Characterization of the antinociceptive and anti-inflammatory activities of doxycycline and minocycline in different experimental models

European Journal of Pharmacology

Volumn 576, Issue 1-3, 2007, Pages 171-179

  Bastos, Leandro Francisco S ^a   Merlo, Leonardo A ^a   Rocha, Leonardo Tadeu S ^a   Coelho, Márcio M ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Doxycycline; Edema; Fever; Fibrovascular tissue; Inflammation; Leukocyte migration; Minocycline; Nociception; Pain; Tetracyclines

Indexed keywords

CARRAGEENAN; DEXAMETHASONE; DOXYCYCLINE; FORMALDEHYDE; MINOCYCLINE; PHORBOL DIDECANOATE;

ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTINOCICEPTION; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DRUG MEGADOSE; FEVER; HOT PLATE TEST; LEUKOCYTE MIGRATION; MALE; MOTOR ACTIVITY; MOTOR COORDINATION; MOUSE; MUSCLE RELAXATION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PAW EDEMA; PRIORITY JOURNAL; RAT; TREATMENT DURATION; VASCULAR TISSUE;

ANALGESICS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; CARRAGEENAN; DOXYCYCLINE; EDEMA; FEVER; FORMALDEHYDE; HEAT; LIPOPOLYSACCHARIDES; MALE; MICE; MINOCYCLINE; MOTOR ACTIVITY; PAIN; PHORBOL ESTERS; RATS; RATS, WISTAR;

EID: 35348890230     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2007.07.049     Document Type: Article

References (61)

