Targeted gene delivery to the enteric nervous system using AAV: A comparison across serotypes and capsid mutants

Molecular Therapy

Volumn 23, Issue 3, 2015, Pages 488-500

  Benskey, Matthew J ^a,b   Kuhn, Nathan C ^a   Galligan, James J ^a,b   Garcia, Joanna ^a   Boye, Shannon E ^c   Hauswirth, William W ^c   Mueller, Christian ^d   Boye, Sanford L ^c   Manfredsson, Fredric P ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; PARVOVIRUS VECTOR; PHENYLALANINE; THREONINE; TYROSINE; VALINE;

ADENO ASSOCIATED VIRUS 1; ADENO ASSOCIATED VIRUS 2; ADENO ASSOCIATED VIRUS 5; ADENO ASSOCIATED VIRUS 6; ADENO ASSOCIATED VIRUS 8; ADENO ASSOCIATED VIRUS 9; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; DESCENDING COLON; GLIA; IMMUNE RESPONSE; IMMUNOGENICITY; INTESTINE INNERVATION; MALE; MOUSE; MYENTERIC PLEXUS; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RAT; SEROTYPE; STRAIN DIFFERENCE; VIRAL GENE DELIVERY SYSTEM; VIRAL TROPISM; VIRUS CAPSID; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS TRANSMISSION; YOUNG ADULT; ANIMAL; C57BL MOUSE; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; CYTOLOGY; DEPENDOPARVOVIRUS; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; INNERVATION; METABOLISM; MUTATION; PROCEDURES; REPORTER GENE; SPRAGUE DAWLEY RAT; TARGETED GENE REPAIR; THERAPEUTIC USE;

ADENO-ASSOCIATED VIRUS; MIRIDAE; MURINAE; RATTUS;

ANIMALS; CAPSID; COLON, DESCENDING; DEPENDOVIRUS; ENTERIC NERVOUS SYSTEM; GENE EXPRESSION; GENES, REPORTER; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MUTATION; NEUROGLIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SEROGROUP; TARGETED GENE REPAIR; TRANSDUCTION, GENETIC; VIRAL TROPISM;

EID: 84924045412     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2015.7     Document Type: Article

References (39)

