CNS-targeted viral delivery of G-CSF in an animal model for ALS: Improved efficacy and preservation of the neuromuscular unit

Molecular Therapy

Volumn 19, Issue 2, 2011, Pages 284-292

  Henriques, Alexandre ^a,b,c   Pitzer, Claudia ^a   Dittgen, Tanjew ^a   Klugmann, Matthias ^d   Dupuis, Luc ^b,c   Schneider, Armin ^a  

^a SYGNIS Bioscience   (Germany)

^b INSERM   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GRANULOCYTE COLONY STIMULATING FACTOR; PARVOVIRUS VECTOR;

ADENO ASSOCIATED VIRUS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; FEMALE; FUNCTIONAL ASSESSMENT; GENE EXPRESSION; GRIP STRENGTH; LIFE EXPECTANCY; MALE; MOTONEURON; MOTOR PERFORMANCE; MOUSE; NERVE FIBER REGENERATION; NEUROMUSCULAR SYNAPSE; NEUROMUSCULAR SYSTEM; NONHUMAN; QUANTITATIVE ANALYSIS; TREATMENT RESPONSE; VIRAL GENE DELIVERY SYSTEM;

ADENO-ASSOCIATED VIRUS; ANIMALIA; MUS;

EID: 79551631827     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.271     Document Type: Article

References (50)

