Naringenin reduces inflammatory pain in mice

Neuropharmacology

Volumn 105, Issue , 2016, Pages 508-519

  Pinho Ribeiro, Felipe A ^a   Zarpelon, Ana C ^a   Fattori, Victor ^a   Manchope, Marília F ^a   Mizokami, Sandra S ^a   Casagrande, Rubia ^a   Verri, Waldiceu A ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

Author keywords

Carrageenan; Cytokines; Hyperalgesia; NF B; Overt pain

Indexed keywords

DIPYRONE; INDOMETACIN; INTERLEUKIN 1BETA; INTERLEUKIN 23; NARINGENIN; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ANALGESIC AGENT; CYTOKINE; FLAVANONE DERIVATIVE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

ANALGESIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; INFLAMMATORY PAIN; MALE; MECHANICAL HYPERALGESIA; MOUSE; NEUROPATHIC PAIN; NONHUMAN; OXIDATIVE STRESS; PAIN INTENSITY; PRIORITY JOURNAL; ANIMAL; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; HYPERALGESIA; INTRAPERITONEAL DRUG ADMINISTRATION; LIVER; METABOLISM; MOTOR ACTIVITY; NEUTROPHIL; PAIN RECEPTOR; STOMACH; VISCERAL PAIN;

ANALGESICS; ANIMALS; CYTOKINES; DIPYRONE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLAVANONES; HYPERALGESIA; INDOMETHACIN; INJECTIONS, INTRAPERITONEAL; KATP CHANNELS; LIVER; MALE; MICE; MOTOR ACTIVITY; NEUTROPHILS; NF-KAPPA B; NOCICEPTORS; STOMACH; VISCERAL PAIN;

EID: 84961662283     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.02.019     Document Type: Article

References (70)

