Diabetic neuropathic pain development in type 2 diabetic mouse model and the prophylactic and therapeutic effects of coenzyme Q10

Neurobiology of Disease

Volumn 58, Issue , 2013, Pages 169-178

  Zhang, Yan Ping ^a   Song, Chun Yu ^b   Yuan, Yue ^a   Eber, Ariel ^a   Rodriguez, Yiliam ^a   Levitt, Roy C ^a,c   Takacs, Peter ^a   Yang, Zhe ^a   Goldberg, Ronald ^a   Candiotti, Keith A ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b THE SECOND AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

^c Miami Veterans Affairs Healthcare System   (United States)

Author keywords

Anti oxidant; Coenzyme Q10; Neuropathic pain; Oxidative stress; Type 2 diabetes

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; SYNAPTOTAGMIN I; TOLL LIKE RECEPTOR 4; UBIDECARENONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BODY MASS; CCL2 GENE; CONTROLLED STUDY; CXCL10 GENE; DIABETIC NEUROPATHY; FEMALE; GENE OVEREXPRESSION; LIPID PEROXIDATION; LIVER; MALE; MOUSE; NERVE CELL; NEUROPATHIC PAIN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD; SPINAL GANGLION; TLR4 GENE;

ANTI-OXIDANT; COENZYME Q10; NEUROPATHIC PAIN; OXIDATIVE STRESS; TYPE 2 DIABETES;

AGE FACTORS; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; CHEMOKINE CCL2; CHEMOKINE CXCL10; DIABETES MELLITUS, TYPE 2; DIABETIC NEUROPATHIES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HYPERALGESIA; LIPID PEROXIDATION; MALE; MICE; PAIN MEASUREMENT; PAIN THRESHOLD; RECOMBINANT FUSION PROTEINS; TOLL-LIKE RECEPTOR 4; UBIQUINONE; VITAMINS;

EID: 84879476551     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2013.05.003     Document Type: Article

References (56)

