Calpain inhibitor, MDL 28170 confer electrophysiological, nociceptive and biochemical improvement in diabetic neuropathy

Neuropharmacology

Volumn 97, Issue , 2015, Pages 113-121

  Kharatmal, Shivsharan B ^a   Singh, Jitendra N ^a   Sharma, Shyam S ^a  

^a NATIONAL INSTITUTE OF PHARMACEUTICAL EDUCATION AND RESEARCH NIPER   (India)

Author keywords

Calpain; Diabetic neuropathy; Dorsal root ganglion; MDL 28170; Tetrodotoxin resistant sodium channels

Indexed keywords

CALPAIN; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; [1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; CALPAIN INHIBITOR III; CALPASTATIN; DIPEPTIDE; GLYCOPROTEIN; NONSTEROID ANTIINFLAMMATORY AGENT; SODIUM CHANNEL;

ACTION POTENTIAL; ADULT; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD FLOW; BODY WEIGHT; CONTROLLED STUDY; DIABETIC NEUROPATHY; ELECTROPHYSIOLOGY; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; LATENT PERIOD; LIPID PEROXIDATION; MALE; NERVE CONDUCTION; NEUROMODULATION; NOCICEPTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT; SPINAL GANGLION; WHOLE CELL PATCH CLAMP; ANIMAL; CELL CULTURE; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DRUG EFFECTS; HYPERALGESIA; IMMUNOMODULATION; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; NOCICEPTIVE PAIN; PATCH CLAMP TECHNIQUE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CALPAIN; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; DIPEPTIDES; GANGLIA, SPINAL; GLYCOPROTEINS; HYPERALGESIA; MALE; MEMBRANE POTENTIALS; NEUROIMMUNOMODULATION; NEURONS; NOCICEPTIVE PAIN; OXIDATIVE STRESS; PATCH-CLAMP TECHNIQUES; RATS, SPRAGUE-DAWLEY; SODIUM CHANNELS;

EID: 84934941448     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.05.040     Document Type: Article

References (73)

