Role of 12/15-lipoxygenase in nitrosative stress and peripheral prediabetic and diabetic neuropathies

Free Radical Biology and Medicine

Volumn 49, Issue 6, 2010, Pages 1036-1045

  Stavniichuk, Roman ^a   Drel, Viktor R ^a   Shevalye, Hanna ^a   Vareniuk, Igor ^a   Stevens, Martin J ^b   Nadler, Jerry L ^c   Obrosova, Irina G ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c EASTERN VIRGINIA MEDICAL SCHOOL   (United States)

Author keywords

12(S) Hydroxyeicosatetraenoic acid; 12 15 Lipoxygenase; Free radicals; Human Schwann cell; Intraepidermal nerve fiber density; Nerve conduction; Nitrosative stress; Peripheral diabetic neuropathy; Tactile allodynia; Thermal algesia

Indexed keywords

ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; CINNAMYL 3,4 DIHYDROXY ALPHA CYANOCINNAMATE; GLUCOSE; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL CULTURE; CONTROLLED STUDY; DIABETIC NEUROPATHY; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; IMPAIRED GLUCOSE TOLERANCE; LIPID DIET; MALE; MOUSE; NERVE CONDUCTION DISORDER; NERVE FIBER; NITROSATIVE STRESS; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHWANN CELL; SCIATIC NERVE; SPINAL CORD; STREPTOZOCIN DIABETES;

MUS;

EID: 77955509447     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.06.016     Document Type: Article

References (80)