1. Daya, S and Berns, KI (2008). Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 21: 583-593.
2. Flotte, TR (2004). Gene therapy progress and prospects: recombinant adeno-associated virus (rAAV) vectors. Gene Ther 11: 805-810.
3. Mueller, C and Flotte, TR (2008). Clinical gene therapy using recombinant adeno-associated virus vectors. Gene Ther 15: 858-863.
4. Mingozzi, F and High, KA (2011). Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet 12: 341-355.
5. During, MJ, Xu, R, Young, D, Kaplitt, MG, Sherwin, RS and Leone, P (1998). Peroral gene therapy of lactose intolerance using an adeno-associated virus vector. Nat Med 4: 1131-1135.
6. Fu, H, Dirosario, J, Killedar, S, Zaraspe, K and McCarty, DM (2011). Correction of neurological disease of mucopolysaccharidosis IIIB in adult mice by rAAV9 trans-blood-brain barrier gene delivery. Mol Ther 19: 1025-1033.
7. Gombash, SE, Cowley, CJ, Fitzgerald, JA, Hall, JC, Mueller, C, Christofi, FL et al. (2014). Intravenous AAV9 efficiently transduces myenteric neurons in neonate and juvenile mice. Front Mol Neurosci 7: 81.
8. Wood, JD. Enteric Nervous System (The-Brain-In-The-Gut). Morgan & Claypool Life Sciences, Princeton, NJ. 2011.
9. Belkind-Gerson, J, Graeme-Cook, F and Winter, H (2006). Enteric nervous system disease and recovery, plasticity, and regeneration. J Pediatr Gastroenterol Nutr 42: 343-350.
10. Forsyth, CB, Shannon, KM, Kordower, JH, Voigt, RM, Shaikh, M, Jaglin, JA et al. (2011). Increased intestinal permeability correlates with sigmoid mucosa alpha-synuclein staining and endotoxin exposure markers in early Parkinson's disease. PLoS One 6: e28032.
11. Braak, H, de Vos, RA, Bohl, J and Del Tredici, K (2006). Gastric alpha-synuclein immunoreactive inclusions in Meissner's and Auerbach's plexuses in cases staged for Parkinson's disease-related brain pathology. Neurosci Lett 396: 67-72.
12. Shannon, KM, Keshavarzian, A, Dodiya, HB, Jakate, S and Kordower, JH (2012). Is alpha-synuclein in the colon a biomarker for premotor Parkinson's disease? Evidence from 3 cases. Mov Disord 27: 716-719.
13. Shannon, KM, Keshavarzian, A, Mutlu, E, Dodiya, HB, Daian, D, Jaglin, JA et al. (2012). Alpha-synuclein in colonic submucosa in early untreated Parkinson's disease. Mov Disord 27: 709-715.
14. Mayer, EA and Collins, SM (2002). Evolving pathophysiologic models of functional gastrointestinal disorders. Gastroenterology 122: 2032-2048.
15. Dawson, TM, Ko, HS and Dawson, VL (2010). Genetic animal models of Parkinson's disease. Neuron 66: 646-661.
16. Kanaan, NM and Manfredsson, FP (2012). Loss of functional alpha-synuclein: a toxic event in Parkinson's disease? J Parkinsons Dis 2: 249-267.
17. Kuhn, M, Haebig, K, Bonin, M, Ninkina, N, Buchman, VL, Poths, S et al. (2007). Whole genome expression analyses of single- and double-knock-out mice implicate partially overlapping functions of alpha- and gamma-synuclein. Neurogenetics 8: 71-81.
18. Kay, CN, Ryals, RC, Aslanidi, GV, Min, SH, Ruan, Q, Sun, J et al. (2013). Targeting photoreceptors via intravitreal delivery using novel, capsid-mutated AAV vectors. PLoS One 8: e62097.
19. Petrs-Silva, H, Dinculescu, A, Li, Q, Min, SH, Chiodo, V, Pang, JJ et al. (2009). High-efficiency transduction of the mouse retina by tyrosine-mutant AAV serotype vectors. Mol Ther 17: 463-471.
20. Petrs-Silva, H, Dinculescu, A, Li, Q, Deng, WT, Pang, JJ, Min, SH et al. (2011). Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol Ther 19: 293-301.
21. Aslanidi, GV, River, AE, Ortiz, L, Song, L, Ling, C, Govindasamy, L et al. (2013). Small, N-terminal tags activate Parkin E3 ubiquitin ligase activity by disrupting its autoinhibited conformation. PLoS One 8: e59142-e59142.
22. Gabriel, N, Hareendran, S, Sen, D, Gadkari, RA, Sudha, G, Selot, R et al. (2013). Bioengineering of AAV2 capsid at specific serine, threonine, or lysine residues improves its transduction efficiency in vitro and in vivo. Hum Gene Ther Methods 24: 80-93.
23. Burger, C. (2004). Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10: 302-317.
24. Reimsnider, S, Manfredsson, FP, Muzyczka, N and Mandel, RJ (2007). Time course of transgene expression after intrastriatal pseudotyped rAAV2/1, rAAV2/2, rAAV2/5, and rAAV2/8 transduction in the rat. Mol Ther 15: 1504-1511.
25. Inagaki, K, Fuess, S, Storm, TA, Gibson, GA, Mctiernan, CF, Kay, MA et al. (2006). Robust systemic transduction with AAV9 vectors in mice: efficient global cardiac gene transfer superior to that of AAV8. Mol Ther 14: 45-53.
26. Zincarelli, C, Soltys, S, Rengo, G and Rabinowitz, JE (2008). Analysis of AAV serotypes 1-9 mediated gene expression and tropism in mice after systemic injection. Mol Ther 16: 1073-1080.
27. Ito, D, Tanaka, K, Suzuki, S, Dembo, T and Fukuuchi, Y (2001). Enhanced expression of Iba1, ionized calcium-binding adapter molecule 1, after transient focal cerebral ischemia in rat brain. Stroke 32: 1208-1215.
28. Qin, L, Wu, X, Block, ML, Liu, Y, Breese, GR, Hong, JS et al. (2007). Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55: 453-462.
29. Streit, WJ, Walter, SA and Pennell, NA (1999). Reactive microgliosis. Prog Neurobiol 57: 563-581.
30. During, MJ, Symes, CW, Lawlor, PA, Lin, J, Dunning, J, Fitzsimons, HL et al. (2000). An oral vaccine against NMDAR1 with efficacy in experimental stroke and epilepsy. Science 287: 1453-1460.
31. Manfredsson, FP, Rising, AC and Mandel, RJ (2009). AAV9: a potential blood-brain barrier buster. Mol Ther 17: 403-405.
32. Foust, KD, Nurre, E, Montgomery, CL, Hernandez, A, Chan, CM and Kaspar, BK (2009). Intravascular AAV9 preferentially targets neonatal neurons and adult astrocytes. Nat Biotechnol 27: 59-65.
33. Zolotukhin, S, Potter, M, Zolotukhin, I, Sakai, Y, Loiler, S, Fraites, TJ Jr et al. (2002). Production and purification of serotype 1, 2, and 5 recombinant adeno-associated viral vectors. Methods 28: 158-167.
34. Wu, Z, Asokan, A, Grieger, JC, Govindasamy, L, Agbandje-McKenna, M and Samulski, RJ (2006). Single amino acid changes can influence titer, heparin binding, and tissue tropism in different adeno-associated virus serotypes. J Virol 80: 11393-11397.
35. Manfredsson, FP, Burger, C, Sullivan, LF, Muzyczka, N, Lewin, AS and Mandel, RJ (2007). rAAV-mediated nigral human parkin over-expression partially ameliorates motor deficits via enhanced dopamine neurotransmission in a rat model of Parkinson's disease. Exp Neurol 207: 289-301.
36. Aschauer, DF, Kreuz, S and Rumpel, S (2013). Analysis of transduction efficiency, tropism and axonal transport of AAV serotypes 1, 2, 5, 6, 8 and 9 in the mouse brain. PLoS One 8: e76310.
37. Zaiss, AK and Muruve, DA (2005). Immune responses to adeno-associated virus vectors. Curr Gene Ther 5: 323-331.
38. Jacobson, SG, Acland, GM, Aguirre, GD, Aleman, TS, Schwartz, SB, Cideciyan, AV et al. (2006). Safety of recombinant adeno-associated virus type 2-RPE65 vector delivered by ocular subretinal injection. Mol Ther 13: 1074-1084.
39. Patel, BA, Dai, X, Burda, JE, Zhao, H, Swain, GM, Galligan, JJ et al. (2010). Inhibitory neuromuscular transmission to ileal longitudinal muscle predominates in neonatal guinea pigs. Neurogastroenterol Motil 22: 909-18, e236.