1. H. Abriel, and R.S. Kass Regulation of the voltage-gated cardiac sodium channel Nav1.5 by interacting proteins Trends Cardiovasc. Med. 15 2005 35 40
2. E. Adamec, P. Mohan, J.P. Vonsattel, and R.A. Nixon Calpain activation in neurodegenerative diseases: confocal immunofluorescence study with antibodies specifically recognizing the active form of calpain 2 Acta Neuropathol. 104 2002 92 104
3. F. Amaya, I. Decosterd, T.A. Samad, C. Plumpton, S. Tate, R.J. Mannion, M. Costigan, and C.J. Woolf Diversity of expression of the sensory neuron-specific TTX-resistant voltage-gated sodium ion channels SNS and SNS2 Mol. Cell. Neurosci. 15 2000 331 342
4. M. Amini, C.L. Ma, R. Farazifard, G. Zhu, Y. Zhang, J. Vanderluit, J.S. Zoltewicz, F. Hage, J.M. Savitt, D.C. Lagace, R.S. Slack, J.C. Beique, M. Baudry, P.A. Greer, R. Bergeron, and D.S. Park Conditional disruption of calpain in the CNS alters dendrite morphology, impairs LTP, and promotes neuronal survival following injury J. Neurosci. 33 2013 5773 5784
5. I.M. Araujo, M.J. Verdasca, E.C. Leal, B.A. Bahr, A.F. Ambrosio, A.P. Carvalho, and C.M. Carvalho Early calpain-mediated proteolysis following AMPA receptor activation compromises neuronal survival in cultured hippocampal neurons J. Neurochem. 91 2004 1322 1331
6. B.A. Bahr, J. Bendiske, Q.B. Brown, S. Munirathinam, E. Caba, M. Rudin, S. Urwyler, A. Sauter, and G. Rogers Survival signaling and selective neuroprotection through glutamatergic transmission Exp. Neurol. 174 2002 37 47
7. R. Baron Peripheral neuropathic pain: from mechanisms to symptoms Clin. J. Pain 16 2000 S12 S20
8. R. Baron Mechanisms of disease: neuropathic pain - a clinical perspective Nat. Clin. Pract. Neurol. 2 2006 95 106
9. M. Baudry, M.M. Chou, and X. Bi Targeting calpain in synaptic plasticity Expert Opin. Ther. Targets 17 2013 579 592
10. A. Bierhaus, T. Fleming, S. Stoyanov, A. Leffler, A. Babes, C. Neacsu, S.K. Sauer, M. Eberhardt, M. Schnolzer, F. Lasitschka, W.L. Neuhuber, T.I. Kichko, I. Konrade, R. Elvert, W. Mier, V. Pirags, I.K. Lukic, M. Morcos, T. Dehmer, N. Rabbani, P.J. Thornalley, D. Edelstein, C. Nau, J. Forbes, P.M. Humpert, M. Schwaninger, D. Ziegler, D.M. Stern, M.E. Cooper, U. Haberkorn, M. Brownlee, P.W. Reeh, and P.P. Nawroth Methylglyoxal modification of Nav1.8 facilitates nociceptive neuron firing and causes hyperalgesia in diabetic neuropathy Nat. Med. 18 2012 926 933
11. W. Boehmerle, K. Zhang, M. Sivula, F.M. Heidrich, Y. Lee, S.E. Jordt, and B.E. Ehrlich Chronic exposure to paclitaxel diminishes phosphoinositide signaling by calpain-mediated neuronal calcium sensor-1 degradation Proc. Natl. Acad. Sci. U. S. A. 104 2007 11103 11108
12. H. Caner, J.L. Collins, S.M. Harris, N.F. Kassell, and K.S. Lee Attenuation of AMPA-induced neurotoxicity by a calpain inhibitor Brain Res. 607 1993 354 356
13. S.L. Chan, and M.P. Mattson Caspase and calpain substrates: roles in synaptic plasticity and cell death J. Neurosci. Res. 58 1999 167 190
14. P.K. Chatterjee, P.A. Brown, S. Cuzzocrea, K. Zacharowski, K.N. Stewart, H. Mota-Filipe, M.C. McDonald, and C. Thiemermann Calpain inhibitor-1 reduces renal ischemia/reperfusion injury in the rat Kidney Int. 59 2001 2073 2083
15. P.K. Chatterjee, Z. Todorovic, A. Sivarajah, H. Mota-Filipe, P.A. Brown, K.N. Stewart, E. Mazzon, S. Cuzzocrea, and C. Thiemermann Inhibitors of calpain activation (PD150606 and E-64) and renal ischemia-reperfusion injury Biochem. Pharmacol. 69 2005 1121 1131
16. B. Chen, Q. Zhao, R. Ni, F. Tang, L. Shan, I. Cepinskas, G. Cepinskas, W. Wang, P.W. Schiller, and T. Peng Inhibition of calpain reduces oxidative stress and attenuates endothelial dysfunction in diabetes Cardiovasc. Diabetol. 13 2014 88
17. A. Das, M.K. Guyton, A. Smith, G.T. Wallace, M.L. McDowell, D.D. Matzelle, S.K. Ray, and N.L. Banik Calpain inhibitor attenuated optic nerve damage in acute optic neuritis in rats J. Neurochem. 124 2012 133 146