1. Natarajan R., Nadler J.L. Lipoxygenases and lipid signaling in vascular cells in diabetes. Front. Biosci. 2003, 8:783-795.
2. Natarajan R., Nadler J.L. Lipid inflammatory mediators in diabetic vascular disease. Arterioscler. Thromb. Vasc. Biol. 2004, 24:1542-1548.
3. Nunemaker C.S., Chen M., Pei H., Kimble S.D., Keller S.R., Carter J.D., Yang Z., Smith K.M., Wu R., Bevard M.H., Garmey J.C., Nadler J.L. 12-Lipoxygenase-knockout mice are resistant to inflammatory effects of obesity induced by Western diet. Am. J. Physiol. Endocrinol. Metab. 2008, 295:E1065-E1075.
4. Chakrabarti S.K., Cole B.K., Wen Y., Keller S.R., Nadler J.L. 12/15-Lipoxygenase products induce inflammation and impair insulin signaling in 3T3-L1 adipocytes. Obesity (Silver Spring) 2009, 17:1657-1663.
5. Bolick D.T., Orr A.W., Whetzel A., Srinivasan S., Hatley M.E., Schwartz M.A., Hedrick C.C. 12/15-Lipoxygenase regulates intercellular adhesion molecule-1 expression and monocyte adhesion to endothelium through activation of RhoA and nuclear factor-kappaB. Arterioscler. Thromb. Vasc. Biol. 2005, 25:2301-2307.
6. Sasson S., Eckel J. Disparate effects of 12-lipoxygenase and 12-hydroxy-eicosatetraenoic acid in vascular endothelial and smooth muscle cells and in cardiomyocytes. Arch. Physiol. Biochem. 2006, 112:119-129.
7. Kang S.W., Natarajan R., Shahed A., Nast C.C., LaPage J., Mundel P., Kashtan C., Adler S.G. Role of 12-lipoxygenase in the stimulation of p38 mitogen-activated protein kinase and collagen alpha5(IV) in experimental diabetic nephropathy and in glucose-stimulated podocytes. J. Am. Soc. Nephrol. 2003, 14:3178-3187.
8. Kim Y.S., Xu Z.G., Reddy M.A., Li S.L., Lanting L., Sharma K., Adler S.G., Natarajan R. Novel interactions between TGF-β1 actions and the 12/15-lipoxygenase pathway in mesangial cells. J. Am. Soc. Nephrol. 2005, 16:352-362.
9. González-Núñez D., Solé M., Natarajan R., Poch E. 12-Lipoxygenase metabolism in mouse distal convoluted tubule cells. Kidney Int. 2005, 67:178-186.
10. Dioszeghy V., Rosas M., Maskrey B.H., Colmont C., Topley N., Chaitidis P., Kühn H., Jones S.A., Taylor P.R., O'Donnell V.B. 12/15-Lipoxygenase regulates the inflammatory response to bacterial products in vivo. J. Immunol. 2008, 181:6514-6524.
11. van Leyen K., Arai K., Jin G., Kenyon V., Gerstner B., Rosenberg P.A., Holman T.R., Lo E.H. Novel lipoxygenase inhibitors as neuroprotective reagents. J. Neurosci. Res. 2008, 86:904-909.
12. Prasad V.V., Nithipatikom K., Harder D.R. Ceramide elevates 12-hydroxy-eicosatetraenoic acid levels and upregulates 12-lipoxygenase in rat primary hippocampal cell cultures containing predominantly astrocytes. Neurochem. Int. 2008, 53:220-229.
13. Li J., Wang H., Rosenberg P.A. Vitamin K prevents oxidative cell death by inhibiting activation of 12-lipoxygenase in developing oligodendrocytes. J. Neurosci. Res. 2009, 87:1997-2005.
14. Rao G.N., Baas A.S., Glasgow W.C., Eling T.E., Runge M.S., Alexander R.W. Activation of mitogen-activated protein kinases by arachidonic acid and its metabolites in vascular smooth muscle cells. J. Biol. Chem. 1994, 269:32586-32591.
15. Natarajan R., Reddy M.A., Malik K.U., Fatima S., Khan B.V. Signaling mechanisms of nuclear factor-kappaB-mediated activation of inflammatory genes by 13-hydroperoxyoctadecadienoic acid in cultured vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 2001, 21:1408-1413.
16. Reddy M.A., Thimmalapura P.R., Lanting L., Nadler J.L., Fatima S., Natarajan R. The oxidized lipid and lipoxygenase product 12(S)-hydroxyeicosa-tetraenoic acid induces hypertrophy and fibronectin transcription in vascular smooth muscle cells via p38 MAPK and cAMP response element-binding protein activation: mediation of angiotensin II effects. J. Biol. Chem. 2002, 277:9920-9928.
