Tuberculosis, pulmonary cavitation, and matrix metalloproteinases

American Journal of Respiratory and Critical Care Medicine

Volumn 190, Issue 1, 2014, Pages 9-18

  Ong, Catherine W M ^a,b   Elkington, Paul T ^c,d   Friedland, Jon S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Cavity; Collagenases; Matrix metalloproteinases; Tuberculosis

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; IMMUNOMODULATING AGENT; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; NEUTROPHIL COLLAGENASE; PROTEINASE; STROMELYSIN; STROMELYSIN 2;

DISEASE COURSE; DISEASE TRANSMISSION; HUMAN; IMMUNOTHERAPY; LUNG CAVITATION; LUNG STRUCTURE; LUNG TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW;

CAVITY; COLLAGENASES; MATRIX METALLOPROTEINASES; TUBERCULOSIS;

ANIMALS; ANTITUBERCULAR AGENTS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DRUG DELIVERY SYSTEMS; HUMANS; IMMUNOMODULATION; MATRIX METALLOPROTEINASES; MYCOBACTERIUM TUBERCULOSIS; PULMONARY INFARCTION; TUBERCULOSIS, MULTIDRUG-RESISTANT; TUBERCULOSIS, PULMONARY; WORLD HEALTH;

EID: 84903840319     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201311-2106PP     Document Type: Review

References (100)

1. Hershkovitz I, Donoghue HD, Minnikin DE, Besra GS, Lee OY, Gernaey AM, Galili E, Eshed V, Greenblatt CL, Lemma E, et al. Detection and molecular characterization of 9,000-year-old Mycobacterium tuberculosis from a Neolithic settlement in the Eastern Mediterranean. PLoS ONE 2008;3: e3426.
2. World Health Organization. Global tuberculosis report 2013. 2013 [accessed 2014 May 8]. Available from: http://apps.who.int/iris/bitstream/10665/ 91355/1/9789241564656-eng.pdf?ua=1
3. Klopper M, Warren RM, Hayes C, Gey van Pittius NC, Streicher EM, M?uller B, Sirgel FA, Chabula-Nxiweni M, Hoosain E, Coetzee G, et al. Emergence and spread of extensively and totally drug-resistant tuberculosis, South Africa. Emerg Infect Dis 2013;19: 449-455.
4. Kempker RR, Rabin AS, Nikolaishvili K, Kalandadze I, Gogishvili S, Blumberg HM, Vashakidze S. Additional drug resistance in Mycobacterium tuberculosis isolates from resected cavities among patients with multidrug-resistant or extensively drug-resistant pulmonary tuberculosis. Clin Infect Dis 2012;54: e51-e54.
5. Chatterjee A, D'Souza D, Vira T, Bamne A, Ambe GT, Nicol MP, Wilkinson RJ, Mistry N. Strains of Mycobacterium tuberculosis from western Maharashtra, India, exhibit a high degree of diversity and strain-specific associations with drug resistance, cavitary disease, and treatment failure. J Clin Microbiol 2010;48: 3593-3599.
6. Nardell EA, Piessens WF. Transmission of tuberculosis. New York: Marcel Dekker; 2000.
7. Ong CWM, Elkington P, Ugarte-Gil C, Tezera LB, Gilman R, Porter JC, Friedland JS. Tissue destruction and cavitation: neutrophils wield a double-edged sword in human pulmonary tuberculosis. Presented at IDweek. October 5, 2013, San Francisco, CA.
8. Ong C, Elkington P, Singh S, Friedland JS. Neutrophils drive MMP-8/-9 gene expression and secretion in tuberculosis by complex mechanisms. Presented at the Annual Meeting of the Society for Leukocyte Biology. September 23, 2011, Kansas City, MO.
9. Ong CWM, Elkington PT, Ugarte-Gil C, Tezera LB, Porter JC, Friedland JS. Neutrophils cause matrix destruction in human pulmonary tuberculosis: in vitro and in vivo evidence from a clinical cohort. Immunology 2012;137: 148-149.
10. Ong CWM, Elkington PT, Ugarte-Gil C, Tezera LB, Patel V, Tome-Esteban MT, Porter JC, Friedland JS. Neutrophil MMP-8/-9 cause matrix destruction in human TB and are regulated by an AMPKdependent pathway. Presented at the Gordon Research Conference: Matrix Metalloproteinases -Crucial Components of Molecular Networks and Disease Pathways. May 23, 2013, Lucca (Barga), Italy.
