Minocycline prevents the development of neuropathic pain, but not acute pain: Possible anti-inflammatory and antioxidant mechanisms

European Journal of Pharmacology

Volumn 601, Issue 1-3, 2008, Pages 79-87

  Padi, Satyanarayana S V ^a,b   Kulkarni, Shrinivas K ^a  

^a PANJAB UNIVERSITY   (India)

^b ISF COLLEGE OF PHARMACY   (India)

Author keywords

Allodynia; Glia; Hyperalgesia; Hypersensitivity; Microglia; Minocycline; Nerve injury; Neuropathic pain

Indexed keywords

ACETIC ACID; ANTIOXIDANT; CYTOKINE; MINOCYCLINE; ZYMOSAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ASTROCYTE; BLOOD VESSEL PERMEABILITY; CELL INFILTRATION; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFECT; DRUG HYPERSENSITIVITY; GLIA CELL; IMMERSION; INFLAMMATORY CELL; MALE; MEDIATOR RELEASE; MICROGLIA; MOUSE; NERVE INJURY; NEUROPATHIC PAIN; NITROSATIVE STRESS; NOCICEPTION; NONHUMAN; OXIDATIVE STRESS; PERITONITIS; PRIORITY JOURNAL; SENSITIZATION; SINGLE DRUG DOSE; TAIL IMMERSION TEST;

ACUTE DISEASE; ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; DRUG ADMINISTRATION SCHEDULE; INFLAMMATION MEDIATORS; INJECTIONS, INTRAPERITONEAL; MALE; MICE; MICROGLIA; MINOCYCLINE; OXIDATIVE STRESS; PAIN; PAIN MEASUREMENT; PERITONITIS; RATS; RATS, WISTAR; SCIATIC NEUROPATHY;

EID: 56949085589     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2008.10.018     Document Type: Article

References (56)