18. S.D. Dib-Hajj, L. Tyrrell, T.R. Cummins, J.A. Black, P.M. Wood, and S.G. Waxman Two tetrodotoxin-resistant sodium channels in human dorsal root ganglion neurons FEBS Lett. 462 1999 117 120
19. S. England, S. Bevan, and R.J. Docherty PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade J. Physiol. 495 Pt 2 1996 429 440
20. J. Fjell, T.R. Cummins, S.D. Dib-Hajj, K. Fried, J.A. Black, and S.G. Waxman Differential role of GDNF and NGF in the maintenance of two TTX-resistant sodium channels in adult DRG neurons Brain Res. Mol. Brain Res. 67 1999 267 282
21. D.E. Goll, V.F. Thompson, H. Li, W. Wei, and J. Cong The calpain system Physiol. Rev. 83 2003 731 801
22. D.E. Goll, V.F. Thompson, R.G. Taylor, and T. Zalewska Is calpain activity regulated by membranes and autolysis or by calcium and calpastatin? Bioessays 14 1992 549 556
23. F. Harris, S. Biswas, J. Singh, S. Dennison, and D.A. Phoenix Calpains and their multiple roles in diabetes mellitus Ann. N. Y. Acad. Sci. 1084 2006 452 480
24. M. Hirade, H. Yasuda, M. Omatsu-Kanbe, R. Kikkawa, and H. Kitasato Tetrodotoxin-resistant sodium channels of dorsal root ganglion neurons are readily activated in diabetic rats Neuroscience 90 1999 933 939
25. S. Hong, T.J. Morrow, P.E. Paulson, L.L. Isom, and J.W. Wiley Early painful diabetic neuropathy is associated with differential changes in tetrodotoxin-sensitive and -resistant sodium channels in dorsal root ganglion neurons in the rat J. Biol. Chem. 279 2004 29341 29350
26. Y. Huang, and K.K. Wang The calpain family and human disease Trends Mol. Med. 7 2001 355 362
27. A. Iwata, P.K. Stys, J.A. Wolf, X.H. Chen, A.G. Taylor, D.F. Meaney, and D.H. Smith Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors J. Neurosci. 24 2004 4605 4613
28. M.F. Jarvis, P. Honore, C.C. Shieh, M. Chapman, S. Joshi, X.F. Zhang, M. Kort, W. Carroll, B. Marron, R. Atkinson, J. Thomas, D. Liu, M. Krambis, Y. Liu, S. McGaraughty, K. Chu, R. Roeloffs, C. Zhong, J.P. Mikusa, G. Hernandez, D. Gauvin, C. Wade, C. Zhu, M. Pai, M. Scanio, L. Shi, I. Drizin, R. Gregg, M. Matulenko, A. Hakeem, M. Gross, M. Johnson, K. Marsh, P.K. Wagoner, J.P. Sullivan, C.R. Faltynek, and D.S. Krafte A-803467, a potent and selective Nav1.8 sodium channel blocker, attenuates neuropathic and inflammatory pain in the rat Proc. Natl. Acad. Sci. U. S. A. 104 2007 8520 8525
29. N. Jette, E. Coderre, M.A. Nikolaeva, P.D. Enright, A. Iwata, D.H. Smith, Q. Jiang, and P.K. Stys Spatiotemporal distribution of spectrin breakdown products induced by anoxia in adult rat optic nerve in vitro J. Cereb. Blood Flow. Metab. 26 2006 777 786
30. A. Kumar, and S.S. Sharma NF-kappaB inhibitory action of resveratrol: a probable mechanism of neuroprotection in experimental diabetic neuropathy Biochem. Biophys. Res. Commun. 394 2010 360 365
31. S. Lankiewicz, C. Marc Luetjens, N. Truc Bui, A.J. Krohn, M. Poppe, G.M. Cole, T.C. Saido, and J.H. Prehn Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death J. Biol. Chem. 275 2000 17064 17071
32. F.Y. Lee, D.W. Kim, J.A. Karmin, D. Hong, S.S. Chang, M. Fujisawa, H. Takayanagi, L.U. Bigliani, T.A. Blaine, and H.J. Lee mu-Calpain regulates receptor activator of NF-kappaB ligand (RANKL)-supported osteoclastogenesis via NF-kappaB activation in RAW 264.7 cells J. Biol. Chem. 280 2005 29929 29936
33. J. Li, F. Grynspan, S. Berman, R. Nixon, and S. Bursztajn Regional differences in gene expression for calcium activated neutral proteases (calpains) and their endogenous inhibitor calpastatin in mouse brain and spinal cord J. Neurobiol. 30 1996 177 191
34. X. Li, Y. Li, L. Shan, E. Shen, R. Chen, and T. Peng Over-expression of calpastatin inhibits calpain activation and attenuates myocardial dysfunction during endotoxaemia Cardiovasc. Res. 83 2009 72 79
