Phosphodiesterase-5 is a therapeutic target for peripheral neuropathy in diabetic mice

Neuroscience

Volumn 193, Issue , 2011, Pages 399-410

  Wang, L ^a   Chopp, M ^a,b   Szalad, A ^a   Liu, Z ^a   Bolz, M ^a   Alvarez F M ^a   Lu, M ^a   Zhang, L ^a   Cui, Y ^a   Zhang, R L ^a   Zhang, Z G ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

Author keywords

Diabetes; Function; Mice; PDE5; Peripheral neuropathy; Sildenafil

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; KT 5823; MYELIN BASIC PROTEIN; PHOSPHODIESTERASE V; PROTEIN KINASE G I; SILDENAFIL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG INHIBITION; ENZYME REGULATION; HYPERGLYCEMIA; IN VITRO STUDY; MALE; MORPHOMETRICS; MOTOR NERVE CONDUCTION; MOUSE; MYELIN SHEATH; NERVE STIMULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SCHWANN CELL; SCIATIC NERVE; SENSORY NERVE CONDUCTION; TREATMENT RESPONSE;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; BROMODEOXYURIDINE; CELLS, CULTURED; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 5; DIABETES COMPLICATIONS; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURAL CONDUCTION; PAIN MEASUREMENT; PAIN THRESHOLD; PHOSPHODIESTERASE 5 INHIBITORS; PIPERAZINES; PURINES; RECEPTORS, LEPTIN; RNA, SMALL INTERFERING; SCHWANN CELLS; SCIATIC NEUROPATHY; SULFONES; TIME FACTORS; TRANSFECTION;

EID: 80052492279     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.07.039     Document Type: Article

References (56)