1. Alano C.C., Kauppinen T.M., Valls A.V., and Swanson R.A. Minocycline inhibits poly (ADP-ribose) polymerase-1 at nanomolar concentrations. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9685-9690
2. Amin A.R., Attur M.G., Thakker G.D., Patel P.D., Vyas P.R., Patel R.N., Patel I.R., and Abramson S.B. A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14014-14019
3. Bentle M.S., Reinicke K.E., Bey E.A., Spitz D.R., and Boothman D.A. Calcium-dependent modulation of poly (ADP-ribose) polymerase-1 alters cellular metabolism and DNA repair. J. Biol. Chem. 281 (2006) 33684-33696
4. Blum D., Chtarto A., Tenenbaum L., Brotchi J., and Levivier M. Clinical potential of minocycline for neurodegenerative disorders. Neurobiol. Dis. 17 (2004) 359-366
5. Bocker R., Estler C.J., Maywald M., and Weber D. Comparison of distribution of doxycycline in mice after oral and intravenous application measured by a high-performance liquid chromatographic method. Arzneimittelforschung 31 (1981) 2116-2117
6. Célérier P., Litoux P., and Dréno B. In vitro modulation of epidermal inflammatory cytokines (IL-1α, IL-6, TNF-α) by minocycline. Arch. Dermatol. Res. 288 (1996) 411-414
7. Charles A.C. Glia-neuron intercellular calcium signaling. Dev. Neurosci. 16 (1994) 196-206
8. Chichorro J.G., Lorenzetti B.B., and Zampronio A.R. Involvement of bradykinin, cytokines, sympathetic amines and prostaglandins in formalin-induced orofacial nociception in rats. Br. J. Pharmacol. 141 (2004) 84-117
9. Cho I., Chung Y.M., Park C., Park S., Li H.Y., Kim D., Piao Z.G., Choi S., Lee S.J., Park K., Kim J.S., Jung S.J., and Oh S.B. Systemic administration of minocycline inhibits formalin-induced inflammatory pain in rat. Brain Res. 1072 (2006) 208-214
10. Chopra I., and Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65 (2001) 232-260
11. Coelho M.M., Luheshi G., Hopkins S.J., Pela I.R., and Rothwell N.J. Multiple mechanisms mediate antipyretic action of glucocorticoids. Am. J. Physiol. 269 (1995) r527-r535
12. Cuzzocrea S., Costantino G., Zingarelli B., and Caputi A.P. Protective effects of poly (ADP-ribose) synthase inhibitors in zymosan-activated plasma induced paw edema. Life Sci. 65 (1999) 957-964
13. Cuzzocrea S., Chatterjee P.K., Mazzon E., Dugo L., Serraino I., Britti D., Mazzullo G., Caputi A.P., and Thiemermann C. Pyrrolidine dithiocarbamate attenuates the development of acute and chronic inflammation. Br. J. Pharmacol. 135 (2002) 496-510
14. D'Agostino P., Ferlazzo V., Milano S., La Rosa M., Di Bella G., Caruso R., Barbera C., Grimaudo S., Tolomeo M., Feo S., and Cillari E. Anti-inflammatory effects of chemically modified tetracyclines by the inhibition of nitric oxide and interleukin-12 synthesis in J774 cell line. Int. Immunopharmacol. 1 (2001) 1765-1776
15. Dinarello C.A., Bernheim H.A., Duff G.W., Le H.V., Nagabhushan T.L., Hamilton N.C., and Coceani F. Mechanism of fever induced by recombinant human interferon. J. Clin. Invest. 74 (1984) 906-913
16. Eady E.A., Cove J.H., Holland K.T., and Cunliffe W.J. Superior antibacterial action and reduced incidence of bacterial resistance in minocycline compared to tetracycline-treated acne patients. Br. J. Dermatol. 122 (1990) 233-244
17. Fagan S.C., Edwards D.J., Borlongan C.V., Xu L., Arora A., Feuerstein G., and Hess D.C. Optimal delivery of minocycline to the brain: implication for human studies of acute neuroprotection. Exp. Neurol. 186 (2004) 248-251
18. Ferreira J., Triches K.M., Medeiros R., and Calixto J.B. Mechanisms involved in the nociception produced by peripheral protein kinase c activation in mice. Pain 117 (2005) 171-181
19. Fröde T.S., Souza G.E., and Calixto J.B. The modulatory role played by TNF-alpha and IL-1 beta in the inflammatory responses induced by carrageenan in the mouse model of pleurisy. Cytokine 13 (2001) 162-168
20. Gabler W.L., and Creamer H.R. Suppression of human neutrophil functions by tetracyclines. J. Periodontal. Res. 26 (1991) 52-58
21. Golub L.M., Ciancio S., Ramamurthy N.S., Leung M., and McNamara T.F. Low-dose doxycycline therapy: effect on gingival and crevicular fluid collagenase activity in humans. J. Periondontal. Res. 25 (1990) 321-330
22. Gordon C.J. Thermal biology of the laboratory rat. Physiol. Behav. 47 (1990) 963-991
23. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
24. Hua X., Svensson C.I., Matsui T., Fitzsimmons B., Yaksh T.L., and Webb M. Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur. J. Neurosci. 22 (2005) 2431-2440
25. Hunskaar S., and Hole K. The formalin test in mice: dissociation between inflammatory and non-inflammatory pain. Pain 30 (1987) 113-114
26. Kamei D., Yamakawa K., Takegoshi Y., Mikami-Nakanishi M., Nakatani Y., Oh-Ishi S., Yasui H., Azuma Y., Hirasawa N., Ohuchi K., Kawaguchi H., Ishikawa Y., Ishii T., Uematsu S., Akira S., Murakami M., and Kudo I. Reduced pain hypersensitivity and inflammation in mice lacking microsomal prostaglandin E synthase-1. J. Biol. Chem. 279 (2004) 33684-33695
27. Kassuya C.A., Ferreira J., Claudino R.F., and Calixto J.B. Intraplantar PGE2 causes nociceptive behaviour and mechanical allodynia: the role of prostanoid E receptors and protein kinases. Br. J. Pharmacol. 150 (2007) 727-737
28. Kloppenburg M., Verweij C.L., Miltenburg A.M., Verhoeven A.J., Daha M.R., Dijkmans B.A., and Breedveld F.C. The influence of tetracyclines on T cell activation. Clin. Exp. Immunol. 102 (1995) 635-641
29. Krady J.K., Basu A., Allen C.M., Xu Y., LaNoue K.F., Gardner T.W., and Levison S.W. Minocycline reduces proinflammatory cytokine expression, microglial activation, and caspase-3 activation in a rodent model of diabetic retinopathy. Diabetes 54 (2005) 1559-1565
