HSV-1-mediated NGF delivery delays nociceptive deficits in a genetic model of diabetic neuropathy

Experimental Neurology

Volumn 198, Issue 1, 2006, Pages 260-270

  Walwyn, W M ^a   Matsuka, Y ^b   Arai, D ^c   Bloom, D C ^a   Lam, H ^a   Tran, C ^a   Spigelman, I ^b   Maidment, N T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

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

Author keywords

Diabetic neuropathy; Herpes Simplex Virus 1; Lepr db db mice; Nerve growth factor; Nociception

Indexed keywords

HERPESVIRUS VECTOR; NERVE GROWTH FACTOR; NEUROTROPHIN; PROTEIN P75; SUBSTANCE P;

AFFERENT NERVE GROUP 1; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; COURSE EVALUATION; DIABETIC NEUROPATHY; DISEASE COURSE; DRUG EFFECT; EXPRESSION VECTOR; GENE TARGETING; HERPES SIMPLEX VIRUS 1; HYPOALGESIA; LIFESPAN; MALE; MEDICAL ASSESSMENT; MOUSE; MOUSE STRAIN; NERVE FIBER C; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SENSORY NERVE; SPINAL GANGLION; VIRAL GENE DELIVERY SYSTEM;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, NORTHERN; CELL COUNT; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GANGLIA, SPINAL; GENE THERAPY; GENETIC VECTORS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NERVE FIBERS; NERVE GROWTH FACTORS; PAIN MEASUREMENT; REACTION TIME; RECEPTOR, NERVE GROWTH FACTOR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIMPLEXVIRUS; SUBSTANCE P;

EID: 32644433171     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2005.12.006     Document Type: Article

References (63)

