Neutrophil-Derived MMP-8 Drives AMPK-Dependent Matrix Destruction in Human Pulmonary Tuberculosis

PLoS Pathogens

Volumn 11, Issue 5, 2015, Pages

  Ong, Catherine W M ^a,b   Elkington, Paul T ^a,c   Brilha, Sara ^a   Ugarte Gil, Cesar ^a,d   Tome Esteban, Maite T ^e   Tezera, Liku B ^a,c   Pabisiak, Przemyslaw J ^a   Moores, Rachel C ^a   Sathyamoorthy, Tarangini ^a   Patel, Vimal ^e   Gilman, Robert H ^f,g   Porter, Joanna C ^h   Friedland, Jon S ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b Dept Medicine Endocrinol Diabet   (Singapore)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^d INSTITUTO DE MEDICINA TROPICAL ALEXANDER VON HUMBOLDT   (Peru)

^e UNIVERSITY COLLEGE LONDON HOSPITALS   (United Kingdom)

^f JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^g UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

^h UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1; GELATIN; GELATINASE B; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MYELOPEROXIDASE; NEUTROPHIL COLLAGENASE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; PHOSPHOTRANSFERASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; ENZYME INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MMP8 PROTEIN, HUMAN; SCLEROPROTEIN;

ADULT; ANATOMICAL CONCEPTS; ARTICLE; CELL CULTURE; CELL STIMULATION; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTRACELLULAR TRAP; FLOW CYTOMETRY; HUMAN; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; LUNG BIOPSY; LUNG TUBERCULOSIS; MAJOR CLINICAL STUDY; MATRIX DESTRUCTION; NEUTROPHIL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; ACTIVE TRANSPORT; CHEMISTRY; COHORT ANALYSIS; DRUG EFFECTS; ENZYMOLOGY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; LUNG; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING; RESPIRATORY MUCOSA; SECRETION (PROCESS); SPUTUM; TUBERCULOSIS, PULMONARY;

MYCOBACTERIUM TUBERCULOSIS;

ACTIVE TRANSPORT, CELL NUCLEUS; ADULT; AMP-ACTIVATED PROTEIN KINASES; CELLS, CULTURED; COHORT STUDIES; ENZYME INHIBITORS; EXTRACELLULAR MATRIX PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; LUNG; MATRIX METALLOPROTEINASE 8; MYCOBACTERIUM TUBERCULOSIS; NEUTROPHIL INFILTRATION; NEUTROPHILS; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RESPIRATORY MUCOSA; SPUTUM; TUBERCULOSIS, PULMONARY;

EID: 84930349477     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004917     Document Type: Article

References (63)

1. Eum SY, Kong JH, Hong MS, Lee YJ, Kim JH, Hwang SH, et al. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest. 2010 Jan;137(1):122–8. doi: 10.1378/chest.09-0903 19749004
2. Nouailles G, Dorhoi A, Koch M, Zerrahn J, Weiner J, 3rd, Fae KC, et al. CXCL5-secreting pulmonary epithelial cells drive destructive neutrophilic inflