The antibiotics doxycycline and minocycline inhibit the inflammatory responses to the lyme disease spirochete borrelia burgdorferi

Journal of Infectious Diseases

Volumn 199, Issue 9, 2009, Pages 1379-1388

  Bernardino, Andrea L F ^a   Kaushal, Deepak ^a   Philipp, Mario T ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MINOCYCLINE; OUTER SURFACE PROTEIN A; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; ASTROCYTE; BORRELIA BURGDORFERI; CELL STIMULATION; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DNA BINDING; DOSE RESPONSE; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYME DISEASE; MICROARRAY ANALYSIS; MICROGLIA; MONOCYTE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RHESUS MONKEY; WESTERN BLOTTING;

ANIMALS; ANTI-BACTERIAL AGENTS; ASTROCYTES; BORRELIA BURGDORFERI; BRAIN; CELL CULTURE TECHNIQUES; CELL LINE; CELL SURVIVAL; DOXYCYCLINE; EXONS; HUMANS; INFLAMMATION; LYME DISEASE; MACACA MULATTA; MICROGLIA; MINOCYCLINE; MONOCYTES; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA; SIGNAL TRANSDUCTION;

EID: 65749115383     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1086/597807     Document Type: Article

References (50)

1. Barthold SW, Persing DH, Armstrong AL, Peeples RA. Kinetics of Borrelia burgdorferi dissemination and evolution of disease after intradermal inoculation of mice. Am J Pathol 1991; 139:263-73.
2. Yang L, Weis JH, Eichwald E, Kolbert CP, Persing DH, Weis JJ. Heritable susceptibility to severe Borrelia burgdorferi-induced arthritis is dominant and is associated with persistence of large numbers of spirochetes in tissues. Infect Immun 1994; 62:492-500.
3. Defosse DL, Johnson RC. In vitro and in vivo induction of tumor necrosis factor alpha by Borrelia burgdorferi. Infect Immun 1992; 60:1109-13.
4. Kenefick KB, Lim LC, Alder JD, Schmitz JL, Czuprynski CJ, Schell RF. Induction of interleukin-1 release by high- and low-passage isolates of Borrelia burgdorferi. J Infect Dis 1993; 167:1086-92.
5. Tai KF, Ma Y, Weis JJ. Normal human B lymphocytes and mononuclear cells respond to the mitogenic and cytokine-stimulatory activities of Borrelia burgdorferi and its lipoprotein OspA. Infect Immun 1994; 62: 520-8.
6. Ganapamo F, Dennis V, Phillip MT. CD19- cells produce IFN-gamma in mice infected with Borrelia burgdorferi. Eur J Immunol 2001; 31: 3460-8.
7. Knauer J, Siegemund S, Müller U, et al. Borrelia burgdorferi potently activates bone marrow-derived conventional dendritic cells for production of IL-23 required for IL-17 release by T cells. FEMS Immunol Med Microbiol 2007; 49:353-63.
8. Grygorczuk S, Pancewicz S, Zajkowska J, Kondrusik M, Rwierzbinska R, Hermanowska-Szpakowicz T. Concentrations of macrophage inflammatory proteins MIP-1alpha and MIP-1beta and interleukin 8 (IL-8) in Lyme borreliosis. Infection 2004; 32:350-5.
9. Zhao Z, McCloud B, Fleming R, Klempner MS. Borrelia burgdorferiinduced monocyte chemoattractant protein-1 production in vivo and in vitro. Biochem Biophys Res Commun 2007; 358:528-33.
10. Seiler KP, Vavrin Z, Eichwald E, Hibbs JB Jr, Weis JJ. Nitric oxide production during murine Lyme disease: lack of involvement in host resistance or pathology. Infect Immun 1995; 63:3886-95.
11. Wormser GP, Dattwyler RJ, Shapiro ED, et al. The clinical assessment, treatment, and prevention of Lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 2006; 43:1089-134.
12. Klein NC, Cunha BA. Tetracycline. Med Clin North Am 1995; 79:789-801.
13. Franklin TJ. The inhibition of incorporation of leucine into protein of cell-free systems from rat liver and Escherichia coli by chlortetracycline. Biochem J 1963; 87:449-53.
14. Sapadin AN, Fleischmajer R. Tetracycline: nonantibiotic properties and their clinical implication. J Am Acad Dermatol 2006; 54:258-65.
15. Clark WM, Lessov N, Lauten JD, Hazel K. Doxycycline treatment reduces ischemic brain damage in transient middle cerebral artery occlusion in the rat. J Mol Neurosci 1997; 9:103-8.
16. Yrjanheikki J, Keinanen R, Pellikka M, Hokfelt T, Koistinaho J. Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc Natl Acad Sci USA 1998; 95:15769-74.
17. Yrjanheikki J, Tikka T, Keinanen R, Goldsteins G, Chain PH, Koistinaho J. A tetracycline derivative, minocycline, reduces inflammation and protects against focal cerebral ischemia with a wide therapeutic window. Proc Natl Acad Sci USA 1999; 96:13496-500.
18. Jantzie LL, Cheung PY, Todd KG. Doxycycline reduces cleaved caspase-3 and microglial activation in an animal model of neonatal hypoxia-ischemia. J Cereb Blood Flow Metab 2005; 25:314-24.
19. Chen M, Ona VO, Li M, et al. Minocycline inhibits caspase-1 and caspase-3 expression and delays mortality in a transgenic mouse model of Huntington's disease. Nat Med 2000; 6:797-801.
20. Wang X, Zhu S, Drozda M, et al. Minocycline inhibits caspaseindependent and -dependent mitochondrial cell death pathways in models of Huntington's disease. Proc Natl Acad Sci USA 2003; 100: 10483-7.