1. S.K. Akkina, C.L. Patterson, and D.E. Wright GDNF rescues nonpeptidergic unmyelinated primary afferents in streptozotocin-treated diabetic mice Exp. Neurol. 167 2001 173 182
2. P. Anand Neurotrophins and peripheral neuropathy Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 351 1996 449 454
3. S.C. Apfel Neurotrophic factors in the therapy of diabetic neuropathy Am. J. Med. 107 1999 34S 42S
4. S.C. Apfel Nerve growth factor for the treatment of diabetic neuropathy: what went wrong, what went right, and what does the future hold? Int. Rev. Neurobiol. 50 2002 393 413
5. S.C. Apfel, J.C. Arezzo, M. Brownlee, H. Federoff, and J.A. Kessler Nerve growth factor administration protects against experimental diabetic sensory neuropathy Brain Res. 634 1994 7 12
6. S.C. Apfel, J.A. Kessler, B.T. Adornato, W.J. Litchy, C. Sanders, and C.A. Rask Recombinant human nerve growth factor in the treatment of diabetic polyneuropathy. NGF Study Group Neurology 51 1998 695 702
7. S.C. Apfel, S. Schwartz, B.T. Adornato, R. Freeman, V. Biton, M. Rendell, A. Vinik, M. Giuliani, J.C. Stevens, R. Barbano, and P.J. Dyck Efficacy and safety of recombinant human nerve growth factor in patients with diabetic polyneuropathy: a randomized controlled trial. rhNGF Clinical Investigator Group JAMA 284 2000 2215 2221
8. S.J. Bird, and M.J. Brown The clinical spectrum of diabetic neuropathy Semin. Neurol. 16 1996 115 122
9. + channel III and SNS gene expression in spinal sensory neurons NeuroReport 8 1997 2331 2335
10. D.C. Bloom HSV vectors for gene therapy M. Brown A.R. MacLean Methods in Molecular Medicine 1996 Humana Press Totowa, NJ 369 386
11. D.C. Bloom, J.R. Lokensgard, N.T. Maidment, L.T. Feldman, and J.G. Stevens Long-term expression of genes in vivo using non-replicating HSV vectors Gene Ther. 1 Suppl. 1 1994 S36 S38
12. T.J. Boucher, and S.B. McMahon Neurotrophic factors and neuropathic pain Curr. Opin. Pharmacol. 1 2001 66 72
13. F. Cai, D.R. Tomlinson, and P. Fernyhough Elevated expression of neurotrophin-3 mRNA in sensory nerve of streptozotocin-diabetic rats Neurosci. Lett. 263 1999 81 84
14. M. Chattopadhyay, J. Goss, D. Lacomis, W.C. Goins, J.C. Glorioso, M. Mata, and D.J. Fink Protective effect of HSV-mediated gene transfer of nerve growth factor in pyridoxine neuropathy demonstrates functional activity of trkA receptors in large sensory neurons of adult animals Eur. J. Neurosci. 17 2003 732 740
15. M. Chattopadhyay, J. Goss, D. Wolfe, W.C. Goins, S. Huang, J.C. Glorioso, M. Mata, and D.J. Fink Protective effect of herpes simplex virus-mediated neurotrophin gene transfer in cisplatin neuropathy Brain 127 2004 929 939
16. J.A. Christianson, J.T. Riekhof, and D.E. Wright Restorative effects of neurotrophin treatment on diabetes-induced cutaneous axon loss in mice Exp. Neurol. 179 2003 188 199
17. J.A. Christianson, J.M. Ryals, K.E. McCarson, and D.E. Wright Beneficial actions of neurotrophin treatment on diabetes-induced hypoalgesia in mice J. Pain 4 2003 493 504
18. J.D. Delcroix, D.R. Tomlinson, and P. Fernyhough Diabetes and axotomy-induced deficits in retrograde axonal transport of nerve growth factor correlate with decreased levels of p75LNTR protein in lumbar dorsal root ganglia Brain Res. Mol. Brain Res. 51 1997 82 90
19. J.D. Delcroix, G.J. Michael, J.V. Priestley, D.R. Tomlinson, and P. Fernyhough Effect of nerve growth factor treatment on p75NTR gene expression in lumbar dorsal root ganglia of streptozocin-induced diabetic rats Diabetes 47 1998 1779 1785
20. L.T. Diemel, W.J. Brewster, P. Fernyhough, and D.R. Tomlinson Expression of neuropeptides in experimental diabetes; effects of treatment with nerve growth factor or brain-derived neurotrophic factor Brain Res. Mol. Brain Res. 21 1994 171 175
21. A.M. Di Giulio, E. Lesma, and A. Gorio Diabetic neuropathy in the rat: 1. Alcar augments the reduced levels and axoplasmic transport of substance P J. Neurosci. Res. 40 1995 414 419
