Modulating molecular chaperones improves sensory fiber recovery and mitochondrial function in diabetic peripheral neuropathy

Experimental Neurology

Volumn 235, Issue 1, 2012, Pages 388-396

  Urban, Michael J ^a   Pan, Pan ^a   Farmer, Kevin L ^a   Zhao, Huiping ^a   Blagg, Brian S J ^a   Dobrowsky, Rick T ^a  

^a UNIVERSITY OF KANSAS   (United States)

Author keywords

Bioenergetics; Intra epidermal nerve fibers; Mitochondria; Nerve conduction velocity; Respiratory capacity; Sensory neurons

Indexed keywords

CHAPERONE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90 INHIBITOR; KU 32; STREPTOZOCIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOENERGY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIABETIC PERIPHERAL NEUROPATHY; DRUG EFFICACY; DRUG STRUCTURE; ELECTROPHYSIOLOGY; EX VIVO STUDY; HYPOALGESIA; MITOCHONDRION; MOUSE; NERVE CONDUCTION; NONHUMAN; PERIPHERAL NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SWISS WEBSTER MOUSE; THERMAL ANALYSIS;

ANIMALS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; EPIDERMIS; HSP90 HEAT-SHOCK PROTEINS; MICE; MITOCHONDRIA; MOLECULAR CHAPERONES; NERVE FIBERS; NEURAL CONDUCTION; PAIN MEASUREMENT; SENSORY RECEPTOR CELLS;

EID: 84859907435     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.03.005     Document Type: Article

References (59)

