Anti-inflammatory properties of Doxycycline and Minocycline in experimental models: An in vivo and in vitro comparative study

Inflammopharmacology

Volumn 19, Issue 2, 2011, Pages 99-110

  Leite, Liz M ^a   Carvalho, Antônio Germano G ^a   Tavares Ferreira, Pollyanna L F ^a   Pessoa, Igor Xavier ^a   Gonçalves, Danilo O ^b   De Araújo Lopes, Amanda ^b   Dos Santos Góes, Jean Guilherme ^b   De Castro Alves, Victor Costa ^b   Leal, Luzia Kalyne A M ^b   Brito, Gerly Anne ^a,b   Viana, Glauce S B ^a,b  

^a Faculty of Medicine of Juazeiro de Norte   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

Author keywords

Antioxidant effect; Cytokines; Doxycycline; Inflammation; Minocycline

Indexed keywords

DEXAMETHASONE; DOXYCYCLINE; INDOMETACIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LACTATE DEHYDROGENASE; MINOCYCLINE; MORPHINE; MYELOPEROXIDASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG EFFICACY; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LEUKOCYTE MIGRATION; MALE; MIGRATION INHIBITION; MOUSE; NONHUMAN; PAIN; PAW EDEMA; PERITONEAL CAVITY; PERITONITIS; PRIORITY JOURNAL; RAT;

ALPHA-TOCOPHEROL; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTIOXIDANTS; BIPHENYL COMPOUNDS; CARRAGEENAN; CELL MOVEMENT; DOXYCYCLINE; EDEMA; FORMALDEHYDE; INFLAMMATION; L-LACTATE DEHYDROGENASE; MALE; MICE; MICE, INBRED STRAINS; MINOCYCLINE; NEUTROPHILS; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; PAIN; PAIN MEASUREMENT; PERITONITIS; PEROXIDASE; PICRATES; RATS; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79958205912     PISSN: 09254692     EISSN: 15685608     Source Type: Journal    
DOI: 10.1007/s10787-011-0077-5     Document Type: Article

References (52)