1. Acheampong E.A., Roschel C., Mukhtar M., Srinivasan A., Rafi M., Pomerantz R.J., Parveen Z. Combined effects of hyperglycemic conditions and HIV-1 Nef: a potential model for induced HIV neuropathogenesis. Virol J 2009, 6:183.
2. Arora N., Kumar D., Veerareddy S., Langston W., Patel R., Kevil C. Sildenafil enhances angiogenesis and blood flow in response to ischemia in diabetic mice. FASEB J 2007, 21:7066.
3. Ayala J.E., Bracy D.P., Julien B.M., Rottman J.N., Fueger P.T., Wasserman D.H. Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice. Diabetes 2007, 56:1025-1033.
4. Ballin R.H., Thomas P.K. Hypertrophic changes in diabetic neuropathy. Acta Neuropathol 1968, 11:93-102.
5. Bhatheja K., Field J. Schwann cells: origins and role in axonal maintenance and regeneration. Int J Biochem Cell Biol 2006, 38:1995-1999.
6. Bianchi R., Buyukakilli B., Brines M., Savino C., Cavaletti G., Oggioni N., Lauria G., Borgna M., Lombardi R., Cimen B., Comelekoglu U., Kanik A., Tataroglu C., Cerami A., Ghezzi P. Erythropoietin both protects from and reverses experimental diabetic neuropathy. Proc Natl Acad Sci U S A 2004, 101:823-828.
7. Brownlee M., Vlassara H., Cerami A. Trapped immunoglobulins on peripheral nerve myelin from patients with diabetes mellitus. Diabetes 1986, 35:999-1003.
8. Butt E., Geiger J., Jarchau T., Lohmann S.M., Walter U. The cGMP-dependent protein kinase-gene, protein, and function. Neurochem Res 1993, 18:27-42.
9. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.
10. Cheng H.T., Dauch J.R., Hayes J.M., Hong Y., Feldman E.L. Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes. J Neuropathol Exp Neurol 2009, 68:1229-1243.
11. Corbin J.D., Francis S.H. Cyclic GMP phosphodiesterase-5: target of sildenafil. J Biol Chem 1999, 274:13729-13732.
12. Di Scipio F., Raimondo S., Tos P., Geuna S. A simple protocol for paraffin-embedded myelin sheath staining with osmium tetroxide for light microscope observation. Microsc Res Tech 2008, 71:497-502.
13. Dixon W.J. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980, 20:441-462.
14. Farhadi H.F., Lepage P., Forghani R., Friedman H.C., Orfali W., Jasmin L., Miller W., Hudson T.J., Peterson A.C. A combinatorial network of evolutionarily conserved myelin basic protein regulatory sequences confers distinct glial-specific phenotypes. J Neurosci 2003, 23:10214-10223.
15. Feldman E.L., Stevens M.J., Greene D.A. Pathogenesis of diabetic neuropathy. Clin Neurosci 1997, 4:365-370.
16. Foster R.E., Whalen C.C., Waxman S.G. Reorganization of the axon membrane in demyelinated peripheral nerve fibers: morphological evidence. Science 1980, 210:661-663.
17. Ginalski-Winkelmann H., Omlin F.X., Matthieu J.M. Myelin basic protein deficit in the PNS of mld mutant mice recovers during development. Dev Neurosci 1983, 6:118-126.
18. Greene D.A., Sima A.A., Stevens M.J., Feldman E.L., Lattimer S.A. Complications: neuropathy, pathogenetic considerations. Diabetes Care 1992, 15:1902-1925.
19. Gumy L.F., Bampton E.T., Tolkovsky A.M. Hyperglycaemia inhibits Schwann cell proliferation and migration and restricts regeneration of axons and Schwann cells from adult murine DRG. Mol Cell Neurosci 2008, 37:298-311.
20. Hackett G. PDE5 inhibitors in diabetic peripheral neuropathy. Int J Clin Pract 2006, 60:1123-1126.
21. Honkanen H., Lahti O., Nissinen M., Myllylä R.M., Kangas S., Päiväläinen S., Alanne M.H., Peltonen S., Peltonen J., Heape A.M. Isolation, purification and expansion of myelination-competent, neonatal mouse Schwann cells. Eur J Neurosci 2007, 26:953-964.
22. Ignarro L.J. Heme-dependent activation of guanylate cyclase by nitric oxide: a novel signal transduction mechanism. Blood Vessels 1991, 28:67-73.
23. Ii M., Nishimura H., Kusano K.F., Qin G., Yoon Y.S., Wecker A., Asahara T., Losordo D.W. Neuronal nitric oxide synthase mediates statin-induced restoration of vasa nervorum and reversal of diabetic neuropathy. Circulation 2005, 112:93-102.
24. Jackson G., Benjamin N., Jackson N., Allen M.J. Effects of sildenafil citrate on human hemodynamics. Am J Cardiol 1999, 83:13C-20C.
25. Kakinoki B., Sekimoto S., Yuki S., Ohgami T., Sejima M., Yamagami K., Saito K. Orally active neurotrophin-enhancing agent protects against dysfunctions of the peripheral nerves in hyperglycemic animals. Diabetes 2006, 55:616-621.
26. Leonelli E., Bianchi R., Cavaletti G., Caruso D., Crippa D., Garcia-Segura L.M., Lauria G., Magnaghi V., Roglio I., Melcangi R.C. Progesterone and its derivatives are neuroprotective agents in experimental diabetic neuropathy: a multimodal analysis. Neuroscience 2007, 144:1293-1304.
27. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
28. Lohmann S.M., Vaandrager A.B., Smolenski A., Walter U., De Jonge H.R. Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem Sci 1997, 22:307-312.
29. Mousa S.A., Zhang Q., Sitte N., Ji R., Stein C. Beta-endorphin-containing memory-cells and mu-opioid receptors undergo transport to peripheral inflamed tissue. J Neuroimmunol 2001, 115:71-78.
30. Päiväläinen S., Nissinen M., Honkanen H., Lahti O., Kangas S.M., Peltonen J., Peltonen S., Heape A.M. Myelination in mouse dorsal root ganglion/Schwann cell cocultures. Mol Cell Neurosci 2008, 37:568-578.
