Amitriptyline suppresses neuroinflammation-dependent interleukin-10-p38 mitogen-activated protein kinase-heme oxygenase-1 signaling pathway in chronic morphine-infused rats

Anesthesiology

Volumn 110, Issue 6, 2009, Pages 1379-1389

  Tai, Yueh Hua ^a   Tsai, Ru Yin ^b   Lin, Shinn Long ^b   Yeh, Chun Chang ^a   Wang, Jhi Joung ^c   Tao, Pao Luh ^b   Wong, Chih Shung ^a  

^a TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c CHI MEI MEDICAL CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMITRIPTYLINE; ANTIBODY; HEME OXYGENASE 1; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE P38; MORPHINE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; BLOCKING ANTIBODY; ENZYME INHIBITOR; IMIDAZOLE DERIVATIVE; NARCOTIC ANALGESIC AGENT; NONSTEROID ANTIINFLAMMATORY AGENT; PROTOPORPHYRIN; PROTOPORPHYRIN ZINC; PYRIDINE DERIVATIVE; TRICYCLIC ANTIDEPRESSANT AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG TOLERANCE; MALE; MICROGLIA; MORPHINE TOLERANCE; MYELITIS; NONHUMAN; PAIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; DRUG ANTAGONISM; ENZYMOLOGY; PAIN ASSESSMENT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD; WISTAR RAT;

AMITRIPTYLINE; ANALGESICS, OPIOID; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIBODIES, BLOCKING; ANTIDEPRESSIVE AGENTS, TRICYCLIC; DRUG TOLERANCE; ENZYME INHIBITORS; HEME OXYGENASE-1; IMIDAZOLES; INTERLEUKIN-10; MALE; MORPHINE; MYELITIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PAIN MEASUREMENT; PROTOPORPHYRINS; PYRIDINES; RATS; RATS, WISTAR; SIGNAL TRANSDUCTION; SPINAL CORD;

EID: 67049157932     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e31819fccd5     Document Type: Article

References (56)