1. S.S. Al-Rejaie, A.M. Aleisa, H.M. Abuohashish, M.Y. Parmar, M.S. Ola, A.A. Al-Hosaini, and M.M. Ahmed Naringenin neutralises oxidative stress and nerve growth factor discrepancy in experimental diabetic neuropathy Neurol. Res. 37 2015 924 933
2. D. Alves, and I. Duarte Involvement of ATP-sensitive K(+) channels in the peripheral antinociceptive effect induced by dipyrone Eur. J. Pharmacol. 444 2002 47 52
3. A.M. Binshtok, H. Wang, K. Zimmermann, F. Amaya, D. Vardeh, L. Shi, G.J. Brenner, R.R. Ji, B.P. Bean, C.J. Woolf, and T.A. Samad Nociceptors are interleukin-1beta sensors J. Neurosci. 28 2008 14062 14073
4. S.M. Borghi, T.T. Carvalho, L. Staurengo-Ferrari, M.S. Hohmann, P. Pinge-Filho, R. Casagrande, and W.A. Verri Jr. Vitexin inhibits inflammatory pain in mice by targeting TRPV1, oxidative stress, and cytokines J. Nat. Prod. 76 2013 1141 1149
5. M.J. Caterina, M.A. Schumacher, M. Tominaga, T.A. Rosen, J.D. Levine, and D. Julius The capsaicin receptor: A heat-activated ion channel in the pain pathway Nature 389 1997 816 824
6. M. Cavia-Saiz, M.D. Busto, M.C. Pilar-Izquierdo, N. Ortega, M. Perez-Mateos, and P. Muniz Antioxidant properties, radical scavenging activity and biomolecule protection capacity of flavonoid naringenin and its glycoside naringin: A comparative study J. Sci. Food Agric. 90 2010 1238 1244
7. T.M. Cunha, G.R. Souza, A.C. Domingues, E.U. Carreira, C.M. Lotufo, M.I. Funez, W.A. Verri Jr., F.Q. Cunha, and S.H. Ferreira Stimulation of peripheral kappa opioid receptors inhibits inflammatory hyperalgesia via activation of the PI3Kgamma/AKT/nNOS/NO signaling pathway Mol. Pain 8 2012 10
8. T.M. Cunha, W.A. Verri Jr., J.S. Silva, S. Poole, F.Q. Cunha, and S.H. Ferreira A cascade of cytokines mediates mechanical inflammatory hypernociception in mice Proc. Natl. Acad. Sci. U. S. A. 102 2005 1755 1760
9. T.M. Cunha, W.A. Verri Jr., G.G. Vivancos, I.F. Moreira, S. Reis, C.A. Parada, F.Q. Cunha, and S.H. Ferreira An electronic pressure-meter nociception paw test for mice Braz. J. Med. Biol. Res. 37 2004 401 407
10. S. Cuzzocrea, B. Pisano, L. Dugo, A. Ianaro, M. Ndengele, and D. Salvemini Superoxide-related signaling cascade mediates nuclear factor-kappaB activation in acute inflammation Antioxid. Redox Signal 6 2004 699 704
11. D. Dal Secco, A.P. Moreira, A. Freitas, J.S. Silva, M.A. Rossi, S.H. Ferreira, and F.Q. Cunha Nitric oxide inhibits neutrophil migration by a mechanism dependent on ICAM-1: Role of soluble guanylate cyclase Nitric Oxide 15 2006 77 86
12. W. Dou, J. Zhang, A. Sun, E. Zhang, L. Ding, S. Mukherjee, X. Wei, G. Chou, Z.T. Wang, and S. Mani Protective effect of naringenin against experimental colitis via suppression of toll-like receptor 4/NF-kappaB signalling Br. J. Nutr. 110 2013 599 608
13. V. Fattori, F.A. Pinho-Ribeiro, S.M. Borghi, J.C. Alves-Filho, T.M. Cunha, F.Q. Cunha, R. Casagrande, and W.A. Verri Jr. Curcumin inhibits superoxide anion-induced pain-like behavior and leukocyte recruitment by increasing Nrf2 expression and reducing NF-kappaB activation Inflamm. Res. 64 2015 993 1003
14. J.P. Gilligan, S.J. Lovato, M.D. Erion, and A.Y. Jeng Modulation of carrageenan-induced hind paw edema by substance P Inflammation 18 1994 285 292
15. D. Gruber-Schoffnegger, R. Drdla-Schutting, C. Honigsperger, G. Wunderbaldinger, M. Gassner, and J. Sandkuhler Induction of thermal hyperalgesia and synaptic long-term potentiation in the spinal cord lamina I by TNF-alpha and IL-1beta is mediated by glial cells J. Neurosci. 33 2013 6540 6551