31. Patil C.S., Singh V.P., Singh S., Kulkarni S.K. Modulatory effect of the PDE-5 inhibitor sildenafil in diabetic neuropathy. Pharmacology 2004, 72:190-195.
32. Pfeifer A., Ruth P., Dostmann W., Sausbier M., Klatt P., Hofmann F. Structure and function of cGMP-dependent protein kinases. Rev Physiol Biochem Pharmacol 1999, 135:105-149.
33. Pittenger G.L., Burcus N.I., McNulty P., Basta B., Vinik A.I. Intraepidermal nerve fibers are indicators of small-fiber neuropathy in both diabetic and nondiabetic patients. Diabetes Care 2004, 27(8):1974-1979. RM.
34. Russell J.W., Golovoy D., Vincent A.M., Mahendru P., Olzmann J.A., Mentzer A., Feldman E.L. High glucose-induced oxidative stress and mitochondrial dysfunction in neurons. FASEB J 2002, 16:1738-1748.
35. Sameni H.R., Panahi M., Sarkaki A., Saki G.H., Makvandi M. The neuroprotective effects of progesterone on experimental diabetic neuropathy in rats. Pak J Biol Sci 2008, 11:1994-2000.
36. Scott J.N., Clark A.W., Zochodne D.W. Neurofilament and tubulin gene expression in progressive experimental diabetes: failure of synthesis and export by sensory neurons. Brain 1999, 122(Pt 11):2109-2118.
37. Shirasaki N., Rosenbluth J. Structural abnormalities in freeze-fractured sciatic nerve fibres of diabetic mice. J Neurocytol 1991, 20:573-584.
38. Smith A.G., Howard J.R., Kroll R., Ramachandran P., Hauer P., Singleton J.R., McArthur J. The reliability of skin biopsy with measurement of intraepidermal nerve fiber density. J Neurol Sci 2005, 228:65-69.
39. South S.M., Smith M.T. Apparent insensitivity of the hotplate latency test for detection of antinociception following intraperitoneal, intravenous or intracerebroventricular M6G administration to rats. J Pharmacol Exp Ther 1998, 286:1326-1332.
40. Sullivan K.A., Hayes J.M., Wiggin T.D., Backus C., Su Oh S., Lentz S.I., Brosius F., Feldman E.L. Mouse models of diabetic neuropathy. Neurobiol Dis 2007, 28:276-285.
41. Thippeswamy T., McKay J.S., Morris R., Quinn J., Wong L.F., Murphy D. Glial-mediated neuroprotection: evidence for the protective role of the NO-cGMP pathway via neuron-glial communication in the peripheral nervous system. Glia 2005, 49:197-210.
42. Tolwani R.J., Cosgaya J.M., Varma S., Jacob R., Kuo L.E., Shooter E.M. BDNF overexpression produces a long-term increase in myelin formation in the peripheral nervous system. J Neurosci Res 2004, 77:662-669.
43. Trojaborg W., Hays A.P., van den Berg L., Younger D.S., Latov N. Motor conduction parameters in neuropathies associated with anti-MAG antibodies and other types of demyelinating and axonal neuropathies. Muscle Nerve 1995, 18:730-735.
44. Vanderah T.W., Suenaga N.M., Ossipov M.H., Malan T.P., Lai J., Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J Neurosci 2001, 21:279-286.
45. Vincent A.M., McLean L.L., Backus C., Feldman E.L. Short-term hyperglycemia produces oxidative damage and apoptosis in neurons. FASEB J 2005, 19:638-640.
46. Walker D.K., Ackland M.J., James G.C., Muirhead G.J., Rance D.J., Wastall P., Wright P.A. Pharmacokinetics and metabolism of sildenafil in mouse, rat, rabbit, dog and man. Xenobiotica 1999, 29:297-310.
47. Walwyn W.M., Matsuka Y., Arai D., Bloom D.C., Lam H., Tran C., Spigelman I., Maidment N.T. HSV-1-mediated NGF delivery delays nociceptive deficits in a genetic model of diabetic neuropathy. Exp Neurol 2006, 198:260-270.
48. Wang L., Gang Zhang Z., Lan Zhang R., Chopp M. Activation of the PI3-K/Akt pathway mediates cGMP enhanced-neurogenesis in the adult progenitor cells derived from the subventricular zone. J Cereb Blood Flow Metab 2005, 25:1150-1158.
49. Wang L., Zhang Z.G., Zhang R.L., Gregg S.R., Hozeska-Solgot A., LeTourneau Y., Wang Y., Chopp M. Matrix metalloproteinase 2 (MMP2) and MMP9 secreted by erythropoietin-activated endothelial cells promote neural progenitor cell migration. J Neurosci 2006, 26:5996-6003.
50. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J Neurochem 1997, 68:443-456.
51. Wright D.E., Johnson M.S., Arnett M.G., Smittkamp S.E., Ryals J.M. Selective changes in nocifensive behavior despite normal cutaneous axon innervation in leptin receptor-null mutant (db/db) mice. J Peripher Nerv Syst 2007, 12:250-261.
52. Yagihashi S., Kamijo M., Watanabe K. Reduced myelinated fiber size correlates with loss of axonal neurofilaments in peripheral nerve of chronically streptozotocin diabetic rats. Am J Pathol 1990, 136:1365-1373.
53. Yamauchi J., Chan J.R., Shooter E.M. Neurotrophins regulate Schwann cell migration by activating divergent signaling pathways dependent on Rho GTPases. Proc Natl Acad Sci U S A 2004, 101:8774-8779.
54. Zhang J.Y., Luo X.G., Xian C.J., Liu Z.H., Zhou X.F. Endogenous BDNF is required for myelination and regeneration of injured sciatic nerve in rodents. Eur J Neurosci 2000, 12:4171-4180.
55. Zhang R., Zhang L., Zhang Z., Wang Y., Lu M., Lapointe M., Chopp M. A nitric oxide donor induces neurogenesis and reduces functional deficits after stroke in rats. Ann Neurol 2001, 50:602-611.
56. Zhuo M., Hu Y., Schultz C., Kandel E.R., Hawkins R.D. Role of guanylyl cyclase and cGMP-dependent protein kinase in long-term potentiation. Nature 1994, 368:635-639.