1. Allen R.G., Tresini M. Oxidative stress and gene regulation. Free Radic. Biol. Med. 2000, 28:463-499.
2. Battinoa M., Ferrib E., Girotti S., Lenazc G. Free radical scavenging activity of coenzyme Q measured by a chemiluminescent assay. Anal. Chim. Acta 1991, 255(2):367-371.
3. Beal M.F., Henshaw D.R., Jenkins B.G., Rosen B.R., Schulz J.B. Coenzyme Q10 and nicotinamide block striatal lesions produced by the mitochondrial toxin malonate. Ann. Neurol. 1994, 36:882-888.
4. Bettoni I., Comelli F., Rossini C., Granucci F., Giagnoni G., Peri F., Costa B. Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia 2008, 56:1312-1319.
5. Calcutt N.A., Stiller C., Gustafsson H., Malmberg A.B. Elevated substance-P-like immunoreactivity levels in spinal dialysates during the formalin test in normal and diabetic rats. Brain Res. 2000, 856:20-27.
6. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature 2001, 410:37-40.
7. Chen H., Charlat O., Tartaglia L.A., Woolf E.A., Weng X., Ellis S.J., Lakey N.D., Culpepper J., Moore K.J., Breitbart R.E., Duyk G.M., Tepper R.I., Morgenstern J.P. Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice. Cell 1996, 84:491-495.
8. Clement K., Vaisse C., Lahlou N., Cabrol S., Pelloux V., Cassuto D., Gourmelen M., Dina C., Chambaz J., Lacorte J.M., Basdevant A., Bougneres P., Lebouc Y., Froguel P., Guy-Grand B. A mutation in the human leptin receptor gene causes obesity and pituitary dysfunction. Nature 1998, 392:398-401.
9. Du Y., Tang J., Li G., Berti-Mattera L., Lee C.A., Bartkowski D., Gale D., Monahan J., Niesman M.R., Alton G., Kern T.S. Effects of p38 MAPK inhibition on early stages of diabetic retinopathy and sensory nerve function. Invest. Ophthalmol. Vis. Sci. 2010, 51:2158-2164.
10. Dzugkoev S.G., Kaloeva M.B., Dzugkoeva F.S. Effect of combination therapy with coenzyme Q10 on functional and metabolic parameters in patients with type 1 diabetes mellitus. Bull. Exp. Biol. Med. 2012, 152:364-366.
11. Edwards J.L., Vincent A.M., Cheng H.T., Feldman E.L. Diabetic neuropathy: mechanisms to management. Pharmacol. Ther. 2008, 120:1-34.
12. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 1991, 11:81-128.
13. Friedman J. Why is the nervous system vulnerable to oxidative stress?. Oxidative Stress and Free Radical Damage in Neurology, Oxidative Stress in Applied Basic Research and Clinical Practice 2011, 19-29. Springer Science Business Media, LLC. N. Gadoth, H.H. Gobel (Eds.).
14. Fu E.S., Zhang Y.P., Sagen J., Yang Z.Q., Bethea J.R. Transgenic glial nuclear factor-kappa B inhibition decreases formalin pain in mice. Neuroreport 2007, 18:713-717.
15. Fu E.S., Zhang Y.P., Sagen J., Candiotti K.A., Morton P.D., Liebl D.J., Bethea J.R., Brambilla R. Transgenic inhibition of glial NF-kappa B reduces pain behavior and inflammation after peripheral nerve injury. Pain 2010, 148:509-518.
16. Harati Y. Diabetic neuropathies: unanswered questions. Neurol. Clin. 2007, 25:303-317.
17. Haskell B.D., Flurkey K., Duffy T.M., Sargent E.E., Leiter E.H. The diabetes-prone NZO/HlLt strain. I. Immunophenotypic comparison to the related NZB/BlNJ and NZW/LacJ strains. Lab. Invest. 2002, 82:833-842.
18. Heubeck E. New treatment options for diabetic neuropathy. Doc News 2006, 3:8-9.
19. Hirayama I., Yi Z., Izumi S., Arai I., Suzuki W., Nagamachi Y., Kuwano H., Takeuchi T., Izumi T. Genetic analysis of obese diabetes in the TSOD mouse. Diabetes 1999, 48:1183-1191.
20. Huynh K., Kiriazis H., Du X.J., Love J.E., Jandeleit-Dahm K.A., Forbes J.M., McMullen J.R., Ritchie R.H. Coenzyme Q10 attenuates diastolic dysfunction, cardiomyocyte hypertrophy and cardiac fibrosis in the db/db mouse model of type 2 diabetes. Diabetologia 2012, 55:1544-1553.
21. Ji R.R., Suter M.R. p38 MAPK, microglial signaling, and neuropathic pain. Mol. Pain 2007, 3:33.
22. Joyce N., Annett G., Wirthlin L., Olson S., Bauer G., Nolta J.A. Mesenchymal stem cells for the treatment of neurodegenerative disease. Regen. Med. 2010, 5:933-946.
23. Jurgens H.S., Schurmann A., Kluge R., Ortmann S., Klaus S., Joost H.G., Tschop M.H. Hyperphagia, lower body temperature, and reduced running wheel activity precede development of morbid obesity in New Zealand obese mice. Physiol. Genomics 2006, 25:234-241.
24. Kanasaki K., Koya D. Biology of obesity: lessons from animal models of obesity. J. Biomed. Biotechnol 2011, Available from:, (Accessed 26th March 2013). 10.1155/2011/197636.
25. Kandhare A.D., Ghosh P., Ghule A.E., Bodhankar S.L. Elucidation of molecular mechanism involved in neuroprotective effect of coenzyme Q10 in alcohol-induced neuropathic pain. Fundam. Clin. Pharmacol. 2012, (Available from: doi: 10.1111. Accessed 26th March 2013).
26. Ko M.K., Saraswathy S., Parikh J.G., Rao N.A. The role of TLR4 activation in photoreceptor mitochondrial oxidative stress. Invest. Ophthalmol. Vis. Sci. 2011, 52:5824-5835.
27. Kucharska J., Braunova Z., Ulicna O., Zlatos L., Gvozdjakova A. Deficit of coenzyme Q in heart and liver mitochondria of rats with streptozotocin-induced diabetes. Physiol. Res. 2000, 49:411-418.
28. Kumar A., Negi G., Sharma S.S. Suppression of NF-kappaB and NF-kappaB regulated oxidative stress and neuroinflammation by BAY 11-7082 (IkappaB phosphorylation inhibitor) in experimental diabetic neuropathy. Biochimie 2012, 94:1158-1165.
29. Leiter E.H., Reifsnyder P.C., Flurkey K., Partke H.J., Junger E., Herberg L. NIDDM genes in mice: deleterious synergism by both parental genomes contributes to diabetogenic thresholds. Diabetes 1998, 47:1287-1295.