16. S. Gudes, O. Barkai, Y. Caspi, B. Katz, S. Lev, and A.M. Binshtok The role of slow and persistent TTX-resistant sodium currents in acute tumor necrosis factor-alpha-mediated increase in nociceptors excitability J. Neurophysiol. 113 2015 601 619
17. A.T. Guerrero, W.A. Verri Jr., T.M. Cunha, T.A. Silva, I.R. Schivo, D. Dal-Secco, C. Canetti, F.A. Rocha, C.A. Parada, F.Q. Cunha, and S.H. Ferreira Involvement of LTB4 in zymosan-induced joint nociception in mice: Participation of neutrophils and PGE2 J. Leukoc. Biol. 83 2008 122 130
18. A. Guo, D. He, H.B. Xu, C.A. Geng, and J. Zhao Promotion of regulatory T cell induction by immunomodulatory herbal medicine licorice and its two constituents Sci. Rep. 5 2015 14046
19. P. Hasanein, and F. Fazeli Role of naringenin in protection against diabetic hyperalgesia and tactile allodynia in male Wistar rats J. Physiol. Biochem. 70 2014 997 1006
20. C.Y. Hu, and Y.T. Zhao Analgesic effects of naringenin in rats with spinal nerve ligation-induced neuropathic pain Biomed. Rep. 2 2014 569 573
21. M. Jamaluddin, S. Wang, I. Boldogh, B. Tian, and A.R. Brasier TNF-alpha-induced NF-kappaB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway Cell Signal 19 2007 1419 1433
22. X. Jin, and R.W. Gereau Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha J. Neurosci. 26 2006 246 255
23. D. Julius TRP channels and pain Annu. Rev. Cell Dev. Biol. 29 2013 355 384
24. S. Kaulaskar, P. Bhutada, A. Rahigude, D. Jain, and U. Harle Effects of naringenin on allodynia and hyperalgesia in rats with chronic constriction injury-induced neuropathic pain Zhong Xi Yi Jie He Xue Bao 10 2012 1482 1489
25. Y. Kawasaki, L. Zhang, J.K. Cheng, and R.R. Ji Cytokine mechanisms of central sensitization: Distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord J. Neurosci. 28 2008 5189 5194
26. M.M. Khattab TEMPOL, a membrane-permeable radical scavenger, attenuates peroxynitrite- A nd superoxide anion-enhanced carrageenan-induced paw edema and hyperalgesia: A key role for superoxide anion Eur. J. Pharmacol. 548 2006 167 173
27. H.Y. Kim, J.M. Chung, and K. Chung Increased production of mitochondrial superoxide in the spinal cord induces pain behaviors in mice: The effect of mitochondrial electron transport complex inhibitors Neurosci. Lett. 447 2008 87 91
28. J. Kim, Y.N. Cha, and Y.J. Surh A protective role of nuclear factor-erythroid 2-related factor-2 (Nrf2) in inflammatory disorders Mutat. Res. 690 2010 12 23
29. B. Liu, L. Fan, S. Balakrishna, A. Sui, J.B. Morris, and S.E. Jordt TRPM8 is the principal mediator of menthol-induced analgesia of acute and inflammatory pain Pain 154 2013 2169 2177
30. H. Lou, X. Jing, X. Wei, H. Shi, D. Ren, and X. Zhang Naringenin protects against 6-OHDA-induced neurotoxicity via activation of the Nrf2/ARE signaling pathway Neuropharmacology 79 2014 380 388
31. O.H. Lowry, N.J. Rosebrough, A.L. Farr, and R.J. Randall Protein measurement with the Folin phenol reagent J. Biol. Chem. 193 1951 265 275
32. D.A. Magro, M.S. Hohmann, S.S. Mizokami, T.M. Cunha, J.C. Alves-Filho, R. Casagrande, S.H. Ferreira, F.Y. Liew, F.Q. Cunha, and W.A. Verri Jr. An interleukin-33/ST2 signaling deficiency reduces overt pain-like behaviors in mice Braz. J. Med. Biol. Res. 46 2013 601 606