17. Kühn H., O'Donnell V.B. Inflammation and immune regulation by 12/15-lipoxygenases. Prog. Lipid Res. 2006, 45:334-356.
18. Kim Y.S., Reddy M.A., Lanting L., Adler S.G., Natarajan R. Differential behavior of mesangial cells derived from 12/15-lipoxygenase knockout mice relative to control mice. Kidney Int. 2003, 64:1702-1714.
19. Li S.L., Dwarakanath R.S., Cai Q., Lanting L., Natarajan R. Effects of silencing leukocyte-type 12/15-lipoxygenase using short interfering RNAs. J. Lipid Res. 2005, 46:220-229.
20. Reilly K.B., Srinivasan S., Hatley M.E., Patricia M.K., Lannigan J., Bolick D.T., Vandenhoff G., Pei H., Natarajan R., Nadler J.L., Hedrick C.C. 12/15-Lipoxygenase activity mediates inflammatory monocyte/endothelial interactions and atherosclerosis in vivo. J. Biol. Chem. 2004, 279:9440-9450.
21. Yuan H., Lanting L., Xu Z.G., Li S.L., Swiderski P., Putta S., Jonnalagadda M., Kato M., Natarajan R. Effects of cholesterol-tagged small interfering RNAs targeting 12/15-lipoxygenase on parameters of diabetic nephropathy in a mouse model of type 1 diabetes. Am. J. Physiol. Ren. Physiol. 2008, 295:F605-F617.
22. Huo Y., Zhao L., Hyman M.C., Shashkin P., Harry B.L., Burcin T., Forlow S.B., Stark M.A., Smith D.F., Clarke S., Srinivasan S., Hedrick C.C., Praticò D., Witztum J.L., Nadler J.L., Funk C.D., Ley K. Critical role of macrophage 12/15-lipoxygenase for atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004, 110:2024-2031.
23. Gubitosi-Klug R.A., Talahalli R., Du Y., Nadler J.L., Kern T.S. 5-Lipoxygenase, but not 12/15-lipoxygenase, contributes to degeneration of retinal capillaries in a mouse model of diabetic retinopathy. Diabetes 2008, 57:1387-1393.
24. Boulton A.J., Vinik A.I., Arezzo J.C., Bril V., Feldman E.L., Freeman R., Malik R.A., Maser R.E., Sosenko J.M., Ziegler D. American Diabetes Association. Diabetic neuropathies: a statement by the American Diabetes Association. Diab. Care 2005, 28:956-962.
25. Obrosova I.G. Diabetic painful and insensate neuropathy: pathogenesis and potential treatments. Neurotherapeutics 2009, 6:638-647.
26. Obrosova I.G., Li F., Abatan O.I., Forsell M.A., Komjáti K., Pacher P., Szabó C., Stevens M.J. Role of poly(ADP-ribose) polymerase activation in diabetic neuropathy. Diabetes 2004, 53:711-720.
27. Obrosova I.G., Ilnytska O., Lyzogubov V.V., Pavlov I.A., Mashtalir N., Nadler J.L., Drel V.R. High-fat diet induced neuropathy of pre-diabetes and obesity: effects of "healthy" diet and aldose reductase inhibition. Diabetes 2007, 56:2598-2608.
28. Song Z., Fu D.T., Chan Y.S., Leung S., Chung S.S., Chung S.K. Transgenic mice overexpressing aldose reductase in Schwann cells show more severe nerve conduction velocity deficit and oxidative stress under hyperglycemic stress. Mol. Cell Neurosci. 2003, 23:638-647.
29. Vareniuk I., Pavlov I.A., Obrosova I.G. Inducible nitric oxide synthase gene deficiency counteracts multiple manifestations of peripheral neuropathy in a streptozotocin-induced mouse model of diabetes. Diabetologia 2008, 51:2126-2133.
30. Vareniuk I., Pacher P., Pavlov I.A., Drel V.R., Obrosova I.G. Peripheral neuropathy in mice with neuronal nitric oxide synthase gene deficiency. Int. J. Mol. Med. 2009, 23:571-580.
31. Zhang L., Yu C., Vasquez F.E., Galeva N., Onyango I., Swerdlow R.H., Dobrowsky R.T. Hyperglycemia alters the Schwann cell mitochondrial proteome and decreases coupled respiration in the absence of superoxide production. J. Proteome Res. 2010, 9:458-471.
32. Obrosova I.G., Drel V.R., Pacher P., Ilnytska O., Wang Z.Q., Stevens M.J., Yorek M.A. Oxidative-nitrosative stress and poly(ADP-ribose) polymerase (PARP) activation in experimental diabetic neuropathy: the relation is revisited. Diabetes 2005, 54:3435-3441.
