Mouse models of diabetic neuropathy

ILAR Journal

Volumn 54, Issue 3, 2014, Pages 259-272

  O'brien, Phillipe D ^a   Sakowski, Stacey A ^a   Feldman, Eva L ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Diabetic peripheral neuropathy; Diet induced obesity; Leptin; Mouse models; Nerve conduction velocity; Nerve fiber density; Type 1 diabetes; Type 2 diabetes

Indexed keywords

ANIMAL; COMPLICATION; DIABETIC NEUROPATHIES; DISEASE MODEL; DYSLIPIDEMIA; GENETICS; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; DYSLIPIDEMIAS; INSULIN RESISTANCE; MICE;

EID: 84897894276     PISSN: 10842020     EISSN: 19306180     Source Type: Journal    
DOI: 10.1093/ilar/ilt052     Document Type: Article

References (111)

1. Aaberg ML, Burch DM, Hud ZR, Zacharias MP. 2008. Gender differences in the onset of diabetic neuropathy. J Diabetes Complications 22:83-87.
2. Apfel SC, Asbury AK, Bril V, Burns TM, Campbell JN, Chalk CH, Dyck PJ, Feldman EL, Fields HL, Grant IA, Griffin JW, Klein CJ, Lindblom U, LitchyWJ, Low PA,MelansonM,Mendell JR, MerrenMD, O'brien PC, Rendell M, Rizza RA, Service FJ, Thomas PK, Walk D, Wang AK, Wessel K,Windebank AJ, Ziegler D, Zochodne DW. 2001. Positive neuropathic sensory symptoms as endpoints in diabetic neuropathy trials. J Neurol Sci 189:3-5.
3. Arulmozhi DK, Kurian R, Bodhankar SL, Veeranjaneyulu A. 2008. Metabolic effects of various antidiabetic and hypolipidaemic agents on a high-fat diet and multiple low-dose streptozocin (MLDS) mouse model of diabetes. J Pharm Pharmacol 60:1167-1173.
4. Beiswenger KK, Calcutt NA, Mizisin AP. 2008. Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice. Neurosci Lett 442:267-272.
5. Bolzan AD, Bianchi MS. 2002. Genotoxicity of streptozotocin. Mutat Res 512:121-134.
6. Brehm MA, Powers AC, Shultz LD, Greiner DL. 2012. Advancing animal models of human type 1 diabetes by engraftment of functional human tissues in immunodeficient mice. Cold Spring Harb Perspect Med 2: a007757.
7. Britland ST, Young RJ, Sharma AK, Clarke BF. 1990. Relationship of endoneurial capillary abnormalities to type and severity of diabetic polyneuropathy. Diabetes 39:909-913.
8. Brussee V, Guo G, Dong Y, Cheng C, Martinez JA, Smith D, Glazner GW, Fernyhough P, Zochodne DW. 2008. Distal degenerative sensory neuropathy in a long-term type 2 diabetes rat model. Diabetes 57:1664-1673.
9. Buettner R, Parhofer KG, Woenckhaus M, Wrede CE, Kunz-Schughart LA, Scholmerich J, Bollheimer LC. 2006. Defining high-fat-diet rat models: Metabolic and molecular effects of different fat types. J Mol Endocrinol 36:485-501.
10. Callaghan B, Cheng HT, Stables CL, Smith AL, Feldman EL. 2012. Diabetic neuropathy: Clinical manifestations and current treatments. Lancet Neurol 11:521-534.
11. Callaghan BC, Hur J, Feldman EL. 2012. Diabetic neuropathy: One disease or two? Curr Opin Neurol 25:536-541.
12. Cederroth CR, Vinciguerra M, Kuhne F, Madani R, Doerge DR, Visser TJ, Foti M, Rohner-Jeanrenaud F, Vassalli JD, Nef S. 2007. A phytoestrogenrich diet increases energy expenditure and decreases adiposity in mice. Environ Health Perspect 115:1467-1473
13. [CDC] Centers for Disease Control and Prevention 2011. National Diabetes Fact Sheet: National Estimates and General Information on Diabetes and Prediabetes in the United States, 2011. Atlanta GA: US Department of Health and Human Services, Centers for Disease Control and Prevention.
14. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. 1994. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
15. Chen YS, Chung SS, Chung SK. 2005. Noninvasive monitoring of diabetes-induced cutaneous nerve fiber loss and hypoalgesia in thy1-YFP transgenic mice. Diabetes 54:3112-3118.
16. Cheng HT, Dauch JR, Hayes JM, Hong Y, Feldman EL. 2009. Nerve growth factor mediates mechanical allodynia in a mouse model of type 2 diabetes. J Neuropathol Exp Neurol 68:1229-1243.
17. Choeiri C, Hewitt K, Durkin J, Simard CJ, Renaud JM, Messier C. 2005. Longitudinal evaluation of memory performance and peripheral neuropathy in the Ins2C96YAkita mice. Behav Brain Res 157:31-38.
18. Clee SM, Nadler ST, Attie AD. 2005. Genetic and genomic studies of the BTBR ob/ob mouse model of type 2 diabetes. Am J Ther 12:491-498.
19. Coppey L, Davidson E, Lu B, Gerard C, Yorek M. 2011. Vasopeptidase inhibitor ilepatril (AVE7688) prevents obesity- and diabetes-induced neuropathy in C57Bl/6J mice. Neuropharmacology 60:259-266.
20. Coppey L, Lu B, Gerard C, Yorek MA. 2012. Effect of inhibition of angiotensin- converting enxyme and/or neutral endopeptidase on neuropathy in high-fat-fed C57BL/6J mice. J Obes 2012:326806
21. Dauch JR, Bender DE, Luna-Wong LA, Hsieh W, Yanik BM, Kelly ZA, Cheng HT 2013. Neurogenic factor-induced Langerhans cell activation in diabetic mice with mechanical allodynia. J Neuroinflammation 10:64.
22. Dauch JR, Yanik BM, Hsieh W, Oh SS, Cheng HT. 2012. Neuron-astrocyte signaling network in spinal cord dorsal horn mediates painful neuropathy of type 2 diabetes. Glia 60:1301-1315.
23. Delovitch TL, Singh B. 1997. The nonobese diabetic mouse as a model of autoimmune diabetes: immune dysregulation gets the NOD. Immunity 7:727-738.
24. Demiot C, Tartas M, Fromy B, Abraham P, Saumet JL, Sigaudo-Roussel D. 2006. Aldose reductase pathway inhibition improved vascular and C-fiber functions, allowing for pressure-induced vasodilation restoration during severe diabetic neuropathy. Diabetes 55:1478-1483.
25. Dillingham TR, Pezzin LE, Shore AD. 2005. Reamputation, mortality, and health care costs among persons with dysvascular lower-limb amputations. Arch Phys Med Rehabil 86:480-486.
26. Drel VR, Mashtalir N, Ilnytska O, Shin J, Li F, Lyzogubov VV, Obrosova IG. 2006. The leptin-deficient (ob/ob) mouse: A new animal model of peripheral neuropathy of type 2 diabetes and obesity. Diabetes 55:3335-3343.
27. Drel VR, Pacher P, Stavniichuk R, Xu W, Zhang J, Kuchmerovska TM, Slusher B, Obrosova IG. 2011. Poly(ADP-ribose)polymerase inhibition counteracts renal hypertrophy and multiple manifestations of peripheral neuropathy in diabetic Akita mice. Int J Mol Med 28:629-35.
28. Eizirik DL, Miani M, Cardozo AK. 2013. Signalling danger: Endoplasmic reticulum stress and the unfolded protein response in pancreatic islet inflammation. Diabetologia 56:234-241.
29. Elias KA, Cronin MJ, Stewart TA, Carlsen RC. 1998. Peripheral neuropathy in transgenic diabetic mice: Restoration of C-fiber function with human recombinant nerve growth factor. Diabetes 47:1637-1642.
