Peripheral administration of morphine attenuates postincisional pain by regulating macrophage polarization through COX-2-dependent pathway

Molecular Pain

Volumn 10, Issue 1, 2014, Pages

  Godai, Kohei ^a   Hasegawa Moriyama, Maiko ^a   Kurimoto, Tae ^a   Saito, Takayuki ^a   Yamada, Tomotsugu ^a   Sato, Takahiro ^b   Kojima, Masayasu ^b   Kanmura, Yuichi ^a  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b KURUME UNIVERSITY   (Japan)

Author keywords

Cyclooxygenase 2; Heme oxygenase 1; M1 M2 macrophages; Morphine; Postoperative pain

Indexed keywords

BETA ENDORPHIN; CYCLOOXYGENASE 2; DYNORPHIN; HEME OXYGENASE 1; INDOMETACIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; MESSENGER RNA; MORPHINE; MU OPIATE RECEPTOR; PROENKEPHALIN; PROSTAGLANDIN E2; PROTOPORPHYRIN TIN; TUMOR NECROSIS FACTOR ALPHA;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; DEPLETION; GENE EXPRESSION; HYPERALGESIA; INFLAMMATION; MACROPHAGE; MALE; MORPHINE TOLERANCE; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; WOUND HEALING;

ANALGESICS, OPIOID; ANIMALS; CELL POLARITY; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; EDEMA; ENZYME INHIBITORS; GENE EXPRESSION REGULATION; HINDLIMB; HYPERALGESIA; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MORPHINE; PAIN; PAIN THRESHOLD; SIGNAL TRANSDUCTION; WOUNDS, STAB;

EID: 84902057647     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-10-36     Document Type: Article

References (37)