35. X. Li, R. Luo, R. Chen, L. Song, S. Zhang, W. Hua, and H. Chen Cleavage of IkappaBalpha by calpain induces myocardial NF-kappaB activation, TNF-alpha expression, and cardiac dysfunction in septic mice Am. J. Physiol. Heart Circ. Physiol. 306 2014 H833 H843
36. Y. Li, Y. Li, Q. Feng, M. Arnold, and T. Peng Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes Cardiovasc. Res. 84 2009 100 110
37. Z. Li, E.L. Hogan, and N.L. Banik Role of calpain in spinal cord injury: increased calpain immunoreactivity in rat spinal cord after impact trauma Neurochem. Res. 21 1996 441 448
38. T.L. Liu, H. Shimada, T. Ochiai, T. Shiratori, S.E. Lin, M. Kitagawa, K. Harigaya, M. Maki, M. Oka, T. Abe, M. Takiguchi, and T. Hiwasa Enhancement of chemosensitivity toward peplomycin by calpastatin-stabilized NF-kappaB p65 in esophageal carcinoma cells: possible involvement of Fas/Fas-L synergism Apoptosis 11 2006 1025 1037
39. R.M. LoPachin, and E.J. Lehning The relevance of axonal swellings and atrophy to gamma-diketone neurotoxicity: a forum position paper Neurotoxicology 18 1997 7 22
40. M. Ma, T.A. Ferguson, K.M. Schoch, J. Li, Y. Qian, F.S. Shofer, K.E. Saatman, and R.W. Neumar Calpains mediate axonal cytoskeleton disintegration during Wallerian degeneration Neurobiol. Dis. 56 2013 34 46
41. V.A. Maltsev, and A.I. Undrovinas A multi-modal composition of the late Na+ current in human ventricular cardiomyocytes Cardiovasc. Res. 69 2006 116 127
42. M.P. Mattson Excitotoxic and excitoprotective mechanisms: abundant targets for the prevention and treatment of neurodegenerative disorders Neuromolecular Med. 3 2003 65 94
43. R. Meerupally, J.N. Singh, and S.S. Sharma Diabetic-induced increased sodium channel activity attenuated by tetracaine in sensory neurons in vitro Biochem. Biophys. Res. Commun. 453 2014 296 301
44. B. Meldrum, and J. Garthwaite Excitatory amino acid neurotoxicity and neurodegenerative disease Trends Pharmacol. Sci. 11 1990 379 387
45. A. Mouatt-Prigent, J.O. Karlsson, Y. Agid, and E.C. Hirsch Increased M-calpain expression in the mesencephalon of patients with Parkinson's disease but not in other neurodegenerative disorders involving the mesencephalon: a role in nerve cell death? Neuroscience 73 1996 979 987
46. M.R. Nangle, M.A. Cotter, and N.E. Cameron The calpain inhibitor, A-705253, corrects penile nitrergic nerve dysfunction in diabetic mice Eur. J. Pharmacol. 538 2006 148 153
47. G. Negi, A. Kumar, R.K. Kaundal, A. Gulati, and S.S. Sharma Functional and biochemical evidence indicating beneficial effect of melatonin and nicotinamide alone and in combination in experimental diabetic neuropathy Neuropharmacology 58 2009 585 592
48. G. Negi, A. Kumar, and S.S. Sharma Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades J. Pineal Res. 50 2011 124 131
49. G. Negi, A. Kumar, and S.S. Sharma Nrf2 and NF-kappaB modulation by sulforaphane counteracts multiple manifestations of diabetic neuropathy in rats and high glucose-induced changes Curr. Neurovasc. Res. 8 2011 294 304
50. G. Negi, and S.S. Sharma Inhibition of IkappaB kinase (IKK) protects against peripheral nerve dysfunction of experimental diabetes Mol. Neurobiol. 51 2015 591 598
51. R.W. Neumar, Y.A. Xu, H. Gada, R.P. Guttmann, and R. Siman Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis J. Biol. Chem. 278 2003 14162 14167
52. F.T. Nickel, F. Seifert, S. Lanz, and C. Maihofner Mechanisms of neuropathic pain Eur. Neuropsychopharmacol. 22 2011 81 91
53. R.A. Nixon Calcium-activated neutral proteinases as regulators of cellular function. Implications for Alzheimer's disease pathogenesis Ann. N. Y. Acad. Sci. 568 1989 198 208
54. R.A. Nixon, K.I. Saito, F. Grynspan, W.R. Griffin, S. Katayama, T. Honda, P.S. Mohan, T.B. Shea, and M. Beermann Calcium-activated neutral proteinase (calpain) system in aging and Alzheimer's disease Ann. N. Y. Acad. Sci. 747 1994 77 91