33. C. Maihofner, C. Euchenhofer, I. Tegeder, K.F. Beck, J. Pfeilschifter, and G. Geisslinger Regulation and immunohistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation Neurosci. Lett. 290 2000 71 75
34. R.M. Martinez, F.A. Pinho-Ribeiro, V.S. Steffen, C.V. Caviglione, J.A. Vignoli, D.S. Barbosa, M.M. Baracat, S.R. Georgetti, W.A. Verri Jr., and R. Casagrande Naringenin inhibits UVB irradiation-induced inflammation and oxidative stress in the skin of hairless mice J. Nat. Prod. 78 2015 1647 1655
35. C.R. McNamara, J. Mandel-Brehm, D.M. Bautista, J. Siemens, K.L. Deranian, M. Zhao, N.J. Hayward, J.A. Chong, D. Julius, M.M. Moran, and C.M. Fanger TRPA1 mediates formalin-induced pain Proc. Natl. Acad. Sci. U. S. A. 104 2007 13525 13530
36. S.S. Mizokami, N.S. Arakawa, S.R. Ambrosio, A.C. Zarpelon, R. Casagrande, T.M. Cunha, S.H. Ferreira, F.Q. Cunha, and W.A. Verri Jr. Kaurenoic acid from Sphagneticola trilobata inhibits inflammatory pain: Effect on cytokine production and activation of the NO-cyclic GMP-protein kinase G-ATP-sensitive potassium channel signaling pathway J. Nat. Prod. 75 2012 896 904
37. N. Nakagawa, H. Sano, and I. Iwamoto Substance P induces the expression of intercellular adhesion molecule-1 on vascular endothelial cells and enhances neutrophil transendothelial migration Peptides 16 1995 721 725
38. R. Nassini, C. Fusi, S. Materazzi, E. Coppi, T. Tuccinardi, I.M. Marone, F. De Logu, D. Preti, R. Tonello, A. Chiarugi, R. Patacchini, P. Geppetti, and S. Benemei The TRPA1 channel mediates the analgesic action of dipyrone and pyrazolone derivatives Br. J. Pharmacol. 172 2015 3397 3411
39. M.M. Ndengele, S. Cuzzocrea, E. Esposito, E. Mazzon, R. Di Paola, G.M. Matuschak, and D. Salvemini Cyclooxygenases 1 and 2 contribute to peroxynitrite-mediated inflammatory pain hypersensitivity FASEB J. 22 2008 3154 3164
40. S.A. Palma-Duran, G. Caire-Juvera, R. Robles-Burgeno Mdel, M.I. Ortega-Velez, L. Gutierrez-Coronado Mde, C. Bermudez Almada Mdel, K. Chavez-Suarez, M. Campa-Siqueiros, P. Grajeda-Cota, S. Saucedo-Tamayo Mdel, and A.I. Valenzuela-Quintanar Serum levels of phytoestrogens as biomarkers of intake in Mexican women Int. J. Food Sci. Nutr. 66 2015 819 825
41. H.Y. Park, G.Y. Kim, and Y.H. Choi Naringenin attenuates the release of pro-inflammatory mediators from lipopolysaccharide-stimulated BV2 microglia by inactivating nuclear factor-kappaB and inhibiting mitogen-activated protein kinases Int. J. Mol. Med. 30 2012 204 210
42. H.A. Paula-Neto, J.C. Alves-Filho, F.O. Souto, F. Spiller, R.S. Amendola, A. Freitas, F.Q. Cunha, and C. Barja-Fidalgo Inhibition of guanylyl cyclase restores neutrophil migration and maintains bactericidal activity increasing survival in sepsis Shock 35 2011 17 27
43. M.I. Possebon, S.S. Mizokami, T.T. Carvalho, A.C. Zarpelon, M.S. Hohmann, L. Staurengo-Ferrari, C.R. Ferraz, T.H. Hayashida, A.R. de Souza, S.R. Ambrosio, N.S. Arakawa, R. Casagrande, and W.A. Verri Jr. Pimaradienoic acid inhibits inflammatory pain: Inhibition of NF-kappaB activation and cytokine production and activation of the NO-cyclic GMP-protein kinase G-ATP-sensitive potassium channel signaling pathway J. Nat. Prod. 77 2014 2488 2496
44. S.S. Raza, M.M. Khan, A. Ahmad, M. Ashafaq, F. Islam, A.P. Wagner, M.M. Safhi, and F. Islam Neuroprotective effect of naringenin is mediated through suppression of NF-kappaB signaling pathway in experimental stroke Neuroscience 230 2013 157 171