11. Kubler A, Luna B, Larsson C, Ammerman N, Urbanowski M, Marshall J, Andrade B, Orandle M, Klunk M, Jain S, et al. A preclinical model of cavitary tuberculosis. Presented at the Imperial College London Division of Infectious Diseases PhD Day. November 7, 2013, London, UK.
12. Dannenberg AMJr. Delayed-Type hypersensitivity and cell-mediated immunity in the pathogenesis of tuberculosis. Immunol Today 1991;12: 228-233.
13. Sturgill-Koszycki S, Schlesinger PH, Chakraborty P, Haddix PL, Collins HL, Fok AK, Allen RD, Gluck SL, Heuser J, Russell DG. Lack of acidification in Mycobacterium phagosomes produced by exclusion of the vesicular proton-ATPase. Science 1994;263: 678-681.
14. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129: 1287-1298.
15. Ramakrishnan L. Revisiting the role of the granuloma in tuberculosis. Nat Rev Immunol 2012;12: 352-366.
16. O'Kane CM, Boyle JJ, Horncastle DE, Elkington PT, Friedland JS. Monocyte-dependent fibroblast CXCL8 secretion occurs in tuberculosis and limits survival of mycobacteria within macrophages. J Immunol 2007;178: 3767-3776.
17. 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.
18. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010;327: 466-469.
19. Dannenberg AM Jr, Sugimoto M. Liquefaction of caseous foci in tuberculosis. Am Rev Respir Dis 1976;113: 257-259.
20. Kim MJ, Wainwright HC, Locketz M, Bekker LG, Walther GB, Dittrich C, Visser A, Wang W, Hsu FF, Wiehart U, et al. Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2010;2: 258-274.
21. Bateman ED, Turner-Warwick M, Adelmann-Grill BC. Immunohistochemical study of collagen types in human foetal lung and fibrotic lung disease. Thorax 1981;36: 645-653.
22. Davidson JM. Biochemistry and turnover of lung interstitium. Eur Respir J 1990;3: 1048-1063.
23. Dannenberg AM Jr. Liquefaction and cavity formation in pulmonary TB: a simple method in rabbit skin to test inhibitors. Tuberculosis (Edinb) 2009;89: 243-247.
24. Khokha R, Murthy A, Weiss A.Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol 2013;13: 649-665.
25. Soslau G, Mason C, Lynch S, Benjamin J, Ashak D, Prakash JM, Moore A, Bagsiyao P, Albert T, Mathew LM, et al. Intracellular matrix metalloproteinase-2 (MMP-2) regulates human platelet activation via hydrolysis of talin. Thromb Haemost 2014;111: 140-153.
26. Brew K, Dinakarpandian D, Nagase H. Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 2000;1477: 267-283.
27. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006;69: 562-573.
28. Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta 2010;1803: 55-71.
29. Hunter RL. Pathology of post primary tuberculosis of the lung: an illustrated critical review. Tuberculosis (Edinb) 2011;91: 497-509.
30. Elkington PT, D'Armiento JM, Friedland JS. Tuberculosis immunopathology: the neglected role of extracellular matrix destruction. Sci Transl Med 2011;3: ps6.
31. Dharmadhikari AS, Nardell EA. What animal models teach humans about tuberculosis. Am J Respir Cell Mol Biol 2008;39: 503-508.
32. Young D. Animal models of tuberculosis. Eur J Immunol 2009;39: 2011-2014.
33. Helke KL, Mankowski JL, Manabe YC. Animal models of cavitation in pulmonary tuberculosis. Tuberculosis (Edinb) 2006;86: 337-348.
34. Heuts F, Gavier-Widé n D, Carow B, Juarez J, Wigzell H, Rottenberg ME. CD41 cell-dependent granuloma formation in humanized mice infected with mycobacteria. Proc Natl Acad Sci USA 2013; 110: 6482-6487.
35. Ehlers S, Benini J, Held HD, Roeck C, Alber G, Uhlig S. Alphabeta T cell receptor-positive cells and interferon-gamma, but not inducible nitric oxide synthase, are critical for granuloma necrosis in a mouse model of mycobacteria-induced pulmonary immunopathology. J Exp Med 2001;194: 1847-1859.