1. Akude E., Zherebitskaya E., Roy Chowdhury S.K., Girling K., Fernyhough P. 4-Hydroxy-2-nonenal induces mitochondrial dysfunction and aberrant axonal outgrowth in adult sensory neurons that mimics features of diabetic neuropathy. Neurotox. Res. 2009, 1:28-38.
2. Akude E., Zherebitskaya E., Chowdhury S.K.R., Smith D.R., Dobrowsky R.T., Fernyhough P. Diminished superoxide generation is associated with respiratory chain dysfunction and changes in the mitochondrial proteome of sensory neurons from diabetic rats. Diabetes 2011, 60:288-297.
3. Beiswenger K.K., Calcutt N.A., Mizisin A.P. Dissociation of thermal hypoalgesia and epidermal denervation in streptozotocin-diabetic mice. Neurosci. Lett. 2008, 442:267-272.
4. Beiswenger K.K., Calcutt N.A., Mizisin A.P. Epidermal nerve fiber quantification in the assessment of diabetic neuropathy. Acta Histochem. 2008, 110:351-362.
5. Bienemann A.S., Lee Y.B., Howarth J., Uney J.B. Hsp70 suppresses apoptosis in sympathetic neurones by preventing the activation of c-jun. J. Neurochem. 2008, 104:271-278.
6. Boucek P., Havrdova T., Voska L., Lodererova A., Saudek F., Lipar K., Janousek L., Adamec M., Sommer C. Severe depletion of intraepidermal nerve fibers in skin biopsies of pancreas transplant recipients. Transplant. Proc. 2005, 37:3574-3575.
7. Brand M.D., Nicholls D.G. Assessing mitochondrial dysfunction in cells. Biochem. J. 2011, 435:297-312.
8. Bu B., Klunemann H., Suzuki K., Li J., Bird T., Jin L.W., Vincent I. Niemann-Pick disease type C yields possible clue for why cerebellar neurons do not form neurofibrillary tangles. Neurobiol. Dis. 2002, 11:285-297.
9. Calcutt N.A. Tolerating diabetes - an alternative therapeutic approach for diabetic neuropathy. ASN Neuro 2010, 2:215-217.
10. Calcutt N.A., Cooper M.E., Kern T.S., Schmidt A.M. Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nat. Rev. Drug Discov. 2009, 8:417-430.
11. Chaudhury S., Welch T.R., Blagg B.S. Hsp90 as a target for drug development. Chem. Med. Chem. 2006, 1:1331-1340.
12. Chen Y.S., Chung S.S.M., Chung S.K. Noninvasive monitoring of diabetes-induced cutaneous nerve fiber loss and hypoalgesia in Thy1-YFP transgenic mice. Diabetes 2005, 54:3112-3118.
13. Choi S.W., Gerencser A.A., Nicholls D.G. Bioenergetic analysis of isolated cerebrocortical nerve terminals on a microgram scale: spare respiratory capacity and stochastic mitochondrial failure. J. Neurochem. 2009, 109:1179-1191.
14. Chowdhury S.K., Zherebitskaya E., Smith D.R., Akude E., Chattopadhyay S., Jolivalt C.G., Calcutt N.A., Fernyhough P. Mitochondrial respiratory chain dysfunction in dorsal root ganglia of streptozotocin-induced diabetic rats and its correction by insulin treatment. Diabetes 2010, 59:1082-1091.
15. Chowdhury S.K.R., Dobrowsky R.T., Fernyhough P. Nutrient excess and altered mitochondrial proteome and function contribute to neurodegeneration in diabetes. Mitochondrion 2011, 11:845-854.
16. Chowdhury, S.K.R., Smith, D.R., Saleh, A., Schapansky, J., Marquez, A., Gomes, S., Akude, E., Morrow, D., Calcutt, N.A., Fernyhough, P., in press. Impaired amp-activated protein kinase signaling in dorsal root ganglia neurons is linked to mitochondrial dysfunction and peripheral neuropathy in diabetes. Brain.
17. Chung J., Nguyen A.K., Henstridge D.C., Holmes A.G., Chan M.H., Mesa J.L., Lancaster G.I., Southgate R.J., Bruce C.R., Duffy S.J., Horvath I., Mestril R., Watt M.J., Hooper P.L., Kingwell B.A., Vigh L., Hevener A., Febbraio M.A. Hsp72 protects against obesity-induced insulin resistance. Proc. Natl. Acad. Sci. 2008, 105:1739-1744.
18. Courchesne S.L., Karch C., Pazyra-Murphy M.F., Segal R.A. Sensory neuropathy attributable to loss of bcl-w. J. Neurosci. 2011, 31:1624-1634.
19. Delree P., Leprince P., Schoenen J., Moonen G. Purification and culture of adult rat dorsal root ganglia neurons. J. Neurosci. Res. 1989, 23:198-206.
20. Dranka B.P., Hill B.G., Darley-Usmar V.M. Mitochondrial reserve capacity in endothelial cells: the impact of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 2010, 48:905-914.
21. Fernyhough P., Roy Chowdhury S.K., Schmidt R.E. Mitochondrial stress and the pathogenesis of diabetic neuropathy. Expert Rev. Endocrinol. Metab. 2010, 5:39-49.
22. Gruden G., Bruno G., Chaturvedi N., Burt D., Pinach S., Schalkwijk C., Stehouwer C.D., Witte D.R., Fuller J.H., Cavallo-Perin P. Anti-hsp60 and anti-hsp70 antibody levels and micro/macrovascular complications in type 1 diabetes: the EURODIAB Study. J. Intern. Med. 2009, 266:527-536. Group, E. P. C. S.
23. Guzhova I., Kislyakova K., Moskaliova O., Fridlanskaya I., Tytell M., Cheetham M., Margulis B. In vitro studies show that hsp70 can be released by glia and that exogenous hsp70 can enhance neuronal stress tolerance. Brain Res. 2001, 914:66-73.
24. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
25. Huang Y.-T., Blagg B.S.J. A library of noviosylated coumarin analogues. J. Org. Chem. 2007, 72:3609-3613.
26. Huang T.J., Price S.A., Chilton L., Calcutt N.A., Tomlinson D.R., Verkhratsky A., Fernyhough P. Insulin prevents depolarization of the mitochondrial inner membrane in sensory neurons of type 1 diabetic rats in the presence of sustained hyperglycemia. Diabetes 2003, 52:2129-2136.
27. Huang T.J., Verkhratsky A., Fernyhough P. Insulin enhances mitochondrial inner membrane potential and increases ATP levels through phosphoinositide 3-kinase in adult sensory neurons. Mol. Cell. Neurosci. 2005, 28:42-54.
28. Kamiya H., Zhangm W., Sima A.A.F. Apoptotic stress is counterbalanced by survival elements preventing programmed cell death of dorsal root ganglions in subacute type 1 diabetic BB/Wor rats. Diabetes 2005, 54:3288-3295.