30. Fagerberg SE. 1959. Diabetic neuropathy: A clinical and histological study on the significance of vascular affections. Acta Med Scand Suppl 345:1-97.
31. Gabra BH, Sirois P. 2005. Hyperalgesia in non-obese diabetic (NOD) mice: A role for the inducible bradykinin B1 receptor. Eur J Pharmacol 514:61-67.
32. Geraldes P, King GL. 2010. Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res 106:1319-1331.
33. Ghibaudi L, Cook J, Farley C, van Heek M, Hwa JJ. 2002. Fat intake affects adiposity, comorbidity factors, and energy metabolism of spraguedawley rats. Obes Res 10:956-963.
34. Guilford BL, Ryals JM, Wright DE. 2011. Phenotypic changes in diabetic neuropathy induced by a high-fat diet in diabetic C57BL/6 mice. Exp Diabetes Res 2011:848307.
35. Hinder LM, Vincent AM, Burant CF, Pennathur S, Feldman EL. 2012. Bioenergetics in diabetic neuropathy: What we need to know. J Peripher Nerv Syst 17:10-14.
36. Hinder LM, Vincent AM, Hayes JM, Mc Lean LL, Feldman EL. 2013. Apolipoprotein E knockout as the basis for mouse models of dyslipidemia-induced neuropathy. Exp Neurol 239:102-110.
37. Homs J, Ariza L, Pages G, Verdu E, Casals L, Udina E, Chillon M, Bosch A, Navarro X. 2011. Comparative study of peripheral neuropathy and nerve regeneration in NOD and ICR diabetic mice. J Peripher Nerv Syst 16:213-227
38. Ii M, Nishimura H, Kusano KF, Qin G, Yoon YS, Wecker A, Asahara T, Losordo DW 2005. Neuronal nitric oxide synthase mediates statin-induced restoration of vasa nervorum and reversal of diabetic neuropathy. Circulation 112:93-102.
39. Ikemoto S, Takahashi M, Tsunoda N, Maruyama K, Itakura H, Ezaki O. 1996. High-fat diet-induced hyperglycemia and obesity in mice: Differential effects of dietary oils. Metabolism 45:1539-1546.
40. International Diabetes Federation. 2012. IDF Diabetes Atlas, 5th ed. Brussels Belgium: International Diabetes Federation.
41. Ize-Ludlow D, Lightfoot YL, Parker M, Xue S, Wasserfall C, Haller MJ, Schatz D, Becker DJ, Atkinson MA, Mathews CE. 2011. Progressive erosion of beta-cell function precedes the onset of hyperglycemia in the NOD mouse model of type 1 diabetes. Diabetes 60:2086-2091.
42. Jack M, Wright D. 2012. Role of advanced glycation endproducts and glyoxalase I in diabetic peripheral sensory neuropathy. Transl Res 159:355-365.
43. Jack MM, Ryals JM, Wright DE. 2012. Protection from diabetes-induced peripheral sensory neuropathy-a role for elevated glyoxalase I?. Exp Neurol 234:62-69.
44. Johnson MS, Ryals JM,Wright DE. 2008. Early loss of peptidergic intraepidermal nerve fibers in an STZ-induced mouse model of insensate diabetic neuropathy. Pain 140:35-47.
45. Kakoki M, Sullivan KA, Backus C, Hyes JM, Oh SS, Hua K, Gasim AM, Tomita H, Grant R, Nossov SB, Kim HS, Jennette JC, Feldman EL, Smithies O. 2010. Lack of both bradykinin B1 and B2 receptors enhances nephropathy, neuropathy, and bone mineral loss in Akita diabetic mice. Proc Natl Acad Sci U S A 107:10190-10195.
46. Kan M, Guo G, Singh B, Singh V, Zochodne DW. 2012. Glucagon-like peptide 1, insulin, sensory neurons, and diabetic neuropathy. J Neuropathol Exp Neurol 71:494-510.
