NADPH-oxidase 2 activation promotes opioid-induced antinociceptive tolerance in mice

Neuroscience

Volumn 241, Issue , 2013, Pages 1-9

  Doyle, T ^a   Esposito, E ^b   Bryant, L ^a   Cuzzocrea, S ^b,c   Salvemini, D ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MESSINA   (Italy)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Antinociceptive tolerance; Morphine; NADPH oxidase; Neuroinflammation; Superoxide

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 4; MANGANESE SUPEROXIDE DISMUTASE; OPIATE; PROTEIN P47; PROTEIN P47 PHOX; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; UNCLASSIFIED DRUG;

ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CATALYSIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SYNTHESIS; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SPINAL CORD;

ANALGESICS, OPIOID; ANIMALS; DRUG TOLERANCE; ENZYME ACTIVATION; INFLAMMATION; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MORPHINE; NADPH OXIDASE; PAIN; PEROXYNITROUS ACID; SPINAL CORD; SUPEROXIDE DISMUTASE;

EID: 84876339519     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.02.042     Document Type: Article

References (72)

1. Anilkumar N., Weber R., Zhang M., Brewer A., Shah A.M. Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 2008, 28:1347-1354.
2. Arner S., Rawal N., Gustafsson L.L. Clinical experience of long-term treatment with epidural and intrathecal opioids - a nationwide survey. Acta Anaesthesiol Scand 1988, 32:253-259.
3. Bae Y.S., Lee J.H., Choi S.H., Kim S., Almazan F., Witztum J.L., Miller Y.I. Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein. Circ Res 2009, 104:210-218.
4. Bánfi B., Molnár G., Maturana A., Steger K., Hegedûs B., Demaurex N., Krause K.-H. A Ca2+-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 2001, 276:37594-37601.
5. Batinic-Haberle I., Ndengele M.M., Cuzzocrea S., Reboucas J.S., Spasojevic I., Salvemini D. Lipophilicity is a critical parameter that dominates the efficacy of metalloporphyrins in blocking the development of morphine antinociceptive tolerance through peroxynitrite-mediated pathways. Free Radic Biol Med 2009, 46:212-219.
6. Beattie E.C., Stellwagen D., Morishita W., Bresnahan J.C., Ha B.K., Von Zastrow M., Beattie M.S., Malenka R.C. Control of synaptic strength by glial TNFalpha. Science 2002, 295:2282-2285.
7. Beckman J.S., Beckman T.W., Chen J., Marshall P.A., Freeman B.A. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci U S A 1990, 87:1620-1624.
8. Bedard K., Krause K.H. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007, 87:245-313.
9. Brennan A.M., Suh S.W., Won S.J., Narasimhan P., Kauppinen T.M., Lee H., Edling Y., Chan P.H., Swanson R.A. NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation. Nat Neurosci 2009, 12:857-863.
10. Castro L., Demicheli V., Tortora V., Radi R. Mitochondrial protein tyrosine nitration. Free Radic Res 2011, 45:37-52.
11. Christie M.J. Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br J Pharmacol 2008, 154:384-396.
12. D'Amour F. A method for determining loss of pain sensation. J Pharmacol Exp Ther 1941, 72:74-79.
13. Dang V.C., Christie M.J. Mechanisms of rapid opioid receptor desensitization, resensitization and tolerance in brain neurons. Br J Pharmacol 2012, 165:1704-1716.
14. Dickinson B.C., Peltier J., Stone D., Schaffer D.V., Chang C.J. Nox2 redox signaling maintains essential cell populations in the brain. Nat Chem Biol 2011, 7:106-112.
15. Doyle T., Bryant L., Batinic-Haberle I., Little J., Cuzzocrea S., Masini E., Spasojevic I., Salvemini D. Supraspinal inactivation of mitochondrial superoxide dismutase is a source of peroxynitrite in the development of morphine antinociceptive tolerance. Neuroscience 2009, 164:702-710.
16. Doyle T., Bryant L., Chen Z., Janes K., Salvemini D. Role of S1P receptor 1 in the development of chemotherapy-induced neuropathic pain: therapeutic potential of novel S1P receptor modulators in CIPN. Neuroscience Meeting Planner 2011, Society for Neuroscience, Washington, DC.
