Mycobacterium tuberculosis, but not vaccine BCG, specifically upregulates matrix metalloproteinase-1

American Journal of Respiratory and Critical Care Medicine

Volumn 172, Issue 12, 2005, Pages 1596-1604

  Elkington, Paul T G ^b   Nuttall, Robert K ^b   Boyle, Joseph J ^b   O'Kane, Cecilia M ^b   Horncastle, Donna E ^b   Edwards, Dylan R ^b   Friedland, Jon S ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b NONE

Author keywords

Macrophage; Matrix metalloproteinases; Mycobacterium tuberculosis; Pathology; Prostaglandin E

Indexed keywords

BCG VACCINE; CYTOKINE; DEXAMETHASONE; DISINTEGRIN; INTERSTITIAL COLLAGENASE; MATRILYSIN; PROSTAGLANDIN; PROSTAGLANDIN E2; TISSUE INHIBITOR OF METALLOPROTEINASE;

ARTICLE; BACTERIAL INFECTION; CONTROLLED STUDY; ENZYME RELEASE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LUNG CAVITATION; LUNG TUBERCULOSIS; MACROPHAGE; MYCOBACTERIUM TUBERCULOSIS; PRIORITY JOURNAL; PROTEIN DOMAIN; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ZYMOGRAPHY;

ADAM PROTEINS; CASE-CONTROL STUDIES; CELL CULTURE TECHNIQUES; HUMANS; MATRIX METALLOPROTEINASES; MONOCYTES; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; RNA, MESSENGER; TISSUE INHIBITOR OF METALLOPROTEINASES; TUBERCULOSIS, PULMONARY;

EID: 30444437042     PISSN: 1073449X     EISSN: 1073449X     Source Type: Journal    
DOI: 10.1164/rccm.200505-753OC     Document Type: Article

References (63)