47. Karabatas L, Oliva ME, Dascal E, Hein GJ, Pastorale C, Chicco A, Lombardo YB, Basabe JC. 2010. Is Lipotoxicity presents in the early stages of an experimental model of autoimmune diabetes? Further studies in the multiple low dose of streptozotocin model. Islets 2:190-199.
48. Kellogg AP, Pop-Busui R. 2005. Peripheral nerve dysfunction in experimental diabetes is mediated by cyclooxygenase-2 and oxidative stress. Antioxid Redox Signal 7:1521-1529.
49. Kellogg AP, Wiggin TD, Larkin DD, Hayes JM, Stevens MJ, Pop-Busui R. 2007. Protective effects of cyclooxygenase-2 gene inactivation against peripheral nerve dysfunction and intraepidermal nerve fiber loss in experimental diabetes. Diabetes 56:2997-3005.
50. Kennedy JM, Zochodne DW. 2005. Experimental diabetic neuropathy with spontaneous recovery: Is there irreparable damage?. Diabetes 54: 830-837.
51. Kim B, Feldman EL. 2012. Insulin resistance in the nervous system. Trends Endocrinol Metab 23:133-141.
52. Korngut L, Ma CH, Martinez JA, Toth CC, Guo GF, Singh V, Woolf CJ, Zochodne DW. 2012. Overexpression of human HSP27 protects sensory neurons from diabetes. Neurobiol Dis 47:436-443.
53. Kountz D. 2012. Special considerations of care and risk management for African American patients with type 2 diabetes mellitus. J Natl Med Assoc 104:265-273.
54. Kusano KF, Allendoerfer KL, MungerW, Pola R, Bosch-MarceM, Kirchmair R, Yoon YS, Curry C, Silver M, Kearney M, Asahara T, Losordo DW. 2004. Sonic hedgehog induces arteriogenesis in diabetic vasa nervorum and restores function in diabetic neuropathy. Arterioscler Thromb Vasc Biol 24:2102-2107.
55. Leiter EH. 1982. Multiple low-dose streptozotocin-induced hyperglycemia and insulitis in C57BL mice: Influence of inbred background, sex, and thymus. Proc Natl Acad Sci U S A 79:630-634.
56. Leiter EH. 1989. The genetics of diabetes susceptibility in mice. Faseb J 3:2231-2241.
57. Leiter EH. 2001. The NOD mouse: A model for insulin-dependent diabetes mellitus. Curr Protoc Immunol 15: 15.9.
58. Leiter EH, Reifsnyder PC. 2004. Differential levels of diabetogenic stress in two new mouse models of obesity and type 2 diabetes. Diabetes 53: S4-S11.
59. Li F, Drel VR, Szabo C, Stevens MJ, Obrosova IG. 2005. Low-dose poly (ADP-ribose) polymerase inhibitor-containing combination therapies reverse early peripheral diabetic neuropathy. Diabetes 54:1514-1522.
60. Li F, Szabo C, Pacher P, Southan GJ, Abatan OI, Charniauskaya T, Stevens MJ, Obrosova IG. 2004. Evaluation of orally active poly (ADP-ribose) polymerase inhibitor in streptozotocin-diabetic rat model of early peripheral neuropathy. Diabetologia 47:710-717.
61. Luo J, Quan J, Tsai J, Hobensack CK, Sullivan C, Hector R, Reaven GM. 1998. Nongenetic mouse models of non-insulin-dependent diabetes mellitus. Metabolism 47:663-668.
62. Lupachyk S, Watcho P, Obrosov AA, Stavniichuk R, Obrosova IG. 2013. Endoplasmic reticulum stress contributes to prediabetic peripheral neuropathy. Exp Neurol 247:342-348.
63. Lupachyk S,Watcho P, Stavniichuk R, Shevalye H, Obrosova IG. 2013. Endoplasmic reticulum stress plays a key role in the pathogenesis of diabetic peripheral neuropathy. Diabetes 62:944-952.