17. Doyle T., Bryant L., Muscoli C., Cuzzocrea S., Esposito E., Chen Z., Salvemini D. Spinal NADPH oxidase is a source of superoxide in the development of morphine-induced hyperalgesia and antinociceptive tolerance. Neurosci Lett 2010, 483:85-89.
18. Doyle T., Chen Z., Muscoli C., Bryant L., Esposito E., Cuzzocrea S., Dagostino C., Ryerse J., Rausaria S., Kamadulski A., Neumann W.L., Salvemini D. Targeting the overproduction of peroxynitrite for the prevention and reversal of paclitaxel-induced neuropathic pain. J Neurosci 2012, 32:6149-6160.
19. Ferrini F., Trang T., Mattioli T.A., Laffray S., Del'guidice T., Lorenzo L.E., Castonguay A., Doyon N., Zhang W., Godin A.G., Mohr D., Beggs S., Vandal K., Beaulieu J.M., Cahill C.M., Salter M.W., De Koninck Y. Morphine hyperalgesia gated through microglia-mediated disruption of neuronal Cl(-) homeostasis. Nat Neurosci 2013, 16:183-192.
20. Foley K.M. Misconceptions and controversies regarding the use of opioids in cancer pain. Anticancer Drugs 1995, 6(Suppl 3):4-13.
21. Girouard H., Wang G., Gallo E.F., Anrather J., Zhou P., Pickel V.M., Iadecola C. NMDA receptor activation increases free radical production through nitric oxide and NOX2. J Neurosci 2009, 29:2545-2552.
22. Groemping Y., Rittinger K. Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J 2005, 386:401-416.
23. Gu M., Miyoshi K., Dubner R., Guo W., Zou S., Ren K., Noguchi K., Wei F. Spinal 5-HT(3) receptor activation induces behavioral hypersensitivity via a neuronal-glial-neuronal signaling cascade. J Neurosci 2011, 31:12823-12836.
24. Guemez-Gamboa A., Estrada-Sanchez A.M., Montiel T., Paramo B., Massieu L., Moran J. Activation of NOX2 by the stimulation of ionotropic and metabotropic glutamate receptors contributes to glutamate neurotoxicity in vivo through the production of reactive oxygen species and calpain activation. J Neuropathol Exp Neurol 2011, 70:1020-1035.
25. Gustafson-Vickers S.L., Lu V.B., Lai A.Y., Todd K.G., Ballanyi K., Smith P.A. Long-term actions of interleukin-1beta on delay and tonic firing neurons in rat superficial dorsal horn and their relevance to central sensitization. Mol Pain 2008, 4:63.
26. Heumüller S., Wind S., Barbosa-Sicard E., Schmidt H.H.H.W., Busse R., Schröder K., Brandes R.P. Apocynin is not an inhibitor of vascular NADPH Oxidases but an antioxidant. Hypertension 2008, 51:211-217.
27. Horvath R.J., DeLeo J.A. Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J Neurosci 2009, 29:998-1005.
28. Horvath R.J., Romero-Sandoval E.A., De Leo J.A. Inhibition of microglial P2X4 receptors attenuates morphine tolerance, Iba1, GFAP and mu opioid receptor protein expression while enhancing perivascular microglial ED2. Pain 2010, 150:401-413.
29. Hutchinson M.R., Coats B.D., Lewis S.S., Zhang Y., Sprunger D.B., Rezvani N., Baker E.M., Jekich B.M., Wieseler J.L., Somogyi A.A., Martin D., Poole S., Judd C.M., Maier S.F., Watkins L.R. Proinflammatory cytokines oppose opioid-induced acute and chronic analgesia. Brain Behav Immun 2008, 22:1178-1189.
30. Hutchinson M.R., Zhang Y., Shridhar M., Evans J.H., Buchanan M.M., Zhao T.X., Slivka P.F., Coats B.D., Rezvani N., Wieseler J., Hughes T.S., Landgraf K.E., Chan S., Fong S., Phipps S., Falke J.J., Leinwand L.A., Maier S.F., Yin H., Rice K.C., Watkins L.R. Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Brain Behav Immun 2009, 164:1821-1832.
31. Ibi M., Matsuno K., Shiba D., Katsuyama M., Iwata K., Kakehi T., Nakagawa T., Sango K., Shirai Y., Yokoyama T., Kaneko S., Saito N., Yabe-Nishimura C. Reactive oxygen species derived from NOX1/NADPH oxidase enhance inflammatory pain. J Neurosci 2008, 28:9486-9494.
32. Jo Y.H., Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci 1999, 2:241-245.