1. Ossipov MH, Lai J, King T, Vanderah TW, Malan TP Jr, Hruby VJ, Porreca F: Antinociceptive and nociceptive actions of opioids. J Neurobiol 2004; 61:126-48
2. Gintzler AR, Chakrabarti S: Opioid tolerance and the emergence of new opioid receptor-coupled signaling. Mol Neurobiol 2000; 21:21-33
3. Hsu MM, Wong CS: The roles of pain facilitatory systems in opioid tolerance. Acta Anaesthesiol Sin 2000; 38:155-66
4. Raghavendra V, Rutkowski MD, DeLeo JA: The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neurosci 2002; 22:9980-9
5. Tai YH, Wang YH, Tsai RY, Wang JJ, Tao PL, Liu TM, Wang YC, Wong CS: Amitriptyline preserves morphine's antinociceptive effect by regulating the glu- tamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats. Pain 2007; 129:343-54
6. Tai YH, Wang YH, Wang JJ, Tao PL, Tung CS, Wong CS: Amitriptyline suppresses neuroinflammation and up-regulates glutamate transporters in morphine-tolerant rats. Pain 2006; 124:77-86
7. Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, CampisiJ, Langer S, Martin D, Green P, Fleshner M, Leinwand L, Maier SF, Watkins LR: A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci2004; 24:7353-65
8. Song P, Zhao ZQ: The involvement of glial cells in the development of morphine tolerance. Neurosci Res 2001; 39:281-6
9. Onghena P, Van Houdenhove B: Antidepressant-induced analgesia in chronic non-malignant pain: A meta-analysis of 39 placebo-controlled studies. Pain 1992; 49:205-19
10. Sawynok J, Esser MJ, Reid AR: Antidepressants as analgesics: An overview of central and peripheral mechanisms of action. J Psychiatry Neurosci 2001; 26:21-9
11. Esser MJ, Sawynok J: Acute amitriptyline in a rat model of neuropathic pain: Differential symptom and route effects. Pain 1999; 80:643-53
12. Eisenach JC, Gebhart GF: Intrathecal amitriptyline. Antinociceptive interactions with intravenous morphine and intrathecal clonidine, neostigmine, and carbamylcholine in rats. AAANESTHESIOLOGY 1995; 83:1036-45
13. Gray AM, Spencer PS, Sewell RD: The involvement of the opioidergic system in the antinociceptive mechanism of action of antidepressant compounds. Br J Pharmacol 1998; 124:669-74
14. Tsai RY, Jang FL, Tai YH, Lin SL, Shen CH, Wong CS: Ultra-low-dose naloxone restores the antinociceptive effect of morphine and suppresses spinal neuroinflammation in PTX-treated rats. Neuropsychopharmacology 2008; 33:2772-82
15. Howard M, O'Garra A: Biological properties of interleukin 10. Immunol Today 1992; 13:198-200
16. Maes M, Song C, Lin AH, Bonaccorso S, Kenis G, De Jongh R, Bosmans E, Scharpe S: Negative immunoregulatory effects of antidepressants: Inhibition of interferon-gamma and stimulation ofinterleukin-10 secretion. Neuropsychophar- macology 1999; 20:370-9
17. Kanaan SA, Poole S, Saade NE, Jabbur S, Safieh-Garabedian B: Interleu- kin-10 reduces the endotoxin-induced hyperalgesia in mice. J Neuroimmunol 1998; 86:142-50.
18. Wagner R, Janjigian M, Myers RR: Anti-inflammatory interleukin-10 therapy in CCI neuropathy decreases thermal hyperalgesia, macrophage recruitment, and endoneurial TNF-alpha expression. Pain 1998; 74:35-42
19. Lee TS, Chau LY: Heme oxygenase-1 mediates the anti-inflammatory effect of interleukin-10 in mice. Nat Med 2002; 8:240-6
20. Xia Z, DePierre JW, Nassberger L: Tricyclic antidepressants inhibit IL-6, IL-1 beta and TNF-alpha release in human blood monocytes and IL-2 and inter- feron-gamma in T cells. Immunopharmacology 1996; 34:27-37
21. Yaron I, Shirazi I, Judovich R, Levartovsky D, Caspi D, Yaron M: Fluoxetine and amitriptyline inhibit nitric oxide, prostaglandin E2, and hyaluronic acid production in human synovial cells and synovial tissue cultures. Arthritis Rheum1999; 42:2561-8
22. Heughan CE, Allen GV, Chase TD, Sawynok J: Peripheral amitriptyline suppresses formalin-induced Fos expression in the rat spinal cord. Anesth Analg 2002; 94:427-31
23. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A: IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991; 147:3815-22
24. Poole S, Cunha FQ, Selkirk S, Lorenzetti BB, Ferreira SH: Cytokine-medi- ated inflammatory hyperalgesia limited by interleukin-10. Br J Pharmacol 1995; 115:684-8
25. Messmer D, Hatsukari I, Hitosugi N, Schmidt-Wolf IG, Singhal PC: Morphine reciprocally regulates IL-10 and IL-12 production by monocyte-derived human dendritic cells and enhances T cell activation. Mol Med 2006; 12:284-90
26. Nelson CJ, Lysle DT: Morphine modulation of the contact hypersensitivity response: Characterization of immunological changes. Clin Immunol 2001; 98:370-7
27. Otterbein L, Sylvester SL, Choi AM: Hemoglobin provides protection against lethal endotoxemia in rats: The role of heme oxygenase-1. Am J Respir Cell Mol Biol 1995; 13:595-601
28. Willis D, Moore AR, Frederick R, Willoughby DA: Heme oxygenase: A novel target for the modulation of the inflammatory response. Nat Med 1996;2:87-90
29. Nascimento CG, Branco LG: Role of the peripheral heme oxygenase- carbon monoxide pathway on the nociceptive response of rats to the formalin test: Evidence for a cGMP signaling pathway. Eur J Pharmacol 2007; 556:55-61