64. Malik RA, Veves A, Masson EA, Sharma AK, Ah-See AK, Schady W, Lye RH, Boulton AJ. 1992. Endoneurial capillary abnormalities in mild human diabetic neuropathy. J Neurol Neurosurg Psychiatry 55:557-561.
65. Manchem VP, Goldfine ID, Kohanski RA, Cristobal CP, Lum RT, Schow SR, Shi S, Spevak WR, Laborde E, Toavs DK, Villar HO, Wick MM, Kozlowski MR. 2001. A novel small molecule that directly sensitizes the insulin receptor in vitro and in vivo. Diabetes 50:824-830.
66. Mc Evoy RC, Andersson J, Sandler S, Hellerstrom C. 1984. Multiple lowdose streptozotocin-induced diabetes in the mouse. Evidence for stimulation of a cytotoxic cellular immune response against an insulinproducing beta cell line. J Clin Invest 74:715-722.
67. Mensah-Brown EP, Stosic Grujicic S, Maksimovic D, Jasima A, Shahin A, Lukic ML. 2002. Downregulation of apoptosis in the target tissue prevents low-dose streptozotocin-induced autoimmune diabetes. Mol Immunol 38:941-946.
68. Muller A, Schott-Ohly P, Dohle C, Gleichmann H. 2002. Differential regulation of Th1-type and Th2-type cytokine profiles in pancreatic islets of C57BL/6 and BALB/c mice by multiple low doses of streptozotocin. Immunobiology 205:35-50.
69. Muller KA, Ryals JM, Feldman EL,Wright DE. 2008. Abnormal muscle spindle innervation and large-fiber neuropathy in diabetic mice. Diabetes 57:1693-1701.
70. Oates PJ. 2002. Polyol pathway and diabetic peripheral neuropathy. Int Rev Neurobiol 50:325-392.
71. Obrosova IG, Ilnytska O, Lyzogubov VV, Pavlov IA, Mashtalir N, Nadler JL, Drel VR. 2007. High-fat diet induced neuropathy of pre-diabetes and obesity: Effects of "healthy" diet and aldose reductase inhibition. Diabetes 56:2598-2608.
72. Obrosova IG, Mabley JG, Zsengeller Z, Charniauskaya T, Abatan OI, Groves JT, Szabo C. 2005. Role for nitrosative stress in diabetic neuropathy: Evidence from studies with a peroxynitrite decomposition catalyst. Faseb J 19:401-403.
73. Pittenger GL, Ray M, Burcus NI, Mc Nulty P, Basta B, Vinik AI. 2004. Intraepidermal nerve fibers are indicators of small-fiber neuropathy in both diabetic and nondiabetic patients. Diabetes Care 27:1974-1979.
74. Quattrini C, Tavakoli M, Jeziorska M, Kallinikos P, Tesfaye S, Finnigan J, Marshall A, Boulton AJ, Efron N, Malik RA. 2007. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 56:2148-2154.
75. Reifsnyder PC, Churchill G, Leiter EH. 2000. Maternal environment and genotype interact to establish diabesity in mice. Genome Res 10:1568-1578.
76. Schmidt RE, Feng D, Wang Q, Green KG, Snipes LL, Yamin M, Brines M. 2011. Effect of insulin and an erythropoietin-derived peptide (ARA290) on established neuritic dystrophy and neuronopathy in Akita (Ins2 Akita) diabetic mouse sympathetic ganglia. Exp Neurol 232:126-135.
77. Schratzberger P, Walter DH, Rittig K, Bahlmann FH, Pola R, Curry C, Silver M, Krainin JG,Weinberg DH, Ropper AH, Isner JM. 2001. Reversal of experimental diabetic neuropathy by VEGF gene transfer. J Clin Invest 107:1083-1092.
78. Shi TJ, Zhang MD, Zeberg H, Nilsson J, Grünler J, Liu SX, Xiang Q, Persson J, Fried KJ, Catrina SB, Watanabe M, Arhem P, Brismar K, Hökfelt TG. Coenzyme Q10 prevents peripheral neuropathy and attenuates neuron loss in the db-/db- mouse, a type 2 diabetes model. Proc Natl Acad Sci U S A 110:690-695.