55. C. Paillart, J.L. Boudier, J.A. Boudier, H. Rochat, F. Couraud, and B. Dargent Activity-induced internalization and rapid degradation of sodium channels in cultured fetal neurons J. Cell. Biol. 134 1996 499 509
56. S.K. Ray, D.D. Matzelle, G.G. Wilford, E.L. Hogan, and N.L. Banik Increased calpain expression is associated with apoptosis in rat spinal cord injury: calpain inhibitor provides neuroprotection Neurochem. Res. 25 2000 1191 1198
57. S.K. Ray, G.G. Wilford, S.F. Ali, and N.L. Banik Calpain upregulation in spinal cords of mice with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinson's disease Ann. N. Y. Acad. Sci. 914 2000 275 283
58. S. Reijonen, J.P. Kukkonen, A. Hyrskyluoto, J. Kivinen, M. Kairisalo, N. Takei, D. Lindholm, and L. Korhonen Downregulation of NF-kappaB signaling by mutant huntingtin proteins induces oxidative stress and cell death Cell. Mol. Life Sci. 67 2010 1929 1941
59. K.E. Saatman, H. Murai, R.T. Bartus, D.H. Smith, N.J. Hayward, B.R. Perri, and T.K. McIntosh Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat Proc. Natl. Acad. Sci. U. S. A. 93 1996 3428 3433
60. S. Samantaray, V.H. Knaryan, D.C. Shields, and N.L. Banik Critical role of calpain in spinal cord degeneration in Parkinson's disease J. Neurochem. 127 2013 880 890
61. S. Samantaray, K.S. Patel, V.H. Knaryan, N.P. Thakore, S. Roudabush, J.H. Heissenbuttle, H.C. Becker, and N.L. Banik Calpain inhibition prevents ethanol-induced alterations in spinal motoneurons Neurochem. Res. 38 2013 1734 1741
62. A.Y. Shanab, T. Nakazawa, M. Ryu, Y. Tanaka, N. Himori, K. Taguchi, M. Yasuda, R. Watanabe, J. Takano, T. Saido, N. Minegishi, T. Miyata, T. Abe, and M. Yamamoto Metabolic stress response implicated in diabetic retinopathy: the role of calpain, and the therapeutic impact of calpain inhibitor Neurobiol. Dis. 48 2012 556 567
63. J. Shen, P. Channavajhala, D.C. Seldin, and G.E. Sonenshein Phosphorylation by the protein kinase CK2 promotes calpain-mediated degradation of IkappaBalpha J. Immunol. 167 2001 4919 4925
64. R. Siman, D. Bozyczko-Coyne, M.J. Savage, and J.M. Roberts-Lewis The calcium-activated protease calpain I and ischemia-induced neurodegeneration Adv. Neurol. 71 1996 167 174 Discussion 174-165
65. J.N. Singh, G. Jain, P. Ramarao, and S.S. Sharma Inhibition of sodium current by carbamazepine in dorsal root ganglion neurons in vitro Indian J. Physiol. Pharmacol. 53 2009 147 154
66. J.N. Singh, G. Jain, and S.S. Sharma In vitro hyperglycemia enhances sodium currents in dorsal root ganglion neurons: an effect attenuated by carbamazepine Neuroscience 232 2013 64 73
67. A. Undrovinas, V.A. Maltsev, and H.N. Sabbah Calpain inhibition reduces amplitude and accelerates decay of the late sodium current in ventricular myocytes from dogs with chronic heart failure PLoS One 8 2013 e54436
68. C.R. von Reyn, J.M. Spaethling, M.N. Mesfin, M. Ma, R.W. Neumar, D.H. Smith, R. Siman, and D.F. Meaney Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit J. Neurosci. 29 2009 10350 10356
69. K.K. Wang Calpain and caspase: can you tell the difference? Trends Neurosci. 23 2000 20 26
70. S.G. Waxman, S. Dib-Hajj, T.R. Cummins, and J.A. Black Sodium channels and pain Proc. Natl. Acad. Sci. U. S. A. 96 1999 7635 7639
71. S.G. Waxman, and M. Estacion Nav1.9, G-proteins, and nociceptors J. Physiol. 586 2008 917 918
72. D. Yang, S. Ma, Y. Tan, D. Li, B. Tang, X. Zhang, M. Sun, and Y. Yang Increased expression of calpain and elevated activity of calcineurin in the myocardium of patients with congestive heart failure Int. J. Mol. Med. 26 2010 159 164
73. Y. Zang, S.X. Chen, G.J. Liao, H.Q. Zhu, X.H. Wei, Y. Cui, X.D. Na, R.P. Pang, W.J. Xin, L.J. Zhou, and X.G. Liu Calpain-2 contributes to neuropathic pain following motor nerve injury via up-regulating interleukin-6 in DRG neurons Brain Behav. Immun. 44 2015 37 47