1. Aronson A.L. Pharmacotherapeutics of the newer tetracyclines. J. Am. Vet. Med. Assoc. 176 (1980) 1061-1068
2. Bastos L.F., Merlo L.A., Rocha L.T., and Coelho M.M. Characterization of the antinociceptive and anti-inflammatory activities of doxycycline and minocycline in different experimental models. Eur. J. Pharmacol. 576 (2007) 171-179
3. Bennett G.J., and Xie Y.-K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 (1988) 87-107
4. Chen M., Ona V.O., Li M., Ferrante R.J., Fink K.B., Zhu S., Bian J., Guo L., Farrell L.A., Hersch S.M., Hobbs W., Vonsattel J.P., Cha J.H., and Friedlander R.M. Minocycline inhibits caspase-1 and caspase-3 expression and delays in a transgenic mouse model of Huntington disease. Nat. Med. 6 (2000) 797-801
5. Clark A.K., Yip P.K., Grist J., Gentry C., Staniland A.A., Marchand F., Dehvari M., Wotherspoon G., Winter J., Ullah J., Bevan S., and Malcangio M. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc. Natl. Acad. Sci. 104 (2007) 10655-10660
6. Colburn R.W., Deleo J.A., Rikman A.J., Yeager M.P., Kwon P., and Hickey W.F. Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat. J. Neuroimmunol. 79 (1997) 163-175
7. Coyle D.E. Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior. Glia 23 (1998) 75-83
8. Cunha F.Q., Poole S., Lorenzetti B.B., and Ferreira S.H. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br. J. Pharmacol. 107 (1992) 660-664
9. DeLeo J.A., and Yezierski R.P. The role of neuroinflammation and neuroimmune activation in the persistent pain. Pain 90 (2001) 1-6
10. Doherty N.S., Griffiths R.J., Hakkinen J.P., Scampoli D.N., and Milici A.J. Post-capillary venules in the "milky spots" of the greater omentum are the major site of plasma protein and leukocyte extravasation in rodent models of peritonitis. Inflamm, Res. 44 (1995) 169-177
11. Guedes R.P., Bosco L.D., Teixeira C.M., Araújo A.S., Llesuy S., Belló-Klein A., Ribeiro M.F., and Partata W.A. Neuropathic pain modifies antioxidant activity in rat spinal cord. Neurochem. Res. 31 (2006) 603-609
12. 2 cannabinoid receptor mediation of antinociception. Pain 122 (2006) 36-42
13. Jin S.X., Zhuang Z.Y., Woolf C.J., and Ji R.R. 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. Neurosci. 23 (2003) 4017-4022
14. Kim H.K., Park S.K., Zhou J.L., Taglialatela G., Chung K., Coggeshall R.E., and Chung J.M. Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111 (2004) 116-124
15. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19 (1996) 312-318
16. 411 attenuates mechanical allodynia in rat models of neuropathic pain. Neuron Glia Biol. 1 (2007) 1-13
17. Ledeboer A., Sloane E.M., Milligan E.D., Frank M.G., Mahony J.H., Maier S.F., and Watkins L.R. Minocycline attenuates mechanical allodynia and pro-inflammatory cytokines expression in rat models of pain facilitation. Pain 15 (2005) 71-83
18. Liu H., and Hong J.-S. Role of microglial in inflammation-mediated neurodegenerative diseases: mechanism and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther., 304 (2003) 1-7
19. Lou M.F., Dickerson Jr. J.E., Garadi R., and York B.M. Glutathione depletion in the lens of galactosemic and diabetic rats. Exp. Eye. Res. 46 (1988) 517-530
20. Ma W., and Eisenach J.C. Cyclooxygenase 2 in infiltrating inflammatory cells in injured nerve is universally up-regulated following various types of peripheral nerve injury. Neuroscience 121 (2003) 691-704
21. 2 from invading macrophages following nerve injury: an in vivo and in vitro study. J Neurochem. 93 (2005) 664-673
22. Mika J., Osikowicz M., Mkuch W., and Przewlocka B. Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur. J. Pharmacol. 560 (2007) 142-149
23. Moalem G., and Tracey D.J. Immune and inflammatory mechanisms in neuropathic pain. Brain Res. Rev. 51 (2006) 240-264
24. Naik A.K., Tandan S.K., Dudhgaonkar S.P., Jadhav S.H., Kataria M., Prakash V.R., and Kumar D. Role of oxidative stress in pathophysiology of peripheral neuropathy and modulation by N-acetyl-l-cysteine in rats. Eur. J. Pain 10 (2006) 573-579
25. Naik A.K., Tandan S.K., Kumar D., and Dudhgaonkar S.P. Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats. Eur. J. Pharmacol. 530 (2006) 59-69
26. Nakagawa T., Wakamatsu K., Zhang N., Maeda S., Minami M., Satoh M., and Kaneko S. Intrathecal administration of ATP produces long-lasting allodynia in rats: differential mechanisms in the phase of the induction and maintenance. Neuroscience 147 (2007) 445-455
27. Narita M., Yoshida T., Nakajima M., Narita M., Miyatake M., Takagi T., Yajima Y., and Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J. Neurochem. 97 (2006) 1337-1348
28. Nathan C. Points of control in inflammation. Nature 420 (2002) 846-852
29. Niehaus Jr. W.G., and Samuelson D. Formation of malondialdehyde from phospholipids arachidonate during microsomal lipid peroxidation. Eur. J. Biochem. 6 (1968) 126-130
30. Owolabi S.A., and Saab C.Y. Fractalkine and minocycline alter neuronal activity in the spinal cord dorsal horn. FEBS Lett. 580 (2006) 4306-4310