79. Sima AA, Robertson DM. 1978. Peripheral neuropathy in mutant diabetic mouse [C57BL/Ks (db/db)]. Acta Neuropathol 41: 85-89
80. Singleton JR, Smith AG, Bromberg MB. 2001. Painful sensory polyneuropathy associated with impaired glucose tolerance.Muscle Nerve 24:1225-1228.
81. Stavniichuk R, Drel VR, Shevalye H, Vareniuk I, Stevens MJ, Nadler JL, Obrosova IG. 2010. Role of 12/15-lipoxygenase in nitrosative stress and peripheral prediabetic and diabetic neuropathies. Free Radic Biol Med 49:1036-1045.
82. Sugano M, Yamato H, Hayashi T, Ochiai H, Kakuchi J, Goto S, Nishijima F, Iino N, Kazama JJ, Takeuchi T, Mokuda O, Ishikawa T, Okazaki R. 2006. High-fat diet in low-dose-streptozotocin-treated heminephrectomized rats induces all features of human type 2 diabetic nephropathy: A new rat model of diabetic nephropathy. Nutr Metab Cardiovasc Dis 16:477-484.
83. Sullivan KA, Hayes JM, Wiggin TD, Backus C, Su Oh S, Lentz SI, Brosius F 3rd, Feldman EL. 2007. Mouse models of diabetic neuropathy. Neurobiol Dis 28:276-285.
84. Sullivan KA, Lentz SI, Roberts JL Jr, Feldman EL. 2008. Criteria for creating and assessing mouse models of diabetic neuropathy. Curr Drug Targets 9:3-13.
85. Surwit RS, Wang S, Petro AE, Sanchis D, Raimbault S, Ricquier D, Collins S. 1998. Diet-induced changes in uncoupling proteins in obesity-prone and obesity-resistant strains of mice. Proc Natl Acad Sci U S A 95:4061-4065.
86. Tam J, Rosenberg L, Maysinger D. 2004. INGAP peptide improves nerve function and enhances regeneration in streptozotocin-induced diabetic C57BL/6 mice. FASAB J 18:1767-1769
87. Tesfaye S, Boulton AJ, Dyck PJ, Freeman R, Horowitz M, Kempler P, Lauria G, Malik RA, Spallone V, Vinik A, Bernardi L, Valensi P 2010. Diabetic neuropathies: Update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 33:2285-2293.
88. Tesfaye S, Malik R, Ward JD. 1994. Vascular factors in diabetic neuropathy. Diabetologia 37:847-854.
89. Timperley WR, Ward JD, Preston FE, Duckworth T, O'malley BC. 1976. A reassessment of vascular factors in relation to intravascular coagulation. Diabetologia 12:237-243.
90. Toth C, Rong LL, Yang C, Martinez J, Song F, Ramji N, Brussee V, Liu W, Durand J, Nguyen MD, Schmidt AM, Zochodne DW. 2008. Receptor for advanced glycation end products (RAGEs) and experimental diabetic neuropathy. Diabetes 57: 1002-1017.
91. Van Belle TL, Taylor P, von Herrath MG. 2009. Mouse models for type 1 diabetes. Drug Discov Today Dis Models 6:41-45.
92. Vareniuk I, Pavlov IA, Drel VR, Lyzogubov VV, Ilnytska O, Bell SR, Tibrewala J, Groves JT, Obrosova IG. 2007. Nitrosative stress and peripheral diabetic neuropathy in leptin-deficient (ob/ob) mice. Exp Neurol 205:425-436.
93. Ventura-Sobrevilla J, Boone-Villa VD, Aguilar CN, Roman-Ramos R, Vega-Avila E, Campos-Sepulveda E, Alarcon-Aguilar F. 2011. Effect of varying dose and administration of streptozotocin on blood sugar in male CD1 mice. ProcWest Pharmacol Soc 54:5-9.