33. Johnston I.N., Milligan E.D., Wieseler-Frank J., Frank M.G., Zapata V., Campisi J., Langer S., Martin D., Green P., Fleshner M., Leinwand L., Maier S.F., Watkins L.R. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci 2004, 24:7353-7365.
34. Kallenborn-Gerhardt W., Schroder K., Del Turco D., Lu R., Kynast K., Kosowski J., Niederberger E., Shah A.M., Brandes R.P., Geisslinger G., Schmidtko A. NADPH oxidase-4 maintains neuropathic pain after peripheral nerve injury. J Neurosci 2012, 32:10136-10145.
35. Kawasaki Y., Zhang L., Cheng J.K., Ji R.R. 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 2008, 28:5189-5194.
36. Kim D., You B., Jo E.K., Han S.K., Simon M.I., Lee S.J. NADPH oxidase 2-derived reactive oxygen species in spinal cord microglia contribute to peripheral nerve injury-induced neuropathic pain. Proc Natl Acad Sci U S A 2010, 107:14851-14856.
37. King T., Vardanyan A., Majuta L., Melemedjian O., Nagle R., Cress A.E., Vanderah T.W., Lai J., Porreca F. Morphine treatment accelerates sarcoma-induced bone pain, bone loss, and spontaneous fracture in a murine model of bone cancer. Pain 2007, 132:154-168.
38. Krysko D.V., Agostinis P., Krysko O., Garg A.D., Bachert C., Lambrecht B.N., Vandenabeele P. Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation. Trends Immunol 2011, 32:157-164.
39. Lin S.L., Tsai R.Y., Tai Y.H., Cherng C.H., Wu C.T., Yeh C.C., Wong C.S. Ultra-low dose naloxone upregulates interleukin-10 expression and suppresses neuroinflammation in morphine-tolerant rat spinal cords. Behav Brain Res 2010, 207:30-36.
40. Liu C.H., Cherng C.H., Lin S.L., Yeh C.C., Wu C.T., Tai Y.H., Wong C.S. N-Methyl-d-aspartate receptor antagonist MK-801 suppresses glial pro-inflammatory cytokine expression in morphine-tolerant rats. Pharmacol Biochem Behav 2011, 99:371-380.
41. Mao J., Mayer D.J. Spinal cord neuroplasticity following repeated opioid exposure and its relation to pathological pain. Ann N Y Acad Sci 2001, 933:175-184.
42. Mao J., Price D.D., Mayer D.J. Mechanisms of hyperalgesia and morphine tolerance: a current view of their possible interactions. Pain 1995, 62:259-274.
43. Mao J., Sung B., Ji R.R., Lim G. Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 2002, 22:8312-8323.
44. Misko T.P., Highkin M.K., Veenhuizen A.W., Manning P.T., Stern M.K., Currie M.G., Salvemini D. Characterization of the cytoprotective action of peroxynitrite decomposition catalysts. J Biol Chem 1998, 273:15646-15653.
45. Moore S.F., MacKenzie A.B. NADPH oxidase NOX2 mediates rapid cellular oxidation following ATP stimulation of endotoxin-primed macrophages. J Immunol 2009, 183:3302-3308.
46. Muscoli C., Cuzzocrea S., Ndengele M.M., Mollace V., Porreca F., Fabrizi F., Esposito E., Masini E., Matuschak G.M., Salvemini D. Therapeutic manipulation of peroxynitrite attenuates the development of opiate-induced antinociceptive tolerance in mice. J Clin Invest 2007, 117:3530-3539.
47. Muscoli C., Doyle T., Dagostino C., Bryant L., Chen Z., Watkins L.R., Ryerse J., Bieberich E., Neumman W., Salvemini D. Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J Neurosci 2010, 30:15400-15408.
48. Muzaffar S., Shukla N., Angelini G.D., Jeremy J.Y. Superoxide auto-augments superoxide formation and upregulates gp91(phox) expression in porcine pulmonary artery endothelial cells: inhibition by iloprost. Eur J Pharmacol 2006, 538:108-114.
49. Narita M., Shimamura M., Imai S., Kubota C., Yajima Y., Takagi T., Shiokawa M., Inoue T., Suzuki M., Suzuki T. Role of interleukin-1beta and tumor necrosis factor-alpha-dependent expression of cyclooxygenase-2 mRNA in thermal hyperalgesia induced by chronic inflammation in mice. Neuroscience 2008, 152:477-486.
50. Ndengele M.M., Cuzzocrea S., Masini E., Vinci M.C., Esposito E., Muscoli C., Petrusca D.N., Mollace V., Mazzon E., Li D., Petrache I., Matuschak G.M., Salvemini D. Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation. J Pharmacol Exp Ther 2009, 329:64-75.