36. Ehlers S, Kutsch S, Ehlers EM, Benini J, Pfeffer K. Lethal granuloma disintegration in mycobacteria-infected TNFRp55-/-mice is dependent on T cells and IL-12. J Immunol 2000;165: 483-492.
37. Pearl JE, Torrado E, Tighe M, Fountain JJ, Solache A, Strutt T, Swain S, Appelberg R, Cooper AM. Nitric oxide inhibits the accumulation of CD41CD44hiTbet1CD69lo T cells in mycobacterial infection. Eur J Immunol 2012;42: 3267-3279.
38. Reece ST, Loddenkemper C, Askew DJ, Zedler U, Schommer-Leitner S, Stein M, Mir FA, Dorhoi A, Mollenkopf HJ, Silverman GA, et al. Serine protease activity contributes to control of Mycobacterium tuberculosis in hypoxic lung granulomas in mice. J Clin Invest 2010; 120: 3365-3376.
39. Elkington P, Shiomi T, Breen R, Nuttall RK, Ugarte-Gil CA, Walker NF, Saraiva L, Pedersen B, Mauri F, Lipman M, et al. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J Clin Invest 2011;121: 1827-1833.
40. Lemâitre V, O'Byrne TK, Borczuk AC, Okada Y, Tall AR, D'Armiento J. ApoE knockout mice expressing human matrix metalloproteinase-1 in macrophages have less advanced atherosclerosis. J Clin Invest 2001;107: 1227-1234.
41. Izzo AA, Izzo LS, Kasimos J, Majka S. A matrix metalloproteinase inhibitor promotes granuloma formation during the early phase of Mycobacterium tuberculosis pulmonary infection. Tuberculosis (Edinb) 2004;84: 387-396.
42. Taylor JL, Hattle JM, Dreitz SA, Troudt JM, Izzo LS, Basaraba RJ, Orme IM, Matrisian LM, Izzo AA. Role for matrix metalloproteinase 9 in granuloma formation during pulmonary Mycobacterium tuberculosis infection. Infect Immun 2006;74: 6135-6144.
43. Balasubramanian V, Wiegeshaus EH, Smith DW. Growth characteristics of recent sputum isolates of Mycobacterium tuberculosis in guinea pigs infected by the respiratory route. Infect Immun 1992;60: 4762-4767.
44. Lurie MB. Experimental epidemiology of tuberculosis: the effect of eliminating exposure to enteric infection on the incidence and course of tuberculosis acquired by normal guinea pigs confined with tuberculous cage mates. J Exp Med 1930;51: 753-768.
45. Zhukova NL, Gedymin LE, Golyshevskaia VI. Comparative characteristics of the activity of proteolytic enzymes and their inhibitors in the lung tissue of guinea pigs during development of generalized and destructive tuberculosis [in Russian]. Vopr Med Khim 1986;32: 80-84.
46. Ratcliffe HL, Wells WF. Tuberculosis of rabbits induced by droplet nuclei infection; response to reinfection. J Exp Med 1948;87: 585-594.
47. Dorman SE, Hatem CL, Tyagi S, Aird K, Lopez-Molina J, Pitt ML, Zook BC, Dannenberg AM Jr, Bishai WR, Manabe YC. Susceptibility to tuberculosis: clues from studies with inbred and outbred New Zealand White rabbits. Infect Immun 2004;72: 1700-1705.
48. Converse PJ, Dannenberg AM Jr, Estep JE, Sugisaki K, Abe Y, Schofield BH, Pitt ML. Cavitary tuberculosis produced in rabbits by aerosolized virulent tubercle bacilli. Infect Immun 1996;64: 4776-4787.
49. Subbian S, Tsenova L, O'Brien P, Yang G, Koo MS, Peixoto B, Fallows D, Zeldis JB, Muller G, Kaplan G. Phosphodiesterase-4 inhibition combined with isoniazid treatment of rabbits with pulmonary tuberculosis reduces macrophage activation and lung pathology. Am J Pathol 2011;179: 289-301.
50. Flynn JL. Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect 2006;8: 1179-1188.
51. Mehra S, Pahar B, Dutta NK, Conerly CN, Philippi-Falkenstein K, Alvarez X, Kaushal D. Transcriptional reprogramming in nonhuman primate (rhesus macaque) tuberculosis granulomas. PLoS ONE 2010;5: e12266.