45. K.W. Ruiz-Miyazawa, F.A. Pinho-Ribeiro, A.C. Zarpelon, L. Staurengo-Ferrari, R.L. Silva, J.C. Alves-Filho, T.M. Cunha, F.Q. Cunha, R. Casagrande, and W.A. Verri Jr. Vinpocetine reduces lipopolysaccharide-induced inflammatory pain and neutrophil recruitment in mice by targeting oxidative stress, cytokines and NF-kappaB Chem. Biol. Interact. 237 2015 9 17
46. D. Sachs, F.Q. Cunha, and S.H. Ferreira Peripheral analgesic blockade of hypernociception: Activation of arginine/NO/cGMP/protein kinase G/ATP-sensitive K+ channel pathway Proc. Natl. Acad. Sci. U. S. A. 101 2004 3680 3685
47. T. Santodomingo-Garzon, T.M. Cunha, W.A. Verri Jr., D.A. Valerio, C.A. Parada, S. Poole, S.H. Ferreira, and F.Q. Cunha Atorvastatin inhibits inflammatory hypernociception Br. J. Pharmacol. 149 2006 14 22
48. A. Schmidtko, I. Tegeder, and G. Geisslinger No no, no pain? the role of nitric oxide and cGMP in spinal pain processing Trends Neurosci. 32 2009 339 346
49. T.J. Shi, K. Holmberg, Z.Q. Xu, H. Steinbusch, J. de Vente, and T. Hokfelt Effect of peripheral nerve injury on cGMP and nitric oxide synthase levels in rat dorsal root ganglia: Time course and coexistence Pain 78 1998 171 180
50. B. St-Jacques, and W. Ma Peripheral prostaglandin E2 prolongs the sensitization of nociceptive dorsal root ganglion neurons possibly by facilitating the synthesis and anterograde axonal trafficking of EP4 receptors Exp. Neurol. 261 2014 354 366
51. L. Staurengo-Ferrari, S.S. Mizokami, V. Fattori, J.J. Silva, P.G. Zanichelli, S.R. Georgetti, M.M. Baracat, L.G. da Franca, W.R. Pavanelli, R. Casagrande, and W.A. Verri Jr. The ruthenium nitric oxide donor, [Ru(HEDTA)NO], inhibits acute nociception in mice by modulating oxidative stress, cytokine production and activating the cGMP/PKG/ATP-sensitive potassium channel signaling pathway Naunyn Schmiedeb. Arch. Pharmacol. 387 2014 1053 1068
52. A.A. Steiner, L.G. Branco, F.Q. Cunha, and S.H. Ferreira Role of the haeme oxygenase/carbon monoxide pathway in mechanical nociceptor hypersensitivity Br. J. Pharmacol. 132 2001 1673 1682
53. I. Straub, F. Mohr, J. Stab, M. Konrad, S.E. Philipp, J. Oberwinkler, and M. Schaefer Citrus fruit and fabacea secondary metabolites potently and selectively block TRPM3 Br. J. Pharmacol. 168 2013 1835 1850
54. H. Suleyman, B. Demircan, and Y. Karagoz Anti-inflammatory and side effects of cyclooxygenase inhibitors Pharmacol. Rep. 59 2007 247 258
55. E. Ting, A.T. Guerrero, T.M. Cunha, W.A. Verri Jr., S.M. Taylor, T.M. Woodruff, F.Q. Cunha, and S.H. Ferreira Role of complement C5a in mechanical inflammatory hypernociception: Potential use of C5a receptor antagonists to control inflammatory pain Br. J. Pharmacol. 153 2008 1043 1053
56. D.A. Valerio, T.M. Cunha, N.S. Arakawa, H.P. Lemos, F.B. Da Costa, C.A. Parada, S.H. Ferreira, F.Q. Cunha, and W.A. Verri Jr. Anti-inflammatory and analgesic effects of the sesquiterpene lactone budlein A in mice: Inhibition of cytokine production-dependent mechanism Eur. J. Pharmacol. 562 2007 155 163
57. W.A. Verri Jr., T.M. Cunha, D.A. Magro, A.C. Domingues, S.M. Vieira, G.R. Souza, F.Y. Liew, S.H. Ferreira, and F.Q. Cunha Role of IL-18 in overt pain-like behaviour in mice Eur. J. Pharmacol. 588 2008 207 212
58. W.A. Verri Jr., T.M. Cunha, D.A. Magro, A.T. Guerrero, S.M. Vieira, V. Carregaro, G.R. Souza, M. Henriques, S.H. Ferreira, and F.Q. Cunha Targeting endothelin ETA and ETB receptors inhibits antigen-induced neutrophil migration and mechanical hypernociception in mice Naunyn Schmiedeb. Arch. Pharmacol. 379 2009 271 279