1. Aladakatti SV, Patil PA, Vivek V (2008) Influence of tetracyclines on inflammation and their interaction with aspirin in male Wistar rats. Pharmacology online 3:808-819
2. Alano CC, Kauppinen TM, Valls AV, Swanson RA (2006) Minocycline inhibits poly (ADP-ribose) polymerase-1 at nanomolar concentrations. Proc Natl Acad Sci USA 103:9685-9690 (Pubitemid 43955885)
3. Amin AR, Attur MG, Thakker GD, Patel PD, Vyas PR, Patel RN, Patel IR, Abramson SB (1996) A novel mechanism of action of tetracyclines: effects on nitric oxide synthases. Proc Natl Acad Sci USA 93:14014-14019 (Pubitemid 26424237)
4. Arvin KL, Han BH, Du Y, Lin SZ, Paul SM, Holtzman DM (2002) Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 52:54-61 (Pubitemid 34693743)
5. Attur MG, Patel RN, Patel PD, Abramson SB, Amin AR (1999) Tetracycline up-regulates COX-2 expression and prostaglandin E2 production independent of its effect on nitric oxide. J Immunol 162:3160-3167 (Pubitemid 29313561)
6. Bastos LF, Merlo LA, Rocha LT, Coelho MM (2007) Characterization of the antinociceptive and anti-inflammatory activities of doxycycline and minocycline in different experimental models. Eur J Pharmacol 576:171-179 (Pubitemid 47588248)
7. Bombardier S, Cattani P, Giabattoni G, Di Munno O, Paero G, Patrono C, Pinca E, Pugliese F (1981) The synovial prostaglandin system in chronic inflammatory arthritis: differential effects of steroidal and non-steroidal antiinfammatory drugs. Br J Pharmacol 73:893-901 (Pubitemid 11033775)
8. Cai ZY, Yan Y, Sun SQ, Zhang J, Huang LG, Yan NN, Wu F, Li JY (2008) Minocycline attenuates cognitive impairment and restrains oxidative stress in the hippocampus of rats with chronic cerebral hypoperfusion. Neurosci Bull 24:305-313
9. Cazalis J, Tanabe S, Gagnon G, Sorsa T, Grenier D (2009) Tetracyclines and chemically modified tetracycline-3 (CMT-3) modulate cytokine secretion by lipopolysaccharide-stimulated whole blood. Inflammation 32:130-137
10. Chen M, Ona VO, Li M, Ferrante RJ, Fink KB, Zhu S, Biau J, Gno L, Farrell LA, Hersch SM, Hobbs W, Vonsattel JP, Cha JH, Friedlander RM (2000) Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington disease. Nat Med 6:797-801 (Pubitemid 30469429)
11. Cho IH, Chung YM, Park CK, Li HY, Kim D, Plao ZH, Choi SY, Lee SJ, Park K, Kim JS, Jung SJ, Oh SB (2006) Systemic administration of minocycline inhibits formalin-induced inflammatory pain in rat. Brain Res 1072:208-214 (Pubitemid 43255466)
12. Daher JB, Tonussi CR (2003) A spinal mechanism for the peripheral anti-inflammatory action of indomethacin. Brain Res 962:207-212 (Pubitemid 36126337)
13. Davies P, MacIntyre DE (1992) Prostaglandins and inflammation. In: Gallin JI, Goldstein IM, Snyderman R (eds) Inflammation: basic principles and clinical correlates. Raven Press, New York, pp 123-138
14. Davies P, Bailey PJ, Goldenberg MM, Ford-Hutchinson AW (1984) The role of arachidonic acid oxygenation products in pain and inflammation. Ann Rev Immunol 2:235-257
15. De Young LM, Kheifets JB, Ballaron SJ, Young JM (1989) Edema and cell infiltration in the phorbol ester-treated mouse ear are temporally separate and can be differentially modulated by pharmacologic agents. Agents Actions 26:335-341 (Pubitemid 19078128)
16. DeClerk YA, Shimada H, Taylor SM, Langley KE (1994) Matrix metalloproteinases and their inhibitors in tumor progression. Ann NY Acad Sci 732:222-232
17. El Kebir D, József L, Pan W, Filep JG (2008) Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation. Circ Res 103:352-359
18. Faith M, Sukumaran A, Pulimood AB, Jacob M (2008) How reliable an indicator of inflammation is myeloperoxidase activity? Clin Chim Acta 396:23-25
19. Foster SJ, McCormick ME, Howarth A, Aked D (1986) Leukocyte recruitment in the subcutaneous sponge implant model of acute inflammation in the rat is not mediated by leukotriene B1. Biochem Pharmacol 35:1709-1717 (Pubitemid 16067791)
20. Fu KY, Light AR, Maixner W (2000) Relationship between nociceptor activity, peripheral edema, spinal microglial activation and long-term hyperalgesia induced by formalin. Neuroscience 101:1127-1135
21. Gilbertson-Beadling S, Powers EA, Stamp-Cole M, Scott PS, Wallace TL, Copeland J, Petzold G, Mitchell M, Ledbetter S, Poorman R (1995) The tetracycline analogs minocycline and doxycycline inhibit angiogenesis in vitro by a non-metalloproteinase-dependent mechanism. Cancer Chemother Pharmacol 36:418-424
22. Giuliani F, Hader W, Yong VW (2005) Minocycline attenuates T cell and microglia activity to impair cytokine production in T cellmicroglia interaction. J Leukoc Biol 78:135-143 (Pubitemid 40979952)
23. Greenwald RA (1994) Treatment of destructive arthritic disorders with MMP inhibitors. Potential role of tetracyclines. Ann N Y Acad Sci 732:181-198
24. Guay J, Bateman K, Gordon R, Mancini J, Riendeau D (2004) Carrageenan-induced paw edema in rat elicits a predominant prostaglandin E2 (PGE2) response in the central nervous system associated with the induction of microsomal PGE2 synthase-1. J Biol Chem 279:24866-24872 (Pubitemid 38725355)
25. Henry CJ, Huang Y, Wynne A, Hanke M, Himler J, Bailey MT, Sheridan JF, Godbout JP (2008) Minocycline attenuates lipopolysaccharide (LPS)-induced neuroinflammation, sickness behavior and anhedonia. J Neuroinflamm 13:5-15