52. Kuo HP, Wang YM, Wang CH, He CC, Lin SM, Lin HC, Liu CY, Huang KH, Hsieh LL, Huang CD. Matrix metalloproteinase-1 polymorphism in Taiwanese patients with endobronchial tuberculosis. Tuberculosis (Edinb) 2008;88: 262-267.
53. Ganachari M, Ruiz-Morales JA, Gomez de la Torre Pretell JC, Dinh J, Granados J, Flores-Villanueva PO. Joint effect of MCP-1 genotype GG and MMP-1 genotype 2G/2G increases the likelihood of developing pulmonary tuberculosis in BCG-vaccinated individuals. PLoS ONE 2010;5: e8881.
54. Wang CH, Lin HC, Lin SM, Huang CD, Liu CY, Huang KH, Hsieh LL, Chung KF, Kuo HP. MMP-1(-1607G) polymorphism as a risk factor for fibrosis after pulmonary tuberculosis in Taiwan. Int J Tuberc Lung Dis 2010;14: 627-634.
55. Lee SH, Han SK, Shim YS, Yim JJ. Effect of matrix metalloproteinase-9 -1562C/T gene polymorphism on manifestations of pulmonary tuberculosis. Tuberculosis (Edinb) 2009;89: 68-70.
56. Elkington PT, Nuttall RK, Boyle JJ, O'Kane CM, Horncastle DE, Edwards DR, Friedland JS. Mycobacterium tuberculosis, but not vaccine BCG, specifically upregulates matrix metalloproteinase-1. Am J Respir Crit Care Med 2005;172: 1596-1604.
57. Singh S, Saraiva L, Elkington PT, Friedland JS. Regulation of matrix metalloproteinase-1, -3, and -9 in Mycobacterium tuberculosisdependent respiratory networks by the rapamycin-sensitive PI3K/p70S6K cascade. FASEB J 2014;28: 85-93.
58. Elkington PT, Emerson JE, Lopez-Pascua LD, O'Kane CM, Horncastle DE, Boyle JJ, Friedland JS. Mycobacterium tuberculosis up-regulates matrix metalloproteinase-1 secretion from human airway epithelial cells via a p38 MAPK switch. J Immunol 2005;175: 5333-5340.
59. Elkington PT, Green JA, Emerson JE, Lopez-Pascua LD, Boyle JJ, O'Kane CM, Friedland JS. Synergistic up-regulation of epithelial cell matrix metalloproteinase-9 secretion in tuberculosis. Am J Respir Cell Mol Biol 2007;37: 431-437.
60. Ugarte-Gil CA, Elkington P, Gilman RH, Coronel J, Tezera LB, Bernabe-Ortiz A, Gotuzzo E, Friedland JS, Moore DA. Induced sputum MMP-1, -3 & -8 concentrations during treatment of tuberculosis. PLoS ONE 2013;8: e61333.
61. Walker NF, Clark SO, Oni T, Andreu N, Tezera L, Singh S, Saraiva L, Pedersen B, Kelly DL, Tree JA, et al. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am J Respir Crit Care Med 2012;185: 989-997.
62. Sundararajan S, Babu S, Das SD. Comparison of localized versus systemic levels of Matrix metalloproteinases (MMPs), its tissue inhibitors (TIMPs) and cytokines in tuberculous and non-Tuberculous pleuritis patients. Hum Immunol 2012;73: 985-991.
63. Thwaites GE, Simmons CP, Than Ha Quyen N, Thi Hong Chau T, Phuong Mai P, Thi Dung N, Hoan Phu N, White NP, Tinh Hien T, Farrar JJ. Pathophysiology and prognosis in vietnamese adults with tuberculous meningitis. J Infect Dis 2003;188: 1105-1115.
64. Coussens AK, Wilkinson RJ, Nikolayevskyy V, Elkington PT, Hanifa Y, Islam K, Timms PM, Bothamley GH, Claxton AP, Packe GE, et al. Ethnic variation in inflammatory profile in tuberculosis. PLoS Pathog 2013;9: e1003468.
65. Coussens A, Timms PM, Boucher BJ, Venton TR, Ashcroft AT, Skolimowska KH, Newton SM, Wilkinson KA, Davidson RN, Griffiths CJ, et al. 1alpha,25- dihydroxyvitamin D3 inhibits matrix metalloproteinases induced by Mycobacterium tuberculosis infection. Immunology 2009;127: 539-548.