59. W.A. Verri Jr., T.M. Cunha, C.A. Parada, S. Poole, F.Q. Cunha, and S.H. Ferreira Hypernociceptive role of cytokines and chemokines: Targets for analgesic drug development? Pharmacol. Ther. 112 2006 116 138
60. W.A. Verri Jr., F.O. Souto, S.M. Vieira, S.C. Almeida, S.Y. Fukada, D. Xu, J.C. Alves-Filho, T.M. Cunha, A.T. Guerrero, R.B. Mattos-Guimaraes, F.R. Oliveira, M.M. Teixeira, J.S. Silva, I.B. McInnes, S.H. Ferreira, P. Louzada-Junior, F.Y. Liew, and F.Q. Cunha IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy Ann. Rheum. Dis. 69 2010 1697 1703
61. W.A. Verri Jr., F.T.M.C. Vicentini, M.M. Baracat, S.R. Georgetti, R.D. Cardoso, C.T. M, S.H. Ferreira, F.Q. Cunha, M.J. Fonseca, and R. Casagrande Flavonoids as anti-inflammatory and analgesic drugs: Mechanisms of action and perspectives in the development of pharmaceutical forms A.U. Rahman, Studies in Natural Products Chemistry 2012 Elsevier Amsterdam 297 330
62. J. Vriens, G. Owsianik, T. Hofmann, S.E. Philipp, J. Stab, X. Chen, M. Benoit, F. Xue, A. Janssens, S. Kerselaers, J. Oberwinkler, R. Vennekens, T. Gudermann, B. Nilius, and T. Voets TRPM3 is a nociceptor channel involved in the detection of noxious heat Neuron 70 2011 482 494
63. J. Wang, L.C. Zhang, Y.W. Lv, Y. Ji, X.J. Yan, and J.P. Xue Involvement of the nitric oxide-cyclic GMP-protein kinase G-K+ channel pathway in the antihyperalgesic effects of bovine lactoferrin in a model of neuropathic pain Brain Res. 1209 2008 1 7
64. Z.Q. Wang, F. Porreca, S. Cuzzocrea, K. Galen, R. Lightfoot, E. Masini, C. Muscoli, V. Mollace, M. Ndengele, H. Ischiropoulos, and D. Salvemini A newly identified role for superoxide in inflammatory pain J. Pharmacol. Exp. Ther. 309 2004 869 878
65. C.J. Woolf, A. Allchorne, B. Safieh-Garabedian, and S. Poole Cytokines, nerve growth factor and inflammatory hyperalgesia: The contribution of tumour necrosis factor alpha Br. J. Pharmacol. 121 1997 417 424
66. F.Y. Yamacita-Borin, A.C. Zarpelon, F.A. Pinho-Ribeiro, V. Fattori, J.C. Alves-Filho, F.Q. Cunha, T.M. Cunha, R. Casagrande, and W.A. Verri Jr. Superoxide anion-induced pain and inflammation depends on TNFalpha/TNFR1 signaling in mice Neurosci. Lett. 605 2015 53 58
67. J. Yu, L. Wang, R.L. Walzem, E.G. Miller, L.M. Pike, and B.S. Patil Antioxidant activity of citrus limonoids, flavonoids, and coumarins J. Agric. Food Chem. 53 2005 2009 2014
68. A.C. Zarpelon, T.M. Cunha, J.C. Alves-Filho, L.G. Pinto, S.H. Ferreira, I.B. McInnes, D. Xu, F.Y. Liew, F.Q. Cunha, and W.A. Verri Jr. IL-33/ST2 signalling contributes to carrageenin-induced innate inflammation and inflammatory pain: Role of cytokines, endothelin-1 and prostaglandin E2 Br. J. Pharmacol. 169 2013 90 101
69. A.C. Zarpelon, F.C. Rodrigues, A.H. Lopes, G.R. Souza, T.T. Carvalho, L.G. Pinto, D. Xu, S.H. Ferreira, J.C. Alves-Filho, I.B. McInnes, B. Ryffel, V.F. Quesniaux, F. Reverchon, S. Mortaud, A. Menuet, F.Y. Liew, F.Q. Cunha, T.M. Cunha, and W.A. Verri Jr. Spinal cord oligodendrocyte-derived alarmin IL-33 mediates neuropathic pain FASEB J. 30 2016 54 65
70. W.C. Zhao, B. Zhang, M.J. Liao, W.X. Zhang, W.Y. He, H.B. Wang, and C.X. Yang Curcumin ameliorated diabetic neuropathy partially by inhibition of NADPH oxidase mediating oxidative stress in the spinal cord Neurosci. Lett. 560 2014 81 85