26. Hsu SM, Raine L (1981) Protein a, avidin, and biotin in immunohistochemistry. J Histochem Cytochem 29:1349-1353 (Pubitemid 12231851)
27. Hua XY, Svensson CI, Matsui T, Fitzsimmons B, Yaksh TL, Webb M (2005) Intrathecal minocycline attenuates peripheral inflammation-induced hyperalgesia by inhibiting p38 MAPK in spinal microglia. Eur J Neurosci 22:2431-2440 (Pubitemid 41758986)
28. Hunskaar S, Fasmer OB, Hole K (1985) Formalin test in mice, a useful technique for evaluating mild analgesics. J Neurosci Methods 14:69-75
29. Ichitani Y, Shi T, Haeggstrom JZ, Samuelsson B, Hökfelt T (1997) Increased levels of cyclooxygenase-2 mRNA in the rat spinal cord after peripheral inflammation: an in situ hybridization study. Neuroreport 8:2949-2952 (Pubitemid 27394824)
30. Kelly KJ, Sutton TA, Weathered N, Ray N, Caldwell EJ, Plotkin Z, Dagher PC (2004) Minocycline inhibits apoptosis and inflammation in a rat model of ischemic renal injury. Am J Physiol Renal Physiol 287:F760-F766 (Pubitemid 39280512)
31. Kraus RL, Pasieczny R, Lariosa-Willingham K, Turner MS, Jiang A, Trauger JW (2005) Antioxidant properties of minocycline: neuroprotection in an oxidative stress and direct radicalscavenging activity. J Neurochem 94:819-827 (Pubitemid 41098513)
32. Ledeboer A, Sloane EM, Milligan ED, Frank MG, Mahony JH, Maler SF, Watkins LR (2005) Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115:71-83
33. Leppert D, Lindberg RL, Kappos L, Leib SL (2001) Matrix metalloproteinases: multifunctional effectors of inflammation in multiple sclerosis and bacterial meningitis. Brain Res. Brain Res. Rev 36:249-257
34. Libby P (2007) Inflammatory mechanisms: the molecular basis of inflammation and disease. Nutr Rev 65:S140-S146
35. Lucisano YM, Mantovani B (1984) Lysosomal enzyme release from polymorphonuclear leukocytes induced by immune complexes of IgM and of IgG. J Immunol 132(4):2015-2020 (Pubitemid 14166676)
36. Nieman GF, Zerler BR (2001) A role for the anti-inflammatory properties of tetracyclines in the prevention of acute lung injury. Curr Med Chem 8:317-325 (Pubitemid 32409783)
37. Omote K, Hozama K, Kawamata T, Kawamata M, Nakayaka Y, Toriyabe M, Namiki A (2001) Peripheral nitric oxide in carraggenan-induced inflammation. Brain Res 912:171-175 (Pubitemid 32800671)
38. Padi SS, Kulkarni SK (2008) Minocycline prevents the development of neurophatic pain, but not acute pain: possible anti-inflammatory and amtioxidant mechanisms. Eur J Pharmacol 601:79-87
39. Ramamurthy NS, Greenwald RA, Moak SA, Scuibba J, Goren A, Turner G, Rifkin B, Golub LM, Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ (2008) Microglial activation and TNF-alpha production mediate altered CNS excitability following peripheral inflammation. PNAS 105:17151-17156
40. Riazi K, Galic MA, Kuzmiski JB, Ho W, Sharkey KA, Pittman QJ (2008) Microglial activation and TNF-alpha production mediate altered CNS excitability following peripheral inflammation. Proc Natl Acad Sci USA 105:15151-17156
41. Rifkin B, Vermillo AT, Golub LM (1993) Blocking periodontal disease progression by inhibiting tissue-destructive enzymes: a potential therapeutic role for tetracyclines and their chemically-modified analogs. J Periodontol 64:819-827 (Pubitemid 23278153)
42. Saint-Cricq de Gaulejac NS, Provost C, Vivas N (1999) Comparative study of polyphenol scavenging activities assessed by different methods. J Agric Food Chem 47:425-431 (Pubitemid 29185203)
43. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, Bonventre JV, Woolf CJ (2001) Interleukin-1 beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410:471-475 (Pubitemid 32240046)
44. Sweitzer SM, Colbum RW, Rutkowski M, DeLeo JA (1999) Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat. Brain Res 829:209-221 (Pubitemid 29251705)
45. Tjolsen A, Berge O-G, Hunskaar S et al (1992) The formalin test: an evaluation of the method. Pain 51:5-17
46. Uitto VJ, Firth JD, Nip L, Golub LM (1994) Doxycycline and chemically modified tetracyclines inhibit gelatinase A (MMP-2) gene expression in human skin keratinocytes. Ann NY Acad Sci 732:140-151
47. Villarreal FJ, Griffin M, Omens J, Dillmann W, Nguyen J, Covell J (2003) Early short-term treatment with doxycycline modulates postinfarction left ventricular remodelling. Circulation 108:1487-1492 (Pubitemid 37176456)
48. Wang AL, Yu AC, Lau LT, Lee C, Wu IM, Zhu X, Tso MO (2005) Minocycline inhibits LPS-induced retinal microglia activation. Neurochem Int 47:152-158 (Pubitemid 40848704)
49. Winter CA, Risley EA, Nuss GW (1962) Carrageenen-induced oedema in hind paw of rat: an assay for anti-inflammatory drugs. Proc Soc Exp Biol Med 111:544-547
50. Xiao QG, Liu ZG, Zhang M, Zheng JL, Zhang ZH, Chen JQ (2005) Effect of doxycycline on inflammation-related cytokines and apoptosis in human conjunctival epthelial cells. Zhonghua Yan Ke Za Zhi 41:842-846
51. Zhang ZY, Zhang Z, Fauser U, Schluesener HJ (2009) Improved outcome of EAN, an animal model of GBS, through amelioration of peripheral and central inflammation by minocycline. J Cell Mol Med 13:341-351
52. Zhu S, Stavrosvskaya IG, Drozda M, Kim BY, Ona V, Li M, Sarang S, Liu AS, Hartley DM, Wu du C, Gullans S, Ferrante RJ, Przedborski S, Kristal BS, Friedlander RM (2002) Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 417:74-78 (Pubitemid 34498818)