgene expression using cardiopulmonary bypass with cardiac isolation. Ann Thorac Surg 2002, 73(6):1939-1946.
88. Bridges C.R., Gopal K., Holt D.E., Yarnall C., Cole S., Anderson R.B., et al. Efficient myocyte gene delivery with complete cardiac surgical isolation in situ. J Thorac Cardiovasc Surg 2005, 130(5):1364.
89. Koransky M.L., Robbins R.C., Blau H.M. VEGF gene delivery for treatment of ischemic cardiovascular disease. Trends Cardiovasc Med 2002, 12(3):108-114.
90. Edelberg J.M., Huang D.T., Josephson M.E., Rosenberg R.D. Molecular enhancement of porcine cardiac chronotropy. Heart 2001, 86(5):559-562.
91. Boekstegers P., von Degenfeld G., Giehrl W., Heinrich D., Hullin R., Kupatt C., et al. Myocardial gene transfer by selective pressure-regulated retroinfusion of coronary veins. Gene Ther 2000, 7(3):232-240.
92. Hoshino K., Kimura T., De Grand A.M., Yoneyama R., Kawase Y., Houser S., et al. Three catheter-based strategies for cardiac delivery of therapeutic gelatin microspheres. Gene Ther 2006, 13(18):1320-1327.
93. Hajjar R.J., Zsebo K., Deckelbaum L., Thompson C., Rudy J., Yaroshinsky A., et al. Design of a phase 1/2 trial of intracoronary administration of AAV1/SERCA2a in patients with heart failure. J Card Fail 2008, 14(5):355-367.
94. Jaski B.E., Jessup M.L., Mancini D.M., Cappola T.P., Pauly D.F., Greenberg B., et al. Calcium upregulation by percutaneous administration of gene therapy in cardiac disease (CUPID Trial), a first-in-human phase 1/2 clinical trial. J Card Fail 2009, 15(3):171-181.
95. Kwon I., Schaffer D.V. Designer gene delivery vectors: molecular engineering and evolution of adeno-associated viral vectors for enhanced gene transfer. Pharm Res 2008, 25(3):489-499.
96. Zaiss A.K., Muruve D.A. Immunity to adeno-associated virus vectors in animals and humans: a continued challenge. Gene Ther 2008, 15(11):808-816.
97. Halbert C.L., Miller A.D., McNamara S., Emerson J., Gibson R.L., Ramsey B., et al. Prevalence of neutralizing antibodies against adeno-associated virus (AAV) types 2, 5, and 6 in cystic fibrosis and normal populations: Implications for gene therapy using AAV vectors. Hum Gene Ther 2006, 17(4):440-447.
98. Calcedo R., Vandenberghe L.H., Gao G., Lin J., Wilson J.M. Worldwide epidemiology of neutralizing antibodies to adeno-associated viruses. J Infect Dis 2009, 199(3):381-390.
99. Boutin S., Monteilhet V., Veron P., Leborgne C., Benveniste O., Montus M.F., et al. Prevalence of serum IgG and neutralizing factors against adeno-associated virus (AAV) types 1, 2, 5, 6, 8, and 9 in the healthy population: implications for gene therapy using AAV vectors. Hum Gene Ther 2010, 21(6):704-712.
100. Buning H., Ried M.U., Perabo L., Gerner F.M., Huttner N.A., Enssle J., et al. Receptor targeting of adeno-associated virus vectors. Gene Ther 2003, 10(14):1142-1151.
101. Cottard V., Valvason C., Falgarone G., Lutomski D., Boissier M.C., Bessis N. Immune response against gene therapy vectors: influence of synovial fluid on adeno-associated virus mediated gene transfer to chondrocytes. J Clin Immunol 2004, 24(2):162-169.
102. Erles K., Rohde V., Thaele M., Roth S., Edler L., Schlehofer J.R. DNA of adeno-associated virus (AAV) in testicular tissue and in abnormal semen samples. Hum Reprod 2001, 16(11):2333-2337.
103. Moskalenko M., Chen L., van Roey M., Donahue B.A., Snyder R.O., McArthur J.G., et al. Epitope mapping of human anti-adeno-associated virus type 2 neutralizing antibodies: implications for gene therapy and virus structure. J Virol 2000, 74(4):1761-1766.
104. Mingozzi F., Meulenberg J.J., Hui D.J., Basner-Tschakarjan E., Hasbrouck N.C., Edmonson S.A., et al. AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-dependent activation of capsid-specific T cells. Blood 2009, 114(10):2077-2086.
105. Mingozzi F., Maus M.V., Hui D.J., Sabatino D.E., Murphy S.L., Rasko J.E., et al. CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat Med 2007, 13(4):419-422.
106. Donahue J.K., Kikkawa K., Johns D.C., Marban E. J. L. Ultrarapid highly efficient viral gene transfer to the heart. Proc Natl Acad Sci 1997, 94:4664-4668.
107. Donahue J.K., Kikkawa K., Thomas A.D., Marban E., Lawrence J.H. Acceleration of widespread adenoviral gene transfer to intact rabbit hearts by coronary perfusion with low calcium and serotonin. Gene Ther 1998, 5(5):630-634.