33. Stevens M.J., Li F., Drel V.R., Abatan O.I., Kim H., Burnett D., Larkin D., Obrosova I.G. Nicotinamide reverses neurological and neurovascular deficits in streptozotocin diabetic rats. J. Pharmacol. Exp. Ther. 2007, 320:458-464.
34. Askwith T., Zeng W., Eggo M.C., Stevens M.J. Oxidative stress and dysregulation of the taurine transporter in high-glucose-exposed human Schwann cells: implications for pathogenesis of diabetic neuropathy. Am. J. Physiol. Endocrinol. Metab. 2009, 297:620-628.
35. Kuruvilla R., Peterson R.G., Kincaid J.C., Eichberg J. Evening primrose oil treatment corrects reduced conduction velocity but not depletion of arachidonic acid in nerve from streptozotocin-induced diabetic rats. Prostaglandins Leukot. Essent. Fatty Acids 1998, 59:195-202.
36. Pop-Busui R., Marinescu V., Van Huysen C., Li F., Sullivan K., Greene D.A., Larkin D., Stevens M.J. Dissection of metabolic, vascular, and nerve conduction interrelationships in experimental diabetic neuropathy by cyclooxygenase inhibition and acetyl-L-carnitine administration. Diabetes 2002, 51:2619-2628.
37. Kellogg A.P., Wiggin T.D., Larkin D.D., Hayes J.M., Stevens M.J., Pop-Busui R. Protective effects of cyclooxygenase-2 gene inactivation against peripheral nerve dysfunction and intraepidermal nerve fiber loss in experimental diabetes. Diabetes 2007, 56:2997-3005.
38. Nagamatsu M., Nickander K.K., Schmelzer J.D., Raya A., Wittrock D.A., Tritschler H., Low P.A. Lipoic acid improves nerve blood flow, reduces oxidative stress, and improves distal nerve conduction in experimental diabetic neuropathy. Diab. Care 1995, 18:1160-1167.
39. Sagara M., Satoh J., Wada R., Yagihashi S., Takahashi K., Fukuzawa M., Muto G., Muto Y., Toyota T. Inhibition of development of peripheral neuropathy in streptozotocin-induced diabetic rats with N-acetylcysteine. Diabetologia 1996, 39:263-269.
40. Love A., Cotter M.A., Cameron N.E. Effects of the sulphydryl donor N-acetyl-L-cysteine on nerve conduction, perfusion, maturation and regeneration following freeze damage in diabetic rats. Eur. J. Clin. Invest. 1996, 26:698-706.
41. Stevens M.J., Obrosova I., Cao X., Van Huysen C., Greene D.A. Effects of DL-alpha-lipoic acid on peripheral nerve conduction, blood flow, energy metabolism, and oxidative stress in experimental diabetic neuropathy. Diabetes 2000, 49:1006-1015.
42. Cameron N.E., Jack A.M., Cotter M.A. Effect of α-lipoic acid on vascular responses and nociception in diabetic rats. Free Radic. Biol. Med. 2001, 31:125-135.
43. Coppey L.J., Gellett J.S., Davidson E.P., Dunlap J.A., Lund D.D., Yorek M.A. Effect of antioxidant treatment of streptozotocin-induced diabetic rats on endoneurial blood flow, motor nerve conduction velocity, and vascular reactivity of epineurial arterioles of the sciatic nerve. Diabetes 2001, 50:1927-1937.
44. Cameron N.E., Tuck Z., McCabe L., Cotter M.A. Effect of the hydroxyl radical scavenger, dimethylthiourea, on peripheral nerve tissue perfusion, conduction velocity and nociception in experimental diabetes. Diabetologia 2001, 44:1161-1169.
45. Inkster M.E., Cotter M.A., Cameron N.E. Effects of trientine, a metal chelator, on defective endothelium-dependent relaxation in the mesenteric vasculature of diabetic rats. Free Radic. Res. 2002, 36:1091-1099.
46. Schmeichel A.M., Schmelzer J.D., Low P.A. Oxidative injury and apoptosis of dorsal root ganglion neurons in chronic experimental diabetic neuropathy. Diabetes 2003, 52:165-171.
47. Coppey L.J., Gellett J.S., Davidson E.P., Dunlap J.A., Lund D.D., Salvemini D., Yorek M.A. Effect of M40403 treatment of diabetic rats on endoneurial blood flow, motor nerve conduction velocity and vascular function of epineurial arterioles of the sciatic nerve. Br. J. Pharmacol. 2001, 134:21-29.