1. Voscopoulos C, Lema M. When does acute pain become chronic?. Br J Anaesth 2010, 105(Suppl 1):i69-i85.
2. Bystrom J, Evans I, Newson J, Stables M, Toor I, van Rooijen N, Crawford M, Colville-Nash P, Farrow S, Gilroy DW. Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 2008, 112:4117-4127.
3. Shaw TJ, Martin P. Wound repair at a glance. J Cell Sci 2009, 122:3209-3213.
4. Abbadie C, Lindia JA, Cumiskey AM, Peterson LB, Mudgett JS, Bayne EK, DeMartino JA, MacIntyre DE, Forrest MJ. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc Natl Acad Sci U S A 2003, 100:7947-7952.
5. Nadeau S, Filali M, Zhang J, Kerr BJ, Rivest S, Soulet D, Iwakura Y, de Rivero Vaccari JP, Keane RW, Lacroix S. Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1beta and TNF: implications for neuropathic pain. J Neurosci 2011, 31:12533-12542.
6. Hasegawa-Moriyama M, Kurimoto T, Nakama M, Godai K, Kojima M, Kuwaki T, Kanmura Y. Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone attenuates inflammatory pain through the induction of heme oxygenase-1 in macrophages. Pain 2013, 154:1402-1412.
7. Egea J, Rosa AO, Lorrio S, del Barrio L, Cuadrado A, Lopez MG. Haeme oxygenase-1 overexpression via nAChRs and the transcription factor Nrf2 has antinociceptive effects in the formalin test. Pain 2009, 146:75-83.
8. Rosa AO, Egea J, Lorrio S, Rojo AI, Cuadrado A, Lopez MG. Nrf2-mediated haeme oxygenase-1 up-regulation induced by cobalt protoporphyrin has antinociceptive effects against inflammatory pain in the formalin test in mice. Pain 2008, 137:332-339.
9. Hasegawa-Moriyama M, Ohnou T, Godai K, Kurimoto T, Nakama M, Kanmura Y. Peroxisome proliferator-activated receptor-gamma agonist rosiglitazone attenuates postincisional pain by regulating macrophage polarization. Biochem Biophys Res Commun 2012, 426:76-82.
10. Perrot S, Guilbaud G, Kayser V. Effects of intraplantar morphine on paw edema and pain-related behaviour in a rat model of repeated acute inflammation. Pain 1999, 83:249-257.
11. Endres-Becker J, Heppenstall PA, Mousa SA, Labuz D, Oksche A, Schafer M, Stein C, Zollner C. Mu-opioid receptor activation modulates transient receptor potential vanilloid 1 (TRPV1) currents in sensory neurons in a model of inflammatory pain. Mol Pharmacol 2007, 71:12-18.
12. Li Y, Tian S, Douglas SD, Ho WZ. Morphine Up-regulates expression of substance P and its receptor in human blood mononuclear phagocytes and lymphocytes. Cell Immunol 2000, 205:120-127.
13. Singhal PC, Sharma P, Kapasi AA, Reddy K, Franki N, Gibbons N. Morphine enhances macrophage apoptosis. J Immunol 1998, 160:1886-1893.
14. Hatsukari I, Hitosugi N, Dinda A, Singhal PC. Morphine modulates monocyte-macrophage conversion phase. Cell Immunol 2006, 239:41-48.
15. Rojavin M, Szabo I, Bussiere JL, Rogers TJ, Adler MW, Eisenstein TK. Morphine treatment in vitro or in vivo decreases phagocytic functions of murine macrophages. Life Sci 1993, 53:997-1006.
16. Patel K, Bhaskaran M, Dani D, Reddy K, Singhal PC. Role of heme oxygenase-1 in morphine-modulated apoptosis and migration of macrophages. J Infect Dis 2003, 187:47-54.
17. Rook JM, Hasan W, McCarson KE. Temporal effects of topical morphine application on cutaneous wound healing. Anesthesiology 2008, 109:130-136.
18. Clark JD, Shi X, Li X, Qiao Y, Liang D, Angst MS, Yeomans DC. Morphine reduces local cytokine expression and neutrophil infiltration after incision. Mol Pain 2007, 3:28.
19. Sindrilaru A, Peters T, Wieschalka S, Baican C, Baican A, Peter H, Hainzl A, Schatz S, Qi Y, Schlecht A, Weiss JM, Wlaschek M, Sunderkotter C, Scharffetter-Kochanek K. An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J Clin Invest 2011, 121:985-997.
20. Brack A, Rittner HL, Machelska H, Beschmann K, Sitte N, Schafer M, Stein C. Mobilization of opioid-containing polymorphonuclear cells by hematopoietic growth factors and influence on inflammatory pain. Anesthesiology 2004, 100:149-157.
21. Brack A, Labuz D, Schiltz A, Rittner HL, Machelska H, Schafer M, Reszka R, Stein C. Tissue monocytes/macrophages in inflammation: hyperalgesia versus opioid-mediated peripheral antinociception. Anesthesiology 2004, 101:204-211.
22. Iuvone T, Capasso A, D'Acquisto F, Carnuccio R. Opioids inhibit the induction of nitric oxide synthase in J774 macrophages. Biochem Biophys Res Commun 1995, 212:975-980.
23. Grochot-Przeczek A, Lach R, Mis J, Skrzypek K, Gozdecka M, Sroczynska P, Dubiel M, Rutkowski A, Kozakowska M, Zagorska A, Walczynski J, Was H, Kotlinowski J, Drukala J, Kurowski K, Kieda C, Herault Y, Dulak J, Jozkowicz A. Heme oxygenase-1 accelerates cutaneous wound healing in mice. PLoS One 2009, 4:e5803.
24. Hervera A, Leanez S, Motterlini R, Pol O. Treatment with carbon monoxide-releasing molecules and an HO-1 inducer enhances the effects and expression of micro-opioid receptors during neuropathic pain. Anesthesiology 2013, 118:1180-1197.
25. Ulmann L, Hirbec H, Rassendren F. P2X4 receptors mediate PGE2 release by tissue-resident macrophages and initiate inflammatory pain. EMBO J 2010, 29:2290-2300.
26. Sergeeva MG, Terentjeva IV, Mevkh AT, Varfolomeev SD. Direct influence of morphine on the release of arachidonic acid and its metabolites. FEBS Lett 1993, 323:163-165.
27. Wolf G, Livshits D, Beilin B, Yirmiya R, Shavit Y. Interleukin-1 signaling is required for induction and maintenance of postoperative incisional pain: genetic and pharmacological studies in mice. Brain Behav Immun 2008, 22:1072-1077.
28. Nakanishi Y, Nakatsuji M, Seno H, Ishizu S, Akitake-Kawano R, Kanda K, Ueo T, Komekado H, Kawada M, Minami M, Chiba T. COX-2 inhibition alters the phenotype of tumor-associated macrophages from M2 to M1 in ApcMin/+mouse polyps. Carcinogenesis 2011, 32:1333-1339.
29. Fukuoka H, Kawatani M, Hisamitsu T, Takeshige C. Cutaneous hyperalgesia induced by peripheral injection of interleukin-1 beta in the rat. Brain Res 1994, 657:133-140.
30. Honore P, Buritova J, Besson JM. Intraplantar morphine depresses spinal c-Fos expression induced by carrageenin inflammation but not by noxious heat. Br J Pharmacol 1996, 118:671-680.
31. Kolesnikov Y, Pasternak GW. Topical opioids in mice: analgesia and reversal of tolerance by a topical N-methyl-D-aspartate antagonist. J Pharmacol Exp Ther 1999, 290:247-252.
32. Zollner C, Mousa SA, Fischer O, Rittner HL, Shaqura M, Brack A, Shakibaei M, Binder W, Urban F, Stein C, Schafer M. Chronic morphine use does not induce peripheral tolerance in a rat model of inflammatory pain. J Clin Invest 2008, 118:1065-1073.
33. Loram LC, Themistocleous AC, Fick LG, Kamerman PR. The time course of inflammatory cytokine secretion in a rat model of postoperative pain does not coincide with the onset of mechanical hyperalgesia. Can J Physiol Pharmacol 2007, 85:613-620.
34. Hull MA, Faluyi OO, Ko CW, Holwell S, Scott DJ, Cuthbert RJ, Poulsom R, Goodlad R, Bonifer C, Markham AF, Coletta PL. Regulation of stromal cell cyclooxygenase-2 in the ApcMin/+mouse model of intestinal tumorigenesis. Carcinogenesis 2006, 27:382-391.
35. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
36. Pogatzki EM, Raja SN. A mouse model of incisional pain. Anesthesiology 2003, 99:1023-1027.
37. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994, 53:55-63.