31. Padi S.S.V., Jain N.K., Singh A., and Kulkarni S.K. Isobolographic analysis of interaction between cyclooxygenase inhibitors and tramadol in acetic acid-induced writhing in mice. Prog. Neuropsychopharmacol. Biol. Psychiat. 28 (2004) 641-649
32. Padi S.S.V., Jain N.K., Singh S., and Kulkarni S.K. Effect of selective inhibition of cyclooxygense-2 on lipopolysaccharide-induced hyperalgesia. Inflammopharmacology 12 (2004) 57-68
33. Padi S.S.V., and Kulkarni S.K. Differential effects of cyclooxygenase inhibitors on the development of hypersensitivity in rats with nerve injury. Pharmacol. Biochem. Behav. 79 (2004) 349-358
34. Padi S.S.V., and Kulkarni S.K. Minocycline prevents hypersensitivity to formalin and nerve injury in rats. Program No. 293.1. 2005 Abstract Viewer/Itinerary Planner (2005), Society for Neuroscience, Washington, DC
35. Park E.S., Gao X., Chung J.M., and Chung K. Levels of mitochondrial reactive oxygen species increase in rat neuropathic spinal dorsal horn neurons. Neurosci. Lett. 391 (2006) 108-111
36. Purisai M.G., McCormacka A.L., Cuminea S., Lia J., Islaa M.Z., and Di Monte D.A. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol. Dis. 25 (2007) 392-400
37. Raghavendra V., Tanga F., and DeLeo J.A. Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J, Pharmacol. Exp. Ther. 306 (2003) 624-630
38. Reeta K.H., Mediratta P.K., Mahajan P., and Sharma K.K. Effect of minocycline and tetracycline on immunological responses in experimental animals. Ind. J. Med. Sci. 56 (2002) 553-559
39. Ribeiro R.A., Vale M.L., Thomazzi S.M., Paschoalato A.B., Poole S., Ferreira S.H., and Cunha F.Q. Involvement of resident macrophages and mast cells in the writhing nociceptive response induced by zymosan and acetic acid in mice. Eur. J. Pharmacol. 387 (2000) 111-118
40. Sastry K.V., Moudgal R.P., Mohan J., Tyagi J.S., and Rao G.S. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal. Biochem. 306 (2001) 79-82
41. Sewell K.L., Breedveld F., Furrie E., O'Brien J., Brinckerhoff C., Dynesius-Trentham R., Nosaka Y., and Trentham D.E. The effect of minocycline in rat models of inflammatory arthritis: correlation of arthritis suppression with enhanced T cell calcium flux. Cell Immunol. 167 (1996) 195-204
42. Shan S., Qi-Liang M.-Y., Hong C., Tingting L., Mei H., Haili P., Yan-Qingb W., Zhi-Qia Z., and Yu-Qiu Z. Is functional state of spinal microglia involved in the anti-allodynic and anti-hyperalgesic effects of electropuncture in rat model of monoarthritis?. Neurobiol. Dis. 26 (2007) 558-568
43. Sherwood E.R., and Toliver-Kinsky T. Mechanisms of the inflammatory response. Best Pract. Res. Clin. Anaesthesiol. 18 (2004) 385-405
44. Tikka T.M., Fiebich B.L., Goldsteins G., Keinanen R., and Koistinaho J.E. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation of microglia. J. Neurosci. 21 (2001) 2580-2588
45. Tikka T.M., and Koistinaho J.E. Minocycline provides neuroprotection against N-methyl-D-aspartate neurotoxicity by inhibiting microglia. J. Immunol. 166 (2001) 7527-7533
46. Tsuda M., Mizokoshi A., Shigemoto-Mogami Y., Koizumi S., and Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45 (2004) 89-95
47. Twining C.M., Sloane E.M., Milligan E.D., Chacur M., Martin D., Poole S., Marsh H., Maier S.F., and Watkins L.R. Peri-sciatic pro-inflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats. Pain 110 (2004) 299-309
48. Vale M.L., Marques J.B., Moreira C.A., Rocha F.A.C., Ferreia S.H., Poole S., Cunha F.Q., and Ribeiro R.A. Antinociceptive effects of interleukin-4, -10, and -13 on the writhing response in mice and zymosan-induced knee joint incapacitation in rats. J. Pharmacol. Exp. Ther. 304 (2003) 102-108
49. Vega-Avelaira D., Moss A., and Fitzgerald M. Age-related changes in the spinal cord microglial and astrocytic response profile to nerve injury. Brain Behav. Immun. 21 (2007) 617-623
50. Watkins L.R., Milligan E.D., and Maier S.F. Glial activation: a driving force for pathological pain. Trends Neurosci. 24 (2001) 450-455
51. Winkelstein B.A., and Deleo J.A. Nerve root injury severity differentially modulates spinal glial activation in a rat lumbar radiculopathy model: consideration for persistent pain. Brain Res. 956 (2002) 294-301
52. Wu D.C., Jackson-Lewis V., Vila M., Teiu K., Teismann K., Vadseth C., Choi D.K., Ischiropoulos H., and Przedborski S. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22 (2002) 1763-1771
53. Yenari M.A., Xu L., Tang X.N., Qiao Y., and Giffard R.G. Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 37 (2006) 1087-1093
54. Zhong J., and Lee W.H. Hydrogen peroxide attenuates insulin-like growth factor-1 neuroprotective effect, prevented by minocycline. Neurochem. Int. 51 (2007) 398-404
55. Zhuang Z.-Y., Gerner P., Woolf C.J., and Ji R.-R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to the mechanical allodynia in this neuropathic pain model. Pain 114 (2005) 149-159
56. Zhuang Z.-Y., Wen Y.-R., Zhang D.R., Borsello T., Bonny C., Strichartz G.R., Decosterd I., and Ji R.-R. A peptide c-jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance. J. Neurosci. 26 (2006) 3551-3560