1. Dye C, Scheele S, Dolin P, Pathania V, Raviglione MC. Global burden of tuberculosis: estimated incidence, prevalence, and mortality by country. WHO Global Surveillance and Monitoring Project [consensus statement]. JAMA 1999;282:677-686.
2. Murray JF. A century of tuberculosis. Am J Respir Crit Care Med 2004;169:1181-1186.
3. Kaplan G, Post FA, Moreira AL, Wainwright H, Kreiswirth BN, Tanverdi M, Mathema B, Ramaswamy SV, Walther G, Steyn LM, et al. Mycobacterium tuberculosis growth at the cavity surface: a microenvironment with failed immunity. Infect Immun 2003;71:7099-7108.
4. Mandell GL, Bennett JE, Dolin R, Douglas RG, editors. Mandell, Douglas, and Bennett's principles and practice of infectious diseases. Philadelphia, PA: Churchill Livingstone; 2000.
5. North RJ, Jung YJ. Immunity to tuberculosis. Annu Rev Immunol 2004;22:599-623.
6. Orme IM. The immunopathogenesis of tuberculosis: a new working hypothesis. Trends Microbiol 1998;6:94-97.
7. Kaufmann SH. A short history of Robert Koch's fight against tuberculosis: those who do not remember the past are condemned to repeat it. Tuberculosis (Edinb) 2003;83:86-90.
8. Crystal RG, West JB. The lung: scientific foundations. Philadelphia, PA: Lippincott; 1997.
9. Owen CA, Campbell EJ. The cell biology of leukocyte-mediated proteolysis. J Leukoc Biol 1999;65:137-150.
10. D'Armiento J, Dalal SS, Okada Y, Berg RA, Chada K. Collagenase expression in the lungs of transgenic mice causes pulmonary emphysema. Cell 1992;71:955-961.
11. Taraseviciene-Stewart L, Scerbavicius R, Choe KH, Moore M, Sullivan A, Nicolls MR, Fontenot AP, Tuder RM, Voelkel NF. An animal model of autoimmune emphysema. Am J Respir Crit Care Med 2005;171:734-742.
12. Churg A, Wang RD, Tai H, Wang X, Xie C, Wright JL. Tumor necrosis factor-α drives 70% of cigarette smoke-induced emphysema in the mouse. Am J Respir Crit Care Med 2004;170:492-498.
13. Choe KH, Taraseviciene-Stewart L, Scerbavicius R, Gera L, Tuder RM, Voelkel NF. Methylprednisolone causes matrix metalloproteinase-dependent emphysema in adult rats. Am J Respir Crit Care Med 2003;167:1516-1521.
14. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 2002;3:207-214.
15. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol 2001;13:534-540.
16. Filippov S, Caras I, Murray R, Matrisian LM, Chapman HA Jr, Shapiro S, Weiss SJ. Matrilysin-dependent elastolysis by human macrophages. J Exp Med 2003;198:925-935.
17. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004;4:617-629.
18. Taggart CC, Greene CM, Carroll TP, O'Neill SJ, McElvaney NG. Elastolytic proteases: inflammation resolution and dysregulation in chronic infective lung disease. Am J Respir Crit Care Med 2005;171:1070-1076.
19. Campbell EJ, Cury JD, Shapiro SD, Goldberg GI, Welgus HG. Neutral proteinases of human mononuclear phagocytes: cellular differentiation markedly alters cell phenotype for serine proteinases, metalloproteinases, and tissue inhibitor of metalloproteinases. J Immunol 1991;146:1286-1293.
20. Welgus HG, Campbell EJ, Cury JD, Eisen AZ, Senior RM, Wilhelm SM, Goldberg GI. Neutral metalloproteinases produced by human mononuclear phagocytes: enzyme profile, regulation, and expression during cellular development. J Clin Invest 1990;86:1496-1502.
21. Lai WC, Zhou M, Shankavaram U, Peng G, Wahl LM. Differential regulation of lipopolysaccharide-induced monocyte matrix metalloproteinase (MMP)-1 and MMP-9 by p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J Immunol 2003;170:6244-6249.
22. Shapiro SD, Kobayashi DK, Pentland AP, Welgus HG. Induction of macrophage metalloproteinases by extracellular matrix: evidence for enzyme- and substrate-specific responses involving prostaglandin-dependent mechanisms. J Biol Chem 1993;268:8170-8175.
23. Busiek DF, Baragi V, Nehring LC, Parks WC, Welgus HG. Matrilysin expression by human mononuclear phagocytes and its regulation by cytokines and hormones. J Immunol 1995;154:6484-6491.