1. Mitchell, JD and Borasio, GD (2007). Amyotrophic lateral sclerosis. Lancet 369: 2031-2041.
2. Gonzalez de Aguilar, JL, Echaniz-Laguna, A, Fergani, A, René, F, Meininger, V, Loeffler, JP et al. (2007). Amyotrophic lateral sclerosis: all roads lead to Rome. J Neurochem 101: 1153-1160.
3. Pasinelli, P and Brown, RH (2006). Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7: 710-723.
4. Rothstein, JD (2009). Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann Neurol 65 Suppl 1: S3-S9.
5. Henriques, A, Pitzer, C and Schneider, A (2010). Neurotrophic growth factors for the treatment of amyotrophic lateral sclerosis: where do we stand? Front Neurosci 4: 32.
6. Welte, K, Platzer, E, Gabrilove, JL, Lu, L, Levi, E, Polivka, A et al. (1985). Purification to apparent homogeneity and biochemical characterization of human pluripotent hematopoietic colony-stimulating factor. Haematol Blood Transfus 29: 398-401.
7. Schneider, A, Krüger, C, Steigleder, T, Weber, D, Pitzer, C, Laage, R et al. (2005). The hematopoietic factor G-CSF is a neuronal ligand that counteracts programmed cell death and drives neurogenesis. J Clin Invest 115: 2083-2098.
8. Pitzer, C, Krüger, C, Plaas, C, Kirsch, F, Dittgen, T, Müller, R et al. (2008). Granulocytecolony stimulating factor improves outcome in a mouse model of amyotrophic lateral sclerosis. Brain 131(Pt 12): 3335-3347.
9. Pitzer, C, Klussmann, S, Krüger, C, Letellier, E, Plaas, C, Dittgen, T et al. (2010). The hematopoietic factor granulocyte-colony stimulating factor improves outcome in experimental spinal cord injury. J Neurochem 113: 930-942.
10. Meuer, K, Pitzer, C, Teismann, P, Krüger, C, Göricke, B, Laage, R et al. (2006). Granulocyte-colony stimulating factor is neuroprotective in a model of Parkinson's disease. J Neurochem 97: 675-686.
11. Henriques, A, Pitzer, C, Dupuis, L and Schneider, A (2010). G-CSF protects motoneurons against axotomy-induced apoptotic death in neonatal mice. BMC Neurosci 11: 25.
12. Atchison, RW, Casto, BC and Hammon, WM (1965). Adenovirus-associated defective virus particles. Science 149: 754-756.
13. Bouard, D, Alazard-Dany, D and Cosset, FL (2009). Viral vectors: from virology to transgene expression. Br J Pharmacol 157: 153-165.
14. Dodge, JC, Haidet, AM, Yang, W, Passini, MA, Hester, M, Clarke, J et al. (2008). Delivery of AAV-IGF-1 to the CNS extends survival in ALS mice through modification of aberrant glial cell activity. Mol Ther 16: 1056-1064.
15. Kaspar, BK, Lladó, J, Sherkat, N, Rothstein, JD and Gage, FH (2003). Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301: 839-842.
16. Palomeque, J, Chemaly, ER, Colosi, P, Wellman, JA, Zhou, S, Del Monte, F et al. (2007). Efficiency of eight different AAV serotypes in transducing rat myocardium in vivo. Gene Ther 14: 989-997.
17. Lepore, AC, Haenggeli, C, Gasmi, M, Bishop, KM, Bartus, RT, Maragakis, NJ et al. (2007). Intraparenchymal spinal cord delivery of adeno-associated virus IGF-1 is protective in the SOD1G93A model of ALS. Brain Res 1185: 256-265.
18. Klugmann, M, Leichtlein, CB, Symes, CW, Serikawa, T, Young, D and During, MJ (2005). Restoration of aspartoacylase activity in CNS neurons does not ameliorate motor deficits and demyelination in a model of Canavan disease. Mol Ther 11: 745-753.
19. Neidhart, J, Mangalik, A, Kohler, W, Stidley, C, Saiki, J, Duncan, P et al. (1989). Granulocyte colony-stimulating factor stimulates recovery of granulocytes in patients receiving dose-intensive chemotherapy without bone marrow transplantation. J Clin Oncol 7: 1685-1692.
20. Hedrich, H, and Bullock, G (2004). The Laboratory Mouse (The Handbook of Experimental Animals). Elsevier Academic Press: London, p. 278.
21. Ludolph, AC, Bendotti, C, Blaugrund, E, Chio, A, Greensmith, L, Loeffler, JP et al. (2010). Guidelines for preclinical animal research in ALS/MND: A consensus meeting. Amyotroph Lateral Scler 11: 38-45.
22. Boillée, S, Yamanaka, K, Lobsiger, CS, Copeland, NG, Jenkins, NA, Kassiotis, G et al. (2006). Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312: 1389-1392.
23. Fischer, LR, Culver, DG, Tennant, P, Davis, AA, Wang, M, Castellano-Sanchez, A et al. (2004). Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185: 232-240.
24. Dupuis, L and Loeffler, JP (2009). Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models. Curr Opin Pharmacol 9: 341-346.
25. Schaefer, AM, Sanes, JR and Lichtman, JW (2005). A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J Comp Neurol 490: 209-219.
26. Pan, HC, Wu, HT, Cheng, FC, Chen, CH, Sheu, ML and Chen, CJ (2009). Potentiation of angiogenesis and regeneration by G-CSF after sciatic nerve crush injury. Biochem Biophys Res Commun 382: 177-182.