66. Seddon J, Kasprowicz V, Walker NF, Yuen HM, Sunpath H, Tezera L, Meintjes G, Wilkinson RJ, Bishai WR, Friedland JS, et al. Procollagen III N-Terminal propeptide and desmosine are released by matrix destruction in pulmonary tuberculosis. J Infect Dis 2013;208: 1571-1579.
67. Eum SY, Kong JH, Hong MS, Lee YJ, Kim JH, Hwang SH, Cho SN, Via LE, Barry CE III. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 2010; 137: 122-128.
68. Rand L, Green JA, Saraiva L, Friedland JS, Elkington PT. Matrix metalloproteinase-1 is regulated in tuberculosis by a p38 MAPKdependent, p-Aminosalicylic acid-sensitive signaling cascade. J Immunol 2009;182: 5865-5872.
69. O'Kane CM, Elkington PT, Jones MD, Caviedes L, Tovar M, Gilman RH, Stamp G, Friedland JS. STAT3, p38 MAPK, and NF-kappaB drive unopposed monocyte-dependent fibroblast MMP-1 secretion in tuberculosis. Am J Respir Cell Mol Biol 2010;43: 465-474.
70. Green JA, Elkington PT, Pennington CJ, Roncaroli F, Dholakia S, Moores RC, Bullen A, Porter JC, Agranoff D, Edwards DR, et al. Mycobacterium tuberculosis upregulates microglial matrix metalloproteinase-1 and -3 expression and secretion via NFkappaB-And Activator Protein-1-dependent monocyte networks. J Immunol 2010;184: 6492-6503.
71. Green JA, Dholakia S, Janczar K, Ong CW, Moores R, Fry J, Elkington PT, Roncaroli F, Friedland JS. Mycobacterium tuberculosis-infected human monocytes down-regulate microglial MMP-2 secretion in CNS tuberculosis via TNFa, NFkB, p38 and caspase 8 dependent pathways. J Neuroinflammation 2011;8: 46.
72. Harris JE, Nuttall RK, Elkington PT, Green JA, Horncastle DE, Graeber MB, Edwards DR, Friedland JS. Monocyte-Astrocyte networks regulate matrix metalloproteinase gene expression and secretion in central nervous system tuberculosis in vitro and in vivo. J Immunol 2007;178: 1199-1207.
73. Harris JE, Fernandez-Vilaseca M, Elkington PT, Horncastle DE, Graeber MB, Friedland JS. IFNgamma synergizes with IL-1beta to upregulate MMP-9 secretion in a cellular model of central nervous system tuberculosis. FASEB J 2007;21: 356-365.
74. Wang S, Zhang C, Zhang M, Liang B, Zhu H, Lee J, Viollet B, Xia L, Zhang Y, Zou MH. Activation of AMP-Activated protein kinase a2 by nicotine instigates formation of abdominal aortic aneurysms in mice in vivo. Nat Med 2012;18: 902-910.
75. Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol 2011;13: 1016-1023.
76. 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.
77. Green JA, Tran CT, Farrar JJ, Nguyen MT, Nguyen PH, Dinh SX, Ho ND, Ly CV, Tran HT, Friedland JS, et al. Dexamethasone, cerebrospinal fluid matrix metalloproteinase concentrations and clinical outcomes in tuberculous meningitis. PLoS ONE 2009;4: e7277.
78. Simmons CP, Thwaites GE, Quyen NT, Chau TT, Mai PP, Dung NT, Stepniewska K, White NJ, Hien TT, Farrar J. The clinical benefit of adjunctive dexamethasone in tuberculous meningitis is not associated with measurable attenuation of peripheral or local immune responses. J Immunol 2005;175: 579-590.
79. Tobin DM, Roca FJ, Oh SF, McFarland R, Vickery TW, Ray JP, Ko DC, Zou Y, Bang ND, Chau TT, et al. Host genotype-specific therapies can optimize the inflammatory response to mycobacterial infections. Cell 2012;148: 434-446.
80. Wallis RS, Kyambadde P, Johnson JL, Horter L, Kittle R, Pohle M, Ducar C, Millard M, Mayanja-Kizza H, Whalen C, et al. A study of the safety, immunology, virology, and microbiology of adjunctive etanercept in HIV-1-Associated tuberculosis. AIDS 2004;18: 257-264.