24. Goetzl EJ, Banda MJ, Leppert D. Matrix metalloproteinases in immunity. J Immunol 1996;156:1-4.
25. Flynn JL, Chan J. Immunology of tuberculosis. Annu Rev Immunol 2001;19:93-129.
26. Munger JS, Chapman HA. Tissue destruction by proteases. In: Rom WN, Garay SM, editors. Tuberculosis, 1st ed. Boston: Little, Brown and Company; 1996. pp. 353-361.
27. Elkington PTG, Nutall RK, Boyle JJ, Edwards DR, Friedland JS. Mycobacterium tuberculosis (MTb) stimulates matrix metalloproteinase-1 and -7 expression in human monocytic cells regulated by divergent mechanisms [abstract]. J Leukoc Biol 2004;40.
28. Elkington PTG, Nutall RK, O'Kane CM, Boyle JJ, Edwards DR, Friedland JS. Mechanisms regulating matrix metalloproteinase gene expression and secretion in pulmonary tuberculosis [abstract]. Thorax 2004;59:T5.
29. Nuttall RK, Pennington CJ, Taplin J, Wheal A, Yong VW, Forsyth PA, Edwards DR. Elevated membrane-type matrix metalloproteinases in gliomas revealed by pro.ling proteases and inhibitors in human cancer cells. Mol Cancer Res 2003;1:333-345.
30. Leber TM, Balkwill FR. Zymography: a single-step staining method for quantitation of proteolytic activity on substrate gels. Anal Biochem 1997;249:24-28.
31. Joint Tuberculosis Committee of the British Thoracic Society. Chemotherapy and management of tuberculosis in the UK: recommendations 1998. Thorax 1998;53:536-548.
32. Shapiro SD, Campbell EJ, Kobayashi DK, Welgus HG. Dexamethasone selectively modulates basal and lipopolysaccharide-induced metalloproteinase and tissue inhibitor of metalloproteinase production by human alveolar macrophages. J Immunol 1991;146:2724-2729.
33. Zhang Y, McCluskey K, Fujii K, Wahl LM. Differential regulation of monocyte matrix metalloproteinase and TIMP-1 production by TNF-α, granulocyte-macrophage CSF, and IL-1β through prostaglandin-dependent and -independent mechanisms. J Immunol 1998;161:3071-3076.
34. Zhou M, Zhang Y, Ardans JA, Wahl LM. Interferon-γ differentially regulates monocyte matrix metalloproteinase-1 and -9 through tumor necrosis factor-α and caspase 8. J Biol Chem. 2003.
35. Wickremasinghe MI, Thomas LH, O'Kane CM, Uddin J, Friedland JS. Transcriptional mechanisms regulating alveolar epithelial cell-specific CCL5 secretion in pulmonary tuberculosis. J Biol Chem 2004;279:27199-27210.
36. Newport MJ, Huxley CM, Huston S, Hawrylowicz CM, Oostra BA, Williamson R, Levin M. A mutation in the interferon-γ-receptor gene and susceptibility to mycobacterial infection. N Engl J Med 1996;335:1941-1949.
37. Lopez-Maderuelo D, Arnalich F, Serantes R, Gonzalez A, Codoceo R, Madero R, Vazquez JJ, Montiel C. Interferon-γ and interleukin-10 gene polymorphisms in pulmonary tuberculosis. Am J Respir Crit Care Med 2003;167:970-975.
38. Wahl LM, Olsen CE, Sandberg AL, Mergenhagen SE. Prostaglandin regulation of macrophage collagenase production. Proc Natl Acad Sci USA 1977;74:4955-4958.
39. Corcoran ML, Stetler-Stevenson WG, Brown PD, Wahl LM. Interleukin 4 inhibition of prostaglandin E2 synthesis blocks interstitial collagenase and 92-kDa type IV collagenase/gelatinase production by human monocytes. J Biol Chem 1992;267:515-519.
40. Welgus HG, Jeffrey JJ, Stricklin GP, Roswit WT, Eisen AZ. Characteristics of the action of human skin fibroblast collagenase on fibrillar collagen. J Biol Chem 1980;255:6806-6813.
41. Davidson JM. Biochemistry and turnover of lung interstitium. Eur Respir J 1990;3:1048-1063.
42. Shapiro SD,Endicott SK, Province MA, Pierce JA, Campbell EJ. Marked longevity of human lung parenchymal elastic fibers deduced from prevalence of D-aspartate and nuclear weapons-related radiocarbon. J Clin Invest 1991;87:1828-1834.
43. Shapiro SD, Campbell EJ, Welgus HG, Senior RM. Elastin degradation by mononuclear phagocytes. Ann N Y Acad Sci 1991;624:69-80.