27. Griffin, JW, Pan, B, Polley, MA, Hoffman, PN and Farah, MH (2010). Measuring nerve regeneration in the mouse. Exp Neurol 223: 60-71.
28. Warita, H, Itoyama, Y and Abe, K (1999). Selective impairment of fast anterograde axonal transport in the peripheral nerves of asymptomatic transgenic mice with a G93A mutant SOD1 gene. Brain Res 819: 120-131.
29. Hollis, ER 2nd, Kadoya, K, Hirsch, M, Samulski, RJ and Tuszynski, MH (2008). Efficient retrograde neuronal transduction utilizing self-complementary AAV1. Mol Ther 16: 296-301.
30. Kaspar, BK, Erickson, D, Schaffer, D, Hinh, L, Gage, FH and Peterson, DA (2002). Targeted retrograde gene delivery for neuronal protection. Mol Ther 5: 50-56.
31. Klugmann, M, Symes, CW, Leichtlein, CB, Klaussner, BK, Dunning, J, Fong, D et al. (2005). AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28: 347-360.
32. Passini, MA, Watson, DJ, Vite, CH, Landsburg, DJ, Feigenbaum, AL and Wolfe, JH (2003). Intraventricular brain injection of adeno-associated virus type 1 (AAV1) in neonatal mice results in complementary patterns of neuronal transduction to AAV2 and total long-term correction of storage lesions in the brains of beta-glucuronidasedeficient mice. J Virol 77: 7034-7040.
33. Taymans, JM, Vandenberghe, LH, Haute, CV, Thiry, I, Deroose, CM, Mortelmans, L et al. (2007). Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. Hum Gene Ther 18: 195-206.
34. Franich, NR, Fitzsimons, HL, Fong, DM, Klugmann, M, During, MJ and Young, D (2008). AAV vector-mediated RNAi of mutant huntingtin expression is neuroprotective in a novel genetic rat model of Huntington's disease. Mol Ther 16: 947-956.
35. Li, B, Duysen, EG, Poluektova, LY, Murrin, LC and Lockridge, O (2006). Protection from the toxicity of diisopropylfluorophosphate by adeno-associated virus expressing acetylcholinesterase. Toxicol Appl Pharmacol 214: 152-165.
36. Hollis, ER 2nd, Jamshidi, P, Lorenzana, AO, Lee, JK, Gray, SJ, Samulski, RJ et al. (2010). Transient demyelination increases the efficiency of retrograde AAV transduction. Mol Ther 18: 1496-1500.
37. Scott, S, Kranz, JE, Cole, J, Lincecum, JM, Thompson, K, Kelly, N et al. (2008). Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph Lateral Scler 9: 4-15.
38. Kaplitt, MG, Feigin, A, Tang, C, Fitzsimons, HL, Mattis, P, Lawlor, PA et al. (2007). Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369: 2097-2105.
39. Moss, RB, Milla, C, Colombo, J, Accurso, F, Zeitlin, PL, Clancy, JP et al. (2007). Repeated aerosolized AAV-CFTR for treatment of cystic fibrosis: a randomized placebocontrolled phase 2B trial. Hum Gene Ther 18: 726-732.
40. Rodino-Klapac, LR, Lee, JS, Mulligan, RC, Clark, KR and Mendell, JR (2008). Lack of toxicity of alpha-sarcoglycan overexpression supports clinical gene transfer trial in LGMD2D. Neurology 71: 240-247.
41. Mandel, RJ (2010). CERE-110, an adeno-associated virus-based gene delivery vector expressing human nerve growth factor for the treatment of Alzheimer's disease. Curr Opin Mol Ther 12: 240-247.
42. Maguire, AM, Simonelli, F, Pierce, EA, Pugh, EN Jr, Mingozzi, F, Bennicelli, J et al. (2008). Safety and efficacy of gene transfer for Leber's congenital amaurosis. N Engl J Med 358: 2240-2248.
43. Manno, CS, Pierce, GF, Arruda, VR, Glader, B, Ragni, M, Rasko, JJ et al. (2006). Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response. Nat Med 12: 342-347.
44. Kay, MA (2007). AAV vectors and tumorigenicity. Nat Biotechnol 25: 1111-1113.
45. Buie, LK, Rasmussen, CA, Porterfield, EC, Ramgolam, VS, Choi, VW, Markovic-Plese, S et al. (2010). Self-complementary AAV virus (scAAV) safe and long-term gene transfer in the trabecular meshwork of living rats and monkeys. Invest Ophthalmol Vis Sci 51: 236-248.
46. Kordower, JH and Olanow, CW (2008). Regulatable promoters and gene therapy for Parkinson's disease: is the only thing to fear, fear itself? Exp Neurol 209: 34-40.
47. Duque, S, Joussemet, B, Riviere, C, Marais, T, Dubreil, L, Douar, AM et al. (2009). Intravenous administration of self-complementary AAV9 enables transgene delivery to adult motor neurons. Mol Ther 17: 1187-1196.
48. Pun, S, Santos, AF, Saxena, S, Xu, L and Caroni, P (2006). Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9: 408-419.
49. Yamasaki, R, Tanaka, M, Fukunaga, M, Tateishi, T, Kikuchi, H, Motomura, K et al. (2010). Restoration of microglial function by granulocyte-colony stimulating factor in ALS model mice. J Neuroimmunol 229: 51-62.
50. Gowing, G, Philips, T, Van Wijmeersch, B, Audet, JN, Dewil, M, Van Den Bosch, L et al. (2008). Ablation of proliferating microglia does not affect motor neuron degeneration in amyotrophic lateral sclerosis caused by mutant superoxide dismutase. J Neurosci 28: 10234-10244.