81. Blackmore TK, Manning L, Taylor WJ, Wallis RS. Therapeutic use of infliximab in tuberculosis to control severe paradoxical reaction of the brain and lymph nodes. Clin Infect Dis 2008;47: e83-e85.
82. Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD, Siegel JN, Braun MM. Tuberculosis associated with infliximab, a tumor necrosis factor alpha-neutralizing agent. N Engl J Med 2001;345: 1098-1104.
83. Gapski R, Hasturk H, Van Dyke TE, Oringer RJ, Wang S, Braun TM, Giannobile WV. Systemic MMP inhibition for periodontal wound repair: results of a multi-centre randomized-controlled clinical trial. J Clin Periodontol 2009;36: 149-156.
84. Dalvi PS, Singh A, Trivedi HR, Ghanchi FD, Parmar DM, Mistry SD. Effect of doxycycline in patients of moderate to severe chronic obstructive pulmonary disease with stable symptoms. Ann Thorac Med 2011;6: 221-226.
85. Bhattacharyya P, Paul R, Bhattacharjee P, Ghosh A, Dey R, Ghosh M, Sharma M. Long-Term use of doxycycline can improve chronic asthma and possibly remodeling: the result of a pilot observation. J Asthma Allergy 2012;5: 33-37.
86. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295: 2387-2392.
87. Peterson JT. The importance of estimating the therapeutic index in the development of matrix metalloproteinase inhibitors. Cardiovasc Res 2006;69: 677-687.
88. Subbian S, Tsenova L, O'Brien P, Yang G, Koo MS, Peixoto B, Fallows D, Dartois V, Muller G, Kaplan G. Phosphodiesterase-4 inhibition alters gene expression and improves isoniazid-mediated clearance of Mycobacterium tuberculosis in rabbit lungs. PLoS Pathog 2011;7: e1002262.
89. 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.
90. Friedland JS, Shaw TC, Price NM, Dayer JM. Differential regulation of MMP-1/9 and TIMP-1 secretion in human monocytic cells in response to Mycobacterium tuberculosis. Matrix Biol 2002;21: 103-110.
91. Taylor JL, Ordway DJ, Troudt J, Gonzalez-Juarrero M, Basaraba RJ, Orme IM. Factors associated with severe granulomatous pneumonia in Mycobacterium tuberculosis-infected mice vaccinated therapeutically with hsp65 DNA. Infect Immun 2005;73: 5189-5193.
92. Harris JE, Green JA, Elkington PT, Friedland JS. Monocytes infected with Mycobacterium tuberculosis regulate MAP kinasedependent astrocyte MMP-9 secretion. J Leukoc Biol 2007;81: 548-556.
93. Price NM, Gilman RH, Uddin J, Recavarren S, Friedland JS. Unopposed matrix metalloproteinase-9 expression in human tuberculous granuloma and the role of TNF-Alpha-dependent monocyte networks. J Immunol 2003;171: 5579-5586.
94. Sheen P, O'Kane CM, Chaudhary K, Tovar M, Santillan C, Sosa J, Caviedes L, Gilman RH, Stamp G, Friedland JS. High MMP-9 activity characterises pleural tuberculosis correlating with granuloma formation. Eur Respir J 2009;33: 134-141.
95. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, Wilkinson KA, Banchereau R, Skinner J, Wilkinson RJ, et al. An interferoninducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature 2010;466: 973-977.
96. O'Kane CM, Elkington PT, Friedland JS. Monocyte-dependent oncostatin M and TNF-Alpha synergize to stimulate unopposed matrix metalloproteinase-1/3 secretion from human lung fibroblasts in tuberculosis. Eur J Immunol 2008;38: 1321-1330.
97. Parks WC, Wilson CL, Ló pez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004;4: 617-629.
98. Kähäri VM, Saarialho-Kere U. Matrix metalloproteinases in skin. Exp Dermatol 1997;6: 199-213.
99. Chandler S, Miller KM, Clements JM, Lury J, Corkill D, Anthony DC, Adams SE, Gearing AJ. Matrix metalloproteinases, tumor necrosis factor and multiple sclerosis: an overview. J Neuroimmunol 1997;72: 155-161.
100. Ashworth JL, Murphy G, Rock MJ, Sherratt MJ, Shapiro SD, Shuttleworth CA, Kielty CM. Fibrillin degradation by matrix metalloproteinases: implications for connective tissue remodelling. Biochem J 1999;340: 171-181.