29. Kamiya H., Zhang W., Sima A.A. Degeneration of the Golgi and neuronal loss in dorsal root ganglia in diabetic Biobreeding/Worcester rats. Diabetologia 2006, 49:2763-2774.
30. Kennedy J.M., Zochodne D.W. Experimental diabetic neuropathy with spontaneous recovery: is there irreparable damage?. Diabetes 2005, 54:830-837.
31. Lauria G., Cornblath D.R., Johansson O., McArthur J.C., Mellgren S.I., Nolano M., Rosenberg N., Sommer C. EFNS guidelines on the use of skin biopsy in the diagnosis of peripheral neuropathy. Eur. J. Neurol. 2005, 12:747-758.
32. Luo W., Dou F., Rodina A., Chip S., Kim J., Zhao Q., Moulick K., Aguirre J., Wu N., Greengard P., Chiosis G. Roles of heat-shock protein 90 in maintaining and facilitating the neurodegenerative phenotype in tauopathies. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:9511-9516.
33. Malik R.A., Veves A., Tesfaye S., Smith G., Cameron N., Zochodne D., Lauria G. Small fibre neuropathy: role in the diagnosis of diabetic sensorimotor polyneuropathy. Diabetes Metab. Res. Rev. 2011, 27:678-684. on behalf of The Toronto Consensus Panel on Diabetic, N.
34. Marcu M.G., Chadli A., Bouhouche I., Catelli M., Neckers L.M. The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. J. Biol. Chem. 2000, 275:37181-37186.
35. Matts R.L., Brandt G.E., Lu Y., Dixit A., Mollapour M., Wang S., Donnelly A.C., Neckers L., Verkhivker G., Blagg B.S. A systematic protocol for the characterization of Hsp90 modulators. Bioorg. Med. Chem. 2011, 19:684-692.
36. 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.
37. Muchowski P.J., Wacker J.L. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 2005, 6:11-22.
38. Nicholls D.G., Johnson-Cadwell L., Vesce S., Jekabsons M., Yadava N. Bioenergetics of mitochondria in cultured neurons and their role in glutamate excitotoxicity. J. Neurosci. Res. 2007, 85:3206-3212.
39. Niemeyer B.A. Structure-function analysis of TRPV channels. Naunyn Schmiedebergs Arch. Pharmacol. 2005, 371:285-294.
40. Obrosova I.G. Diabetes and the peripheral nerve. Biochim. Biophys. Acta 2009, 10:931-940.
41. Obrosova I.G., Stavniichuk R., Drel V.R., Shevalye H., Vareniuk I., Nadler J.L., Schmidt R.E. Different roles of 12/15-lipoxygenase in diabetic large and small fiber peripheral and autonomic neuropathies. Am. J. Pathol. 2010, 177:1436-1447.
42. Ouyang Y.B., Xu L.J., Sun Y.J., Giffard R.G. Overexpression of inducible heat shock protein 70 and its mutants in astrocytes is associated with maintenance of mitochondrial physiology during glucose deprivation stress. Cell Stress Chaperones 2006, 11:180-186.
43. Pabbidi R.M., Yu S.Q., Peng S., Khardori R., Pauza M.E., Premkumar L.S. Influence of TRPV1 on diabetes-induced alterations in thermal pain sensitivity. Mol. Pain 2008, 4:9.
44. Pittenger G.L., Mehrabyan A., Simmons K., Amandarice, Dublin C., Barlow P., Vinik A.I. Small fiber neuropathy is associated with the metabolic syndrome. Metab. Syndr. Relat. Disord. 2005, 3:113-121.
45. Pratt W.B., Morishima Y., Peng H.M., Osawa Y. Proposal for a role of the Hsp90/Hsp70-based chaperone machinery in making triage decisions when proteins undergo oxidative and toxic damage. Exp. Biol. Med. 2010, 235:278-289.
46. Sansbury B.E., Jones S.P., Riggs D.W., Darley-Usmar V.M., Hill B.G. Bioenergetic function in cardiovascular cells: the importance of the reserve capacity and its biological regulation. Chem. Biol. Interact. 2011, 191:288-295.
47. Schmidt O., Pfanner N., Meisinger C. Mitochondrial protein import: from proteomics to functional mechanisms. Nat. Rev. Mol. Cell Biol. 2010, 11:655-667.
48. Smith A.G., Ramachandran P., Tripp S., Singleton J.R. Epidermal nerve innervation in impaired glucose tolerance and diabetes-associated neuropathy. Neurology 2001, 57:1701-1704.
49. Stavniichuk R., Drel V.R., Shevalye H., Maksimchyk Y., Kuchmerovska T.M., Nadler J.L., Obrosova I.G. Baicalein alleviates diabetic peripheral neuropathy through inhibition of oxidative-nitrosative stress and p38 MAPK activation. Exp. Neurol. 2011, 230:106-113.
50. Ullman-Cullere M.H., Foltz C.J. Body condition scoring: a rapid and accurate method for assessing health status in mice. Lab. Anim. Sci. 1999, 49:319-323.
51. Urban M.J., Li C., Yu C., Lu Y., Krise J.M., McIntosh M.P., Rajewski R.A., Blagg B.S.J., Dobrowsky R.T. Inhibiting heat shock protein 90 reverses sensory hypoalgesia in diabetic mice. ASN Neuro 2010, 2:e00040. (DOI :00189-00199).
52. 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.
53. Vincent A.M., Edwards J.L., McLean L.L., Hong Y., Cerri F., Lopez I., Quattrini A., Feldman E.L. Mitochondrial biogenesis and fission in axons in cell culture and animal models of diabetic neuropathy. Acta Neuropathol. 2010, 120:477-489.
54. Wu M., Neilson A., Swift A.L., Moran R., Tamagnine J., Parslow D., Armistead S., Lemire K., Orrell J., Teich J., Chomicz S., Ferrick D.A. Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 2007, 292:C125-C136.
55. Yorek M.A. The potential role of angiotensin converting enzyme and vasopeptidase inhibitors in the treatment of diabetic neuropathy. Curr. Drug Targets 2008, 9:77-84.
56. Yorek M.A. Treatment of diabetic neuropathy with baicalein: intervention at multiple sites. Exp. Neurol. 2011, 232:105-109.
57. Young J.C., Hoogenraad N.J., Hartl F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor TOM70. Cell 2003, 112:41-50.
58. Yu C., Rouen S., Dobrowsky R.T. Hyperglycemia and downregulation of caveolin-1 enhance neuregulin-induced demyelination. Glia 2008, 56:877-887.
59. Zherebitskaya E., Akude E., Smith D.R., Fernyhough P. Development of selective axonopathy in adult sensory neurons isolated from diabetic rats: role of glucose-induced oxidative stress. Diabetes 2009, 58:1356-1364.