30. Le Bars D., Gozariu M., and Cadden S.W. Animal models of nociception. Pharmacol. Rev. 53 (2001) 597-652
31. 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 proinflammatory cytokine expression in rat models of pain facilitation. Pain 115 (2005) 71-83
32. LeMay L.G., Otterness I.G., Vander A.J., and Kluger M.J. In vivo evidence that the rise in plasma IL 6 following injection of a fever-inducing dose of LPS is mediated by IL 1β. Cytokine 2 (1990) 199-204
33. Long N.C., Otterness I., Kunkel S.L., Vander A.J., and Kluger M.J. Roles of interleukin 1b and tumor necrosis factor in lipopolysaccharide fever in rats. Am. J. Physiol. 259 (1990) r724-r728
34. Loram L.C., Fuller A., Fick L.G., Cartmell T., Poole S., and Mitchell D. Cytokine profiles during carrageenan-induced inflammatory hyperalgesia in rat muscle and hind paw. J. Pain 8 (2007) 127-136
35. Lukacs N.W., Chensue S.W., Smith R.E., Strieter R.M., Warmington K., Wilke C., and Kunkel S.L. Production of monocyte chemoattractant protein-1 and macrophage inflammatory protein-1 alpha by inflammatory granuloma fibroblasts. Am. J. Pathol. 144 (1994) 711-718
36. Milano S., Arcoleo F., D'Agostino P., and Cillari E. Intraperitoneal injection of tetracyclines protects mice from lethal endotoxemia downregulating inducible nitric oxide synthase in various organs and cytokine and nitrate secretion in blood. Antimicrob. Agents Chemother. 41 (1997) 117-121
37. 2+channel blockers. Eur. J. Pharmacol. 217 (1992) 137-141
38. Moore P.K., Oluyomi A.O., Babbedge R.C., Wallace P., and Hart S.L. L-NG-nitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br. J. Pharmacol. 102 (1991) 198-202
39. Moore A.R., Greenslade K.J., Alam C.A., and Willoughby D.A. Effects of diacerhein on granuloma induced cartilage breakdown in the mouse. Osteoarthr. Cartil. 6 (1998) 19-23
40. Ogino M., Majima M., Kawamura M., Hatanaka K., Saito M., Harada Y., and Katori M. Increased migration of neutrophils to granulocyte-colony stimulating factor in rat carrageenin-induced pleurisy: roles of complement, bradykinin, and inducible cyclooxygenase-2. Inflamm. Res. 45 (1996) 335-346
41. 2 production. J. Immunol. 163 (1999) 3459-3467
42. 2 by minocycline and doxycycline. Biochem. Pharmacol. 44 (1992) 1165-1170
43. Raghavendra V., Tanga F., and Deleo J. 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
44. Rocha A.C., Fernandes E.S., Quintão N.L., Campos M.M., and Calixto J.B. Relevance of tumour necrosis factor-alpha for the inflammatory and nociceptive responses evoked by carrageenan in the mouse paw. Br. J. Pharmacol. 148 (2006) 688-695
45. Salvemini D., Wang Z.Q., Wyatt P.S., Bourdon D.M., Marino M.H., Manning P.T., and Currie M.G. Nitric oxide: a key mediator in the early and late phase of carrageenan-induced rat paw inflammation. Br. J. Pharmacol. 118 (1996) 829-838
46. Sandler C., Ekokoski E., Lindstedt K.A., Vainio P.J., Finel M., Sorsa T., Kovanen P.T., Golub L.M., and Eklund K.K. Chemically modified tetracycline (CMT-3) inhibits histamine release and cytokine production in mast cells: possible involvement of protein kinase C. Inflamm. Res. 54 (2005) 304-312
47. Shapira L., Soskolne W.A., Houri Y., Barak V., Halabi A., and Stabholz A. Protection against endotoxic shock and lipopolysaccharide-induced local inflammation by tetracycline: correlation with inhibition of cytokine secretion. Infect. Immun. 64 (1996) 825-828
48. Skotnicki J.S., Zask A., Nelson F.C., Albright J.D., and Levin J.I. Design and synthetic considerations of matrix metalloproteinases inhibitors. Ann. N.Y. Acad. Sci. 30 (1999) 61-72
49. 2+/calmodulin signaling system in the neural response to excitability. Involvement of neuronal and glial cells. Prog. Neurobiol. 59 (1999) 207-232
50. Souza A.L.S., Moreira F.A., Almeida K.R., Bertollo C.M., Costa K.A., and Coelho M.M. In vivo evidence for a role of protein kinase C in peripheral nociceptive processing. Br. J. Pharmacol. 135 (2002) 239-247
51. Stone M., Fortin P.R., Pacheco-Tena C., and Inman R.D. Should tetracycline treatment be used more extensively for rheumatoid arthritis? Meta analysis demonstrates clinical benefit with reduction in disease activity. J. Rheumatol. 30 (2003) 2112-2122
52. Takano K., Al-Mokdad M., Shibata F., Tsuchiya H., and Nakagawa H. Rat macrophage inflammatory protein-1alpha, a CC chemokine, acts as a neutrophil chemoattractant in vitro and in vivo. Inflammation 23 (1999) 411-424
53. Tikka T., Fiebich B.L., Goldsteins G., Keinanen R., and Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21 (2001) 2580-2588
54. Tjølsen A., Berge O.-G., Hunskaar S., Rosland J.H., and Hole K. The formalin test: an evaluation of the method. Pain 51 (1992) 5-17
55. Watkins L.R., and Maier S.F. Glia: a novel drug discovery target for clinical pain. Nat. Rev. Drug Discov. 2 (2003) 973-985
56. Watkins L.R., Martin D., Ulrich P., Tracey K.J., and Maier S.F. Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat. Pain 71 (1997) 225-235
57. Webster G.F., Toso S.M., and Hegemann L. Inhibition of a model of in vitro granuloma formation by tetracyclines and ciprofloxacin: Involvement of protein kinase C. Arch. Dermatol. 130 (1994) 748-752
58. Yrjänheikki J., Keinänen R., Pellikka M., Hökfelt T., and Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 15769-15774
59. Yrjänheikki J., Tikka T., Keinänen R., Goldsteins G., Chan P.H., and Koistinaho J. A tetracycline derivate, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 13496-13500
60. Zanjani T.M., Sabetkasaei M., Mosaffa N., Manaheji H., Labibi F., and Farokhi B. Supression of interleukin-6 by minocycline in a rat model of neuropathic pain. Eur. J. Pharmacol. 538 (2006) 66-72
61. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 (1983) 109-110