94. Vincent AM, Callaghan BC, Smith AL, Feldman EL. 2011. Diabetic neuropathy: Cellular mechanisms as therapeutic targets. Nat Rev Neurol 7:573-583.
95. Vincent AM, Hayes JM, Mc Lean LL, Vivekanandan-Giri A, Pennathur S, Feldman EL. 2009. Dyslipidemia-induced neuropathy in mice: The role of oxLDL/LOX-1. Diabetes 58:2376-2385.
96. Vincent AM, Hinder LM, Pop-Busui R, Feldman EL. 2009. Hyperlipidemia: A new therapeutic target for diabetic neuropathy. J Peripher Nerv Syst 14:257-267.
97. Vincent AM, Russell JW, Sullivan KA, Backus C, Hayes JM, Mc Lean LL, Feldman EL. 2007. SOD2 protects neurons from injury in cell culture and animal models of diabetic neuropathy. Exp Neurol 208:216-227.
98. Wang H, Storlien LH, Huang XF. 2002. Effects of dietary fat types on body fatness, leptin, and ARC leptin receptor, NPY, and AgRP mRNA expression. Am J Physiol Endocrinol Metab 282:E1352-1359.
99. Wang L, Chopp M, Szalad A, Liu Z, Bolz M, Alvarez FM, Lu M, Zhang L, Cui Y, Zhang RL, Zhang ZG. 2011. Phosphodiesterase-5 is a therapeutic target for peripheral neuropathy in diabetic mice. Neuroscience 193: 399-410.
100. Wang Z, Gleichmann H. 1998. GLUT2 in pancreatic islets: crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 47:50-56.
101. Warden CH, Fisler JS. 2008. Comparisons of diets used in animal models of high-fat feeding. Cell Metab 7:277.
102. Watcho P, Stavniichuk R, Ribnicky DM, Raskin I, Obrosova IG. High-fat diet-induced neuropathy of prediabetes and obesity: Effect of PMI- 5011, an ethanolic extract of Artemisia dracunculus L. Mediators Inflamm 2010:268547.
103. Wiggin TD, Kretzler M, Pennathur S, Sullivan KA, Brosius FC, Feldman EL. 2008. Rosiglitazone treatment reduces diabetic neuropathy in streptozotocin-treated DBA/2J mice. Endocrinology 149:4928-4937.
104. Wiggin TD, Sullivan KA, Pop-Busui R, Amato A, Sima AA, Feldman EL. 2009. Elevated triglycerides correlate with progression of diabetic neuropathy. Diabetes 58:1634-1640.
105. Wilson GL, Leiter EH. 1990. Streptozotocin interactions with pancreatic beta cells and the induction of insulin-dependent diabetes. Curr Top Microbiol Immunol 156:27-54.
106. Wilson N, Wright D. 2011. Inflammatory mediators in diabetic neuropathy. J Diabetes Metab S5:004.
107. Wright A, Nukada H. 1994. Sciatic nerve morphology and morphometry in mature rats with streptozocin-induced diabetes. Acta Neuropathol 88:571-578.
108. Wright DE, Johnson MS, Arnett MG, Smittkamp SE, Ryals JM. 2007. Selective changes in nocifensive behavior despite normal cutaneous axon innervation in leptin receptor-null mutant (db/db) mice. J Peripher Nerv Syst 12:250-261.
109. YangW, Lu J,Weng J, JiaW, Ji L, Xiao J, Shan Z, Liu J, Tian H, Ji Q, Zhu D, Ge J, Lin L, Chen L, Guo X, Zhao Z, Li Q, Zhou Z, Shan G, He J. 2010. Prevalence of diabetes among men and women in China. N Engl J Med 362:1090-1101.
110. Yasuda H, Dyck PJ. 1987. Abnormalities of endoneurial microvessels and sural nerve pathology in diabetic neuropathy. Neurology 37:20-28.
111. Yoshioka M, Kayo T, Ikeda T, Koizumi A. 1997. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes 46:887-894.