22. A.T. Dobson, T.P. Margolis, F. Sedarati, J.G. Stevens, and L.T. Feldman A latent, nonpathogenic HSV-1-derived vector stably expresses beta-galactosidase in mouse neurons Neuron 5 1990 353 360
23. B. Doubleday, and P.P. Robinson The effect of NGF depletion on the neurotropic influence exerted by the distal stump following nerve transection J. Anat. 186 Pt. 3 1995 593 605
24. D.G. Drubin, S.C. Feinstein, E.M. Shooter, and M.W. Kirschner Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors J. Cell Biol. 101 1985 1799 1807
25. P.J. Dyck, and C. Giannini Pathologic alterations in the diabetic neuropathies of humans: a review J. Neuropathol. Exp. Neurol. 55 1996 1181 1193
26. P.J. Dyck, K.M. Kratz, J.L. Karnes, W.J. Litchy, R. Klein, J.M. Pach, D.M. Wilson, P.C. O'Brien, L.J. Melton III, and F.J. Service The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study Neurology 43 1993 817 824
27. K.A. Elias, M.J. Cronin, T.A. Stewart, and R.C. Carlsen Peripheral neuropathy in transgenic diabetic mice: restoration of C-fiber function with human recombinant nerve growth factor Diabetes 47 1998 1637 1642
28. P. Fernyhough, L.T. Diemel, W.J. Brewster, and D.R. Tomlinson Deficits in sciatic nerve neuropeptide content coincide with a reduction in target tissue nerve growth factor messenger RNA in streptozotocin-diabetic rats: effects of insulin treatment Neuroscience 62 1994 337 344
29. P. Fernyhough, L.T. Diemel, and D.R. Tomlinson Target tissue production and axonal transport of neurotrophin-3 are reduced in streptozotocin-diabetic rats Diabetologia 41 1998 300 306
30. J. Fjell, T.R. Cummins, S.D. Dib-Hajj, K. Fried, J.A. Black, and S.G. Waxman Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons Brain Res. Mol. Brain Res. 67 1999 267 282
31. J. Fjell, T.R. Cummins, K. Fried, J.A. Black, and S.G. Waxman In vivo NGF deprivation reduces SNS expression and TTX-R sodium currents in IB4-negative DRG neurons J. Neurophysiol. 81 1999 803 810
32. N. Ghilardi, S. Ziegler, A. Wiestner, R. Stoffel, M.H. Heim, and R.C. Skoda Defective STAT signaling by the leptin receptor in diabetic mice Proc. Natl. Acad. Sci. U. S. A. 93 1996 6231 6235
33. J.R. Goss, W.F. Goins, D. Lacomis, M. Mata, J.C. Glorioso, and D.J. Fink Herpes simplex-mediated gene transfer of nerve growth factor protects against peripheral neuropathy in streptozotocin-induced diabetes in the mouse Diabetes 51 2002 2227 2232
34. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 32 1988 77 88
35. J. Jakobsen, S. Brimijoin, K. Skau, P. Sidenius, and D. Wells Retrograde axonal transport of transmitter enzymes, fucose-labeled protein, and nerve growth factor in streptozotocin-diabetic rats Diabetes 30 1981 797 803
36. R. Levi-Montalcini, S.D. Skaper, R. Dal Toso, L. Petrelli, and A. Leon Nerve growth factor: from neurotrophin to neurokine Trends Neurosci. 19 1996 514 520
37. J.R. Lokensgard, H. Berthomme, and L.T. Feldman The latency-associated promoter of herpes simplex virus type 1 requires a region downstream of the transcription start site for long-term expression during latency J. Virol. 71 1997 6714 6719
38. K. Maeda, P. Fernyhough, and D.R. Tomlinson Regenerating sensory neurones of diabetic rats express reduced levels of mRNA for GAP-43, gamma-preprotachykinin and the nerve growth factor receptors, trkA and p75NGFR Brain Res. Mol. Brain Res. 37 1996 166 174
39. J. Mamet, M. Lazdunski, and N. Voilley How nerve growth factor drives physiological and inflammatory expressions of acid-sensing ion channel 3 in sensory neurons J. Biol. Chem. 278 2003 48907 48913
40. M.D. Mastropaolo, N.P. Evans, M.K. Byrnes, A.M. Stevens, J.L. Robertson, and S.B. Melville Synergy in polymicrobial infections in a mouse model of type 2 diabetes Infect. Immun. 73 2005 6055 6063