21. Du Y, Ma Z, Lin S, et al. Minocycline prevents nigrostriatal dopaminergic neurodegeneration in the MPTP model of Parkinson's disease. Proc Natl Acad Sci USA 2001; 98:14669-74.
22. Choi Y, Kim HS, Shin KY, et al. Minocycline attenuates neuronal cell death and improves cognitive impairment in Alzheimer's disease models. Neuropsychopharmacology 2007; 32:2393-404.
23. Zhu S, Stavrovskaya IG, Drozda M, et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002; 417:74-8.
24. Brundula V, Rewcastle NB, Metz LM, Bernard CC, Yong VW. Targeting leukocyte MMPs and transmigration: minocycline as a potencial therapy for multiple sclerosis. Brain 2002; 125:1297-308.
25. Lee SM, Yune TY, Kim SJ, et al. Minocycline reduces cell death and improves functional recovery after traumatic spinal cord injury in the rat. J Neurotrauma 2003; 20:1017-27.
26. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J. Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 2001; 21:2580 - 8.
27. WuDC, Jackson-Lewis V, Vila M, et al. Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J Neurosci 2002; 22:1763-71.
28. Nikodemova M, Ducan ID, Watters JJ. Minocycline exerts inhibitory effects on multiple mitogen-activated protein kinases and I-B- degradation in a stimulus-specific manner in microglia. J Neurochem 2006; 96:314-23.
29. Bernardino AL, Myers TA, Alvarez X, Hasegawa A, Philipp MT. Tolllike receptors: insights into their possible role in the pathogenesis of Lyme neuroborreliosis. Infect Immun 2008; 76:4385-95.
30. Tekautz TM, Zhu K, Grenet J, Kaushal D, Kidd VJ, Lahti JM. Evaluation of IFN-gamma effects on apoptosis and gene expression in neuroblastoma- preclinical studies. Biochim Biophys Acta 2006; 1763:1000-10.
31. Kaushal D, Naeve CW. Analyzing and visualizing expression data with Spotfire. Baxevanis AD et al, eds. Current protocols in bioinformatics. Unit 7, chapter 9. Hoboken, NJ: John Wiley & Sons, 2004:7.9.1-7.9.25.
32. Yang YH, Dudoit S, Luu P, et al. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 2002; 30:e15.
33. Kielian T, Esen N, Liu S, et al. Minocycline modulates neuroinflammation independently of its antimicrobial activity in Staphylococcus aureusinduced brain abscess. Am J Pathol 2007; 171:1199-213.
34. Giambartolomei GH, Dennis V, Lasater BL, Philipp MT. Induction of pro- and anti-inflammatory cytokines by Borrelia burgdorferi lipoproteins in monocytes is mediated by CD14. Infect Immun 1999; 67:140-7.
35. MooreMW,Cruz AR, LaVake CJ, et al. Phagocytosis of Borrelia burgdorferi and Treponema pallidum potentiates innateimmuneactivation and induces gamma interferon production. Infect Immun 2007; 75:2046-62.
36. Zhang J, Ghosh S. Toll-like receptor-mediated NF-B activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest 2001; 107:13-9.
37. Karin M, Lin A. NF-B at the crossroad of life and death. Nat Immunol 2002; 3:221-7.
38. Hayden MS, Ghosh S. Shared principles in NF-B signaling. Cell 2008; 132:344 - 61.
39. Norgard MV, Arndt LL, Akins DR, Curetty LL, Harrich DA, Radolf JD. Activation of human monocytes cells by Trepanema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopropeptides proceeds via a pathway distinct from the lipopolysaccharide but involves the transcriptional activator NF-kappa B. Infect Immun 1996; 64:3845-52.
40. Cruz AR, Moore MW, La Vake CJ, Eggers CH, Salazar JC, Radolf JD. Phagocytosis of Borrelia burgdorferi, the Lyme disease spirochete, potentiates innate immune activation and induces apoptosis in human monocytes. Infect Immun 2008; 76:56-70.
41. Ghosh S, Karin M. Missing piece in the NF-B puzzle. Cell 2002; 109(Suppl):S81-96.
42. Izadi H, Motameni AT, Bates TC, et al. c-Jun N-terminal kinase 1 is required for Toll-like receptor 1 gene expression in macrophages. Infect Immun 2007; 75:5027-34.
43. Gonzalez-Scarano F, Baltuch G. Microglia as mediators of inflammatory and degenerative disease. Annu Rev Neurosci 1999; 22:219-40.
44. Kreutzberg GW. Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996; 19:312-8.
45. Familian A, Boshuizen RS, Eikelenboom P, Veerhuis R. Inhibitory effect of minocycline on amyloid - fibril formation and human microglial activation. Glia 2006; 53:233-40.
46. Dong Y, Benveniste EN. Immune function of astrocytes. Glia 2001; 36: 180-90.
47. Lee SM, Yune TY, Kim SJ, et al. Minocycline inhibits apoptotic cell death via attenuation of TNF- expression following iNOS/NO induction by lipopolysaccharide in neuron/glia co-cultures. J Neurochem 2004; 91: 568-78.
48. Wang AL, Yu ACH, Lau LT, et al. Minocycline inhibits LPS-induced retinal microglia activation. Neurochem Int 2005; 47:152-8.
49. Nowakowski J, Nadelman RB, Sell R, et al. Long-term follow-up of patients with culture-confirmed Lyme disease. Am J Med 2003; 115: 91-6.
50. Klempner MS, Hu LT, Evans J, et al. Two controlled trials of antibiotic treatment in patients with persistent symptoms and a history of Lyme disease. N Engl J Med 2001; 345:85-92.