30. Nascimento CG, Branco LG: Role of the spinal cord heme oxygenase- carbon monoxide-cGMP pathway in the nociceptive response of rats. Eur J Pharmacol 2008; 581:71-6
31. 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; 137:332-9
32. Otterbein LE, Mantell LL, Choi AM: Carbon monoxide provides protection against hyperoxic lung injury. Am J Physiol 1999; 276:L688-94
33. Sato K, BallaJ, Otterbein L, Smith RN, Brouard S, Lin Y, Csizmadia E, Sevigny J, Robson SC, Vercellotti G, Choi AM, Bach FH, Soares MP: Carbon monoxide generated by heme oxygenase-1 suppresses the rejection of mouse- to-rat cardiac transplants. J Immunol 2001; 166:4185-94
34. Lin Q, Weis S, Yang G, Weng YH, Helston R, Rish K, Smith A, Bordner J, Polte T, Gaunitz F, Dennery PA: Heme oxygenase-1 protein localizes to the nucleus and activates transcription factors important in oxidative stress. J BiolChem 2007; 282:20621-33
35. O'Farrell AM, Liu Y, Moore KW, Mui AL: IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: Evidence for Stat3- dependent and-independent pathways. EmboJ 1998; 17:1006-18
36. Crawley JB, Williams LM, Mander T, Brennan FM, Foxwell BM: Interleu- kin-10 stimulation of phosphatidylinositol 3-kinase and p70 S6 kinase is required for the proliferative but not the antiinflammatory effects of the cytokine. J BiolChem 1996; 271:16357-62
37. Naito Y, Takagi T, Yoshikawa T: Heme oxygenase-1: A new therapeutic target for inflammatory bowel disease. Aliment Pharmacol Ther 2004; 20(Suppl 1):177-84
38. Alam J, Wicks C, Stewart D, Gong P, Touchard C, Otterbein S, Choi AM,Burow ME, Tou J: Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcriptionfactor. J Biol Chem 2000; 275:27694-702
39. Zhang X, Bedard EL, Potter R, Zhong R, Alam J, Choi AM, Lee PJ: Mitogen- activated protein kinases regulate HO-1 gene transcription after ischemia-reper- fusion lung injury. Am J Physiol Lung Cell Mol Physiol 2002; 283:L815-29
40. Da Silva J, Pierrat B, Mary JL, Lesslauer W: Blockade of p38 mitogen- activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes. J Biol Chem 1997; 272:28373-80
41. Svensson CI, Hua XY, Protter AA, Powell HC, Yaksh TL: Spinal p38 MAPkinase is necessary for NMDA-induced spinal PGE(2) release and thermal hyper- algesia. Neuroreport 2003; 14:1153-7
42. Svensson CI, Marsala M, Westerlund A, Calcutt NA, Campana WM, Freshwater JD, Catalano R, Feng Y, Protter AA, Scott B, Yaksh TL: Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing. J Neurochem 2003; 86:1534-44
43. Milligan ED, Twining C, Chacur M, Biedenkapp J, O'Connor K, Poole S, Tracey K, Martin D, Maier SF, Watkins LR: Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J Neurosci 2003; 23:1026-40
44. Jin SX, Zhuang ZY, Woolf CJ, Ji RR: p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neu- rosci 2003; 23:4017-22
45. Kim SY, Bae JC, Kim JY, Lee HL, Lee KM, Kim DS, Cho HJ: Activation of p38 MAP kinase in the ratdorsal root gangliaand spinal cord following peripheral inflammation and nerve injury. Neuroreport 2002; 13:2483-6
46. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K: Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004; 45:89-95
47. Cui Y, Chen Y, Zhi JL, Guo RX, Feng JQ, Chen PX: Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antino- ciceptive tolerance. Brain Res 2006; 1069:235-43
48. Ono K, Han J: The p38 signal transduction pathway: Activation and function. Cell Signal 2000; 12:1-13
49. Zhang C, Baumgartner RA, Yamada K, Beaven MA: Mitogen-activated protein (MAP) kinase regulates production of tumor necrosis factor-alpha and release of arachidonic acid in mast cells. Indications of communication between p38 and p42 MAP kinases. J Biol Chem 1997; 272:13397-402
50. van den Blink B, Juffermans NP, ten Hove T, Schultz MJ, van Deventer SJ, van der Poll T, Peppelenbosch MP: p38 mitogen-activated protein kinase inhibition increases cytokine release by macrophages IN vitro and during infection IN vivo. J Immunol 2001; 166:582-7
51. Fields RD, Stevens-Graham B: New insights into neuron-glia communication. Science 2002; 298:556-62
52. Verge GM, Milligan ED, Maier SF, Watkins LR, Naeve GS, Foster AC: Fractalkine (CX3CL1) and fractalkine receptor (CX3CR1) distribution in spinal cord and dorsal root ganglia under basal and neuropathic pain conditions. Eur J Neurosci 2004; 20:1150-60
53. Narita M, Suzuki M, Narita M, Yajima Y, Suzuki R, Shioda S, Suzuki T: Neuronal protein kinase C gamma-dependent proliferation and hypertrophy of spinal cord astrocytes following repeated IN vivo administration of morphine. Eur J Neurosci 2004; 19:479-84
54. DeLeo JA, Tanga FY, Tawfik VL: Neuroimmune activation and neuroin- flammation in chronic pain and opioid tolerance/hyperalgesia. Neuroscientist 2004; 10:40-52
55. Campbell JN, Meyer RA: Mechanisms of neuropathic pain. Neuron 2006; 52:77-92
56. Rintala DH, Holmes SA, Courtade D, Fiess RN, Tastard LV, Loubser PG: Comparison of the effectiveness of amitriptyline and gabapentin on chronic neuropathic pain in persons with spinal cord injury. Arch Phys Med Rehabil2007; 88:1547-60