41. Y. Matsuka, and I. Spigelman Hyperosmolar solutions selectively block action potentials in rat myelinated sensory fibers: implications for diabetic neuropathy J. Neurophysiol. 91 2004 48 56
42. S.A. Moore, R.G. Peterson, D.L. Felten, T.R. Cartwright, and B.L. O'Connor Reduced sensory and motor conduction velocity in 25-week-old diabetic [C57BL/Ks (db/db)] mice Exp. Neurol. 70 1980 548 555
43. F. Norido, R. Canella, R. Zanoni, and A. Gorio Development of diabetic neuropathy in the C57BL/Ks (db/db) mouse and its treatment with gangliosides Exp. Neurol. 83 1984 221 232
44. J.C. Petruska, and L.M. Mendell The many functions of nerve growth factor: multiple actions on nociceptors Neurosci. Lett. 361 2004 168 171
45. J. Pirart, J.P. Lauvaux, and W. Rey Blood sugar and diabetic complications N. Engl. J. Med. 298 1978 1149
46. G. Pittenger, and A. Vinik Nerve growth factor and diabetic neuropathy Exp. Diabesity Res. 4 2003 271 285
47. J.V. Priestley, G.J. Michael, S. Averill, M. Liu, and N. Willmott Regulation of nociceptive neurons by nerve growth factor and glial cell line derived neurotrophic factor Can. J. Physiol. Pharmacol. 80 2002 495 505
48. D.M. Robertson, and A.A. Sima Diabetic neuropathy in the mutant mouse [C57BL/ks(db/db)]: a morphometric study Diabetes 29 1980 60 67
49. S.R. Sullivan, R.A. Underwood, N.S. Gibran, R.O. Sigle, M.L. Usui, W.G. Carter, and J.E. Olerud Validation of a model for the study of multiple wounds in the diabetic mouse (db/db) Plast. Reconstr. Surg. 113 2004 953 960
50. Y. Schmidt, J.W. Unger, I. Bartke, and R. Reiter Effect of nerve growth factor on peptide neurons in dorsal root ganglia after taxol or cisplatin treatment and in diabetic (db/db) mice Exp. Neurol. 132 1995 16 23
51. I. Spigelman, M.S. Gold, and A.R. Light Electrophysiological recording techniques in pain research L. Kruger Methods in Pain Research 2001 CRC Press Boca Raton 147 168
52. C.L. Stucky, and G.R. Lewin Isolectin B(4)-positive and -negative nociceptors are functionally distinct J. Neurosci. 19 1999 6497 6505
53. C.L. Stucky, J.B. Shin, and G.R. Lewin Neurotrophin-4: a survival factor for adult sensory neurons Curr. Biol. 12 2002 1401 1404
54. P.K. Stys, B.R. Ransom, and S.G. Waxman Compound action potential of nerve recorded by suction electrode: a theoretical and experimental analysis Brain Res. 546 1991 18 32
55. H. Thoenen, Y.A. Barde, A.M. Davies, and J.E. Johnson Neurotrophic factors and neuronal death Ciba Found. Symp. 126 1987 82 95
56. D.R. Tomlinson, G.B. Willars, and E.F. Calthrop-Owen Defects of axonal transport in experimental diabetes that are unrelated to the sorbitol pathway Exp. Neurol. 96 1987 194 202
57. D.R. Tomlinson, P. Fernyhough, and L.T. Diemel Neurotrophins and peripheral neuropathy Philos. Trans. R. Soc. London, Ser. B Biol. Sci. 351 1996 455 462
58. D.R. Tomlinson, P. Fernyhough, L.T. Diemel, and K. Maeda Deficient neurotrophic support in the aetiology of diabetic neuropathy Diabet. Med. 13 1996 679 681
59. D.R. Tomlinson, P. Fernyhough, and L.T. Diemel Role of neurotrophins in diabetic neuropathy and treatment with nerve growth factors Diabetes 46 Suppl. 2 1997 S43 S49
60. D.E. Wright, J.M. Ryals, K.E. McCarson, and J.A. Christianson Diabetes-induced expression of activating transcription factor 3 in mouse primary sensory neurons J. Peripher. Nerv. Sys. 9 2004 242 254
61. L. Yang, C.C. Voytek, and T.P. Margolis Immunohistochemical analysis of primary sensory neurons latently infected with herpes simplex virus type 1 J. Virol. 74 2000 209 217
62. Y.H. Zhang, M.R. Vasko, and G.D. Nicol Ceramide, a putative second messenger for nerve growth factor, modulates the TTX-resistant Na(+) current and delayed rectifier K(+) current in rat sensory neurons J. Physiol. 544 2002 385 402
63. F.Q. Zhou, J. Zhou, S. Dedhar, Y.H. Wu, and W.D. Snider NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC Neuron 42 2004 897 912