48. Cotter M.A., Cameron N.E. Effect of the NAD(P)H oxidase inhibitor, apocynin, on peripheral nerve perfusion and function in diabetic rats. Life Sci. 2003, 73:1813-1824.
49. Inkster M.E., Cotter M.A., Cameron N.E. Treatment with the xanthine oxidase inhibitor, allopurinol, improves nerve and vascular function in diabetic rats. Eur. J. Pharmacol. 2007, 561:63-71.
50. Obrosova I.G., Van Huysen C., Fathallah L., Cao X.C., Greene D.A., Stevens M.J. An aldose reductase inhibitor reverses early diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J. 2002, 16:123-125.
51. 2-terminal kinase activation, depletion of reduced glutathione, increased superoxide accumulation, and DNA damage. Diabetes 2006, 55:1946-1953.
52. Vincent A.M., Russell J.W., Sullivan K.A., Backus C., Hayes J.M., McLean L.L., Feldman E.L. SOD2 protects neurons from injury in cell culture and animal models of diabetic neuropathy. Exp. Neurol. 2007, 208:216-227.
53. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 2007, 87:315-424.
54. Szabó C., Ischiropoulos H., Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 2007, 6:662-680.
55. Souza J.M., Giasson B.I., Chen Q., Lee V.M., Ischiropoulos H. Dityrosine cross-linking promotes formation of stable alpha-synuclein polymers: implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J. Biol. Chem. 2000, 275:18344-18349.
56. Zhang Y.J., Xu Y.F., Liu Y.H., Yin J., Li H.L., Wang Q., Wang J.Z. Peroxynitrite induces Alzheimer-like tau modifications and accumulation in rat brain and its underlying mechanisms. FASEB J. 2006, 20:1431-1442.
57. Horiguchi T., Uryu K., Giasson B.I., Ischiropoulos H., LightFoot R., Bellmann C., Richter-Landsberg C., Lee V.M., Trojanowski J.Q. Nitration of tau protein is linked to neurodegeneration in tauopathies. Am. J. Pathol. 2003, 163:1021-1031.
58. Obrosova I.G., Mabley J.G., Zsengellér Z., Charniauskaya T., Abatan O.I., Groves J.T., Szabó C. Role for nitrosative stress in diabetic neuropathy: evidence from studies with a peroxynitrite decomposition catalyst. FASEB J. 2005, 19:401-403.
59. Drel V.R., Pacher P., Vareniuk I., Pavlov I.A., Ilnytska O., Lyzogubov V.V., Bell S.R., Groves J.T., Obrosova I.G. Evaluation of the peroxynitrite decomposition catalyst Fe(III) tetra-mesitylporphyrin octasulfonate on peripheral neuropathy in a mouse model of type 1 diabetes. Int. J. Mol. Med. 2007, 20:783-792.
60. Obrosova I.G., Drel V.R., Oltman C.L., Mashtalir N., Tibrewala J., Groves J.T., Yorek M.A. Role of nitrosative stress in early neuropathy and vascular dysfunction in streptozotocin-diabetic rats. Am. J. Physiol. Endocrinol. Metab. 2007, 293:E1645-E1655.
61. Nangle M.R., Cotter M.A., Cameron N.E. Effects of the peroxynitrite decomposition catalyst, FeTMPyP, on function of corpus cavernosum from diabetic mice. Eur. J. Pharmacol. 2004, 502:143-148.
62. Vincent A.M., Hayes J.M., McLean L.L., Vivekanandan-Giri A., Pennathur S., Feldman E.L. Dyslipidemia-induced neuropathy in mice: the role of oxLDL/LOX-1. Diabetes 2009, 58:2376-2385.
63. Szabó C., Zanchi A., Komjáti K., Pacher P., Krolewski A.S., Quist W.C., LoGerfo F.W., Horton E.S., Veves A. Poly(ADP-ribose) polymerase is activated in subjects at risk of developing type 2 diabetes and is associated with impaired vascular reactivity. Circulation 2002, 106:2680-2686.
64. Drel V.R., Lupachyk S., Shevalye H., Vareniuk I., Xu W., Zhang J., Delamere N.A., Shahidullah M., Slusher B., Obrosova I.G. New therapeutic and biomarker discovery for peripheral diabetic neuropathy: PARP inhibitor, nitrotyrosine, and tumor necrosis factor-α. Endocrinology 2010, 151:2547-2555.