44. Imai K, Dalal SS, Chen ES, Downey R, Schulman LL, Ginsburg M, D'Armiento J. Human collagenase (matrix metalloproteinase-1) expression in the lungs of patients with emphysema. Am J Respir Crit Care Med 2001;163:786-791.
45. Finlay GA, O'Driscoll LR, Russell KJ, D'Arcy EM, Masterson JB, FitzGerald MX, O'Connor CM. Matrix metalloproteinase expression and production by alveolar macrophages in emphysema. Am J Respir Crit Care Med 1997;156:240-247.
46. Segura-Valdez L, Pardo A, Gaxiola M, Uhal BD, Becerril C, Selman M. Upregulation of gelatinases A and B, collagenases 1 and 2, and increased parenchymal cell death in COPD. Chest 2000;117:684-694.
47. Selman M, Montano M, Ramos C, Vanda B, Becerril C, Delgado J, Sansores R, Barrios R, Pardo A. Tobacco smoke-induced lung emphysema in guinea pigs is associated with increased interstitial collagenase. Am J Physiol 1996;271:L734-L743.
48. Balbin M, Fueyo A, Knauper V, Lopez JM, Alvarez J, Sanchez LM, Quesada V, Bordallo J, Murphy G, Lopez-Otin C. Identification and enzymatic characterization of two diverging murine counterparts of human interstitial collagenase (MMP-1) expressed at sites of embryo implantation. J Biol Chem 2001;276:10253-10262.
49. Wahl SM, Wahl LM, McCarthy JB, Chedid L, Mergenhagen SE. Macrophage activation by mycobacterial water soluble compounds and synthetic muramyl dipeptide. J Immunol 1979;122:2226-2231.
50. Chang JC, Wysocki A, Tchou-Wong KM, Moskowitz N, Zhang Y, Rom WN. Effect of Mycobacterium tuberculosis and its components on macrophages and the release of matrix metalloproteinases. Thorax 1996;51:306-311.
51. Price NM, Farrar J, Tran TT, Nguyen TH, Tran TH, Friedland JS. Identification of a matrix-degrading phenotype in human tuberculosis in vitro and in vivo. J Immunol 2001;166:4223-4230.
52. Rivera-Marrero CA, Schuyler W, Roser S, Ritzenthaler JD, Newburn SA, Roman J. M. tuberculosis induction of matrix metalloproteinase-9: the role of mannose and receptor-mediated mechanisms. Am J Physiol Lung Cell Mol Physiol 2002;282:L546-L555.
53. Quiding-Jarbrink M, Smith DA, Bancroft GJ. Production of matrix metalloproteinases in response to mycobacterial infection. Infect Immun 2001;69:5661-5670.
54. Price NM, Gilman RH, Uddin J, Recavarren S, Friedland JS. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-α-dependent monocyte networks. J Immunol 2003;171:5579-5586.
55. Pierce RA, Sandefur S, Doyle GA, Welgus HG. Monocytic cell type-specific transcriptional induction of collagenase. J Clin Invest 1996;97:1890-1899.
56. Grosset J. Mycobacterium tuberculosis in the extracellular compartment: an underestimated adversary. Antimicrob Agents Chemother 2003;47:833-836.
57. Turner OC, Basaraba RJ, Orme IM. Immunopathogenesis of pulmonary granulomas in the guinea pig after infection with Mycobacterium tuberculosis. Infect Immun 2003;71:864-871.
58. Thwaites GE, Nguyen DB, Nguyen HD, Hoang TQ, Do TT, Nguyen TC, Nguyen QH, Nguyen TT, Nguyen NH, Nguyen TN, et al. Dexamethasone for the treatment of tuberculous meningitis in adolescents and adults. N Engl J Med 2004;351:1741-1751.
59. Jonat C, Rahmsdorf HJ, Park KK, Cato AC, Gebel S, Ponta H, Herrlich P. Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell 1990;62:1189-1204.
60. Saren P, Welgus HG, Kovanen PT. TNF-α and IL-1β selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol 1996;157:4159-4165.
61. Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 1996;178:1274-1282.
62. Tse HM, Josephy SI, Chan ED, Fouts D, Cooper AM. Activation of the mitogen-activated protein kinase signaling pathway is instrumental in determining the ability of Mycobacterium avium to grow in murine macrophages. J Immunol 2002;168:825-833.
63. Harris SG, Padilla J, Koumas L, Ray D, Phipps RP. Prostaglandins as modulators of immunity. Trends Immunol 2002;23:144-150.