51. O'Donnell B.V., Tew D.G., Jones O.T., England P.J. Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. Biochem J 1993, 290(Pt 1):41-49.
52. Ossipov M.H., Lai J., Vanderah T.W., Porreca F. Induction of pain facilitation by sustained opioid exposure: relationship to opioid antinociceptive tolerance. Life Sci 2003, 73:783-800.
53. Parvathenani L.K., Tertyshnikova S., Greco C.R., Roberts S.B., Robertson B., Posmantur R. P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 2003, 278:13309-13317.
54. Puntambekar P., Mukherjea D., Jajoo S., Ramkumar V. Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression. J Neurochem 2005, 95:1689-1703.
55. Qian L., Tan K.S., Wei S.J., Wu H.M., Xu Z., Wilson B., Lu R.B., Hong J.S., Flood P.M. Microglia-mediated neurotoxicity is inhibited by morphine through an opioid receptor-independent reduction of NADPH oxidase activity. J Immunol 2007, 179:1198-1209.
56. Radi R., Cassina A., Hodara R., Quijano C., Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic Biol Med 2002, 33:1451-1464.
57. Rivera J., Sobey C.G., Walduck A.K., Drummond G.R. Nox isoforms in vascular pathophysiology: insights from transgenic and knockout mouse models. Redox Rep 2010, 15:50-63.
58. Salvemini D., Little J.W., Doyle T., Neumann W.L. Roles of reactive oxygen and nitrogen species in pain. Free Radic Biol Med 2011, 51:951-966.
59. Salvemini D., Neumann W.L. Peroxynitrite: a strategic linchpin of opioid analgesic tolerance. Trends Pharmacol Sci 2009, 30:194-202.
60. Sareila O., Kelkka T., Pizzolla A., Hultqvist M., Holmdahl R. NOX2 complex-derived ROS as immune regulators. Antioxid Redox Signal 2011, 15:2197-2208.
61. Simonnet G., Rivat C. Opioid-induced hyperalgesia: abnormal or normal pain?. Neuroreport 2003, 14:1-7.
62. Sorce S., Krause K.H. NOX enzymes in the central nervous system: from signaling to disease. Antioxid Redox Signal 2009, 11:2481-2504.
63. Stuehr D.J., Fasehun O.A., Kwon N.S., Gross S.S., Gonzalez J.A., Levi R., Nathan C.F. Inhibition of macrophage and endothelial cell nitric oxide synthase by diphenyleneiodonium and its analogs. FASEB J 1991, 5:98-103.
64. Taylor D.A., Fleming W.W. Unifying perspectives of the mechanisms underlying the development of tolerance and physical dependence to opioids. J Pharmacol Exp Ther 2001, 297:11-18.
65. Trotti D., Rossi D., Gjesdal O., Levy L.M., Racagni G., Danbolt N.C., Volterra A. Peroxynitrite inhibits glutamate transporter subtypes. J Biol Chem 1996, 271:5976-5979.
66. Trujillo K.A., Akil H. Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 1991, 251:85-87.
67. Vera-Portocarrero L.P., Zhang E.T., King T., Ossipov M.H., Vanderah T.W., Lai J., Porreca F. Spinal NK-1 receptor expressing neurons mediate opioid-induced hyperalgesia and antinociceptive tolerance via activation of descending pathways. Pain 2007, 129:35-45.
68. Wang Q., Zhou H., Gao H., Chen S.H., Chu C.H., Wilson B., Hong J.S. Naloxone inhibits immune cell function by suppressing superoxide production through a direct interaction with gp91phox subunit of NADPH oxidase. J Neuroinflammation 2012, 9:32.
69. Wang X., Loram L.C., Ramos K., de Jesus A.J., Thomas J., Cheng K., Reddy A., Somogyi A.A., Hutchinson M.R., Watkins L.R., Yin H. Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci 2012, 109:6325-6330.
70. Wang Z.Q., Porreca F., Cuzzocrea S., Galen K., Lightfoot R., Masini E., Muscoli C., Mollace V., Ndengele M., Ischiropoulos H., Salvemini D. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 2004, 309:869-878.
71. Yang L., Wang S., Lim G., Sung B., Zeng Q., Mao J. Inhibition of the ubiquitin-proteasome activity prevents glutamate transporter degradation and morphine tolerance. Pain 2008, 140:472-478.
72. Zhou R., Yazdi A.S., Menu P., Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature 2011, 469:221-225.