30. Liao Y.H., Zhang G.H., Jia D., Wang P., Qian N.S., He F., Zeng X.T., He Y., Yang Y.L., Cao D.Y., Zhang Y., Wang D.S., Tao K.S., Gao C.J., Dou K.F. Spinal astrocytic activation contributes to mechanical allodynia in a mouse model of type 2 diabetes. Brain Res. 2011, 1368:324-335.
31. Mancuso M., Coppede F., Migliore L., Siciliano G., Murri L. Mitochondrial dysfunction, oxidative stress and neurodegeneration. J. Alzheimers Dis. 2006, 10:59-73.
32. Matsuoka N., Ogawa Y., Hosoda K., Matsuda J., Masuzaki H., Miyawaki T., Azuma N., Natsui K., Nishimura H., Yoshimasa Y., Nishi S., Thompson D.B., Nakao K. Human leptin receptor gene in obese Japanese subjects: evidence against either obesity-causing mutations or association of sequence variants with obesity. Diabetologia 1997, 40:1204-1210.
33. Mezawa M., Takemoto M., Onishi S., Ishibashi R., Ishikawa T., Yamaga M., Fujimoto M., Okabe E., He P., Kobayashi K., Yokote K. The reduced form of coenzyme Q10 improves glycemic control in patients with type 2 diabetes: an open label pilot study. Biofactors 2012, 38:416-421.
34. Montine K.S., Olson S.J., Amarnath V., Whetsell W.O., Graham D.G., Montine T.J. Immunohistochemical detection of 4-hydroxy-2-nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4. Am. J. Pathol. 1997, 150:437-443.
35. Morrow T.J. Animal models of painful diabetic neuropathy: the STZ rat model. Curr. Protoc. Neurosci. Supplement 2004, 29(9.18):1-11.
36. Otto K.J., Wyse B.D., Cabot P.J., Smith M.T. Longitudinal study of painful diabetic neuropathy in the Zucker diabetic fatty rat model of type 2 diabetes: impaired basal G-protein activity appears to underpin marked morphine hyposensitivity at 6months. Pain Med. 2011, 12:437-450.
37. Pajovic S.B., Saicic Z.S., Spasic M.B., Petrovic V.M. The effect of ovarian hormones on antioxidant enzyme activities in the brain of male rats. Physiol. Res. 2003, 52:189-194.
38. Persson M.F., Franzen S., Catrina S.B., Dallner G., Hansell P., Brismar K., Palm F. Coenzyme Q10 prevents GDP-sensitive mitochondrial uncoupling, glomerular hyperfiltration and proteinuria in kidneys from db/db mice as a model of type 2 diabetes. Diabetologia 2012, 55:1535-1543.
39. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008, 22:659-661.
40. Runchel C., Matsuzawa A., Ichijo H. Mitogen-activated protein kinases in mammalian oxidative stress responses. Antioxid. Redox Signal. 2011, 15:205-218.
41. Shi T.J., Zhang M.D., Zeberg H., Nilsson J., Grunler J., Liu S.X., Xiang Q., Persson J., Fried K.J., Catrina S.B., Watanabe M., Arhem P., Brismar K., Hokfelt T.G. 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. 2013, 110:690-695.
42. Smith T., Nicholson R.A. Review of duloxetine in the management of diabetic peripheral neuropathic pain. Vasc. Health Risk Manag. 2007, 3:833-844.
43. Sourris K.C., Harcourt B.E., Tang P.H., Morley A.L., Huynh K., Penfold S.A., Coughlan M.T., Cooper M.E., Nguyen T.V., Ritchie R.H., Forbes J.M. Ubiquinone (coenzyme Q10) prevents renal mitochondrial dysfunction in an experimental model of type 2 diabetes. Free Radic. Biol. Med. 2012, 52:716-723.
44. Springer J.E., Azbill R.D., Mark R.J., Begley J.G., Waeg G., Mattson M.P. 4-hydroxynonenal, a lipid peroxidation product, rapidly accumulates following traumatic spinal cord injury and inhibits glutamate uptake. J. Neurochem. 1997, 68:2469-2476.
45. Stanzione P., Tropepi D. Drugs and clinical trials in neurodegenerative diseases. Ann. Ist. Super. Sanita 2011, 47:49-54.
46. Talbot S., Couture R. Emerging role of microglial kinin B1 receptor in diabetic pain neuropathy. Exp. Neurol. 2012, 234:373-381.
47. Tanga F.Y., Nutile-McMenemy N., DeLeo J.A. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:5856-5861.
48. Tjolsen A., Berge O.G., Hunskaar S., Rosland J.H., Hole K. The formalin test: an evaluation of the method. Pain 1992, 51:5-17.
49. Veves A., Backonja M., Malik R.A. Painful diabetic neuropathy: epidemiology, natural history, early diagnosis, and treatment options. Pain Med. 2008, 9:660-674.
50. Vincent A.M., Edwards J.L., Sadidi M., Feldman E.L. The antioxidant response as a drug target in diabetic neuropathy. Curr. Drug Targets 2008, 9:94-100.
51. Vinik A. Clinical review: use of antiepileptic drugs in the treatment of chronic painful diabetic neuropathy. J. Clin. Endocrinol. Metab. 2005, 90:4936-4945.
52. Wadsworth T.L., Bishop J.A., Pappu A.S., Woltjer R.L., Quinn J.F. Evaluation of coenzyme Q as an antioxidant strategy for Alzheimer's disease. J. Alzheimers Dis. 2008, 14:225-234.
53. Wheeler-Aceto H., Cowan A. Standardization of the rat paw formalin test for the evaluation of analgesics. Psychopharmacology (Berl) 1991, 104:35-44.
54. Yang L., Calingasan N.Y., Wille E.J., Cormier K., Smith K., Ferrante R.J., Beal M.F. Combination therapy with coenzyme Q10 and creatine produces additive neuroprotective effects in models of Parkinson's and Huntington's diseases. J. Neurochem. 2009, 109:1427-1439.
55. Zhang Y.P., Eber A., Yuan Y., Yang Z., Rodriguez Y., Levitt R.C., Takacs P., Candiotti K.A. Prophylactic and antinociceptive effects of coenzyme Q10 on diabetic neuropathic pain in a mouse model of type 1 diabetes. Anesthesiology 2013, 118:945-954.
56. Zhou M., Zhi Q., Tang Y., Yu D., Han J. Effects of coenzyme Q10 on myocardial protection during cardiac valve replacement and scavenging free radical activity in vitro. J. Cardiovasc. Surg. (Torino) 1999, 40:355-361.