65. Ceriello A., Esposito K., Piconi L., Ihnat M.A., Thorpe J.E., Testa R., Boemi M., Giugliano D. Oscillating glucose is more deleterious to endothelial function and oxidative stress than mean glucose in normal and type 2 diabetic patients. Diabetes 2008, 57:1349-1354.
66. Nourooz-Zadeh J., Ziegler D., Sohr C., Betteridge J.D., Knight J., Hothersall J. The use of pholasin as a probe for the determination of plasma total antioxidant capacity. Clin. Biochem. 2006, 39:55-61.
67. El-Remessy A.B., Abou-Mohamed G., Caldwell R.W., Caldwell R.B. High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest. Ophthalmol. Visual Sci. 2003, 44:3135-3143.
68. Obrosova I.G., Pacher P., Szabó C., Zsengeller Z., Hirooka H., Stevens M.J., Yorek M.A. Aldose reductase inhibition counteracts oxidative-nitrosative stress and poly(ADP-ribose) polymerase activation in tissue sites for diabetes complications. Diabetes 2005, 54:234-242.
69. Cheung A.K., Fung M.K., Lo A.C., Lam T.T., So K.F., Chung S.S., Chung S.K. Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes 2005, 54:3119-3125.
70. Drel V.R., Xu W., Zhang J., Kador P.F., Ali T.K., Shin J., Julius U., Slusher B., El-Remessy A.B., Obrosova I.G. Poly(ADP-ribose)polymerase inhibition counteracts cataract formation and early retinal changes in streptozotocin-diabetic rats. Invest. Ophthalmol. Visual Sci. 2009, 50:1778-1790.
71. Drel V.R., Xu W., Zhang J., Pavlov I.A., Shevalye H., Slusher B., Obrosova I.G. Poly(adenosine 5'-diphosphate-ribose) polymerase inhibition counteracts multiple manifestations of experimental type 1 diabetic nephropathy. Endocrinology 2009, 150:5273-5283.
72. Nakamura J., Kato K., Hamada Y., Nakayama M., Chaya S., Nakashima E., Naruse K., Kasuya Y., Mizubayashi R., Miwa K., Yasuda Y., Kamiya H., Ienaga K., Sakakibara F., Koh N., Hotta N. A protein kinase C-beta-selective inhibitor ameliorates neural dysfunction in streptozotocin-induced diabetic rats. Diabetes 1999, 48:2090-2095.
73. Obrosova I.G., Van Huysen C., Fathallah L., Cao X., Stevens M.J., Greene D.A. Evaluation of alpha(1)-adrenoceptor antagonist on diabetes-induced changes in peripheral nerve function, metabolism, and antioxidative defense. FASEB J. 2000, 14:1548-1558.
74. Nakae M., Kamiya H., Naruse K., Horio N., Ito Y., Mizubayashi R., Hamada Y., Nakashima E., Akiyama N., Kobayashi Y., Watarai A., Kimura N., Horiguchi M., Tabata Y., Oiso Y., Nakamura J. Effects of basic fibroblast growth factor on experimental diabetic neuropathy in rats. Diabetes 2006, 55:1470-1477.
75. McGuire J.F., Rouen S., Siegfreid E., Wright D.E., Dobrowsky R.T. Caveolin-1 and altered neuregulin signaling contribute to the pathophysiological progression of diabetic peripheral neuropathy. Diabetes 2009, 58:2677-2686.
76. Yagihashi S., Yamagishi S.I., Wada Ri R., Baba M., Hohman T.C., Yabe-Nishimura C., Kokai Y. Neuropathy in diabetic mice overexpressing human aldose reductase and effects of aldose reductase inhibitor. Brain 2001, 124:2448-2458.
77. Pittenger G.L., Ray M., 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. Diab. Care 2004, 27:1974-1979.
78. Quattrini C., Tavakoli M., Jeziorska M., Kallinikos P., Tesfaye S., Finnigan J., Marshall A., Boulton A.J., Efron N., Malik R.A. Surrogate markers of small fiber damage in human diabetic neuropathy. Diabetes 2007, 56:2148-2154.
79. Brussee V., Guo G., Dong Y., Cheng C., Martinez J.A., Smith D., Glazner G.W., Fernyhough P., Zochodne D.W. Distal degenerative sensory neuropathy in a long-term type 2 diabetes rat model. Diabetes 2008, 57:1664-1673.
80. Kuruvilla R., Eichberg J. Depletion of phospholipid arachidonoyl-containing molecular species in a human Schwann cell line grown in elevated glucose and their restoration by an aldose reductase inhibitor. J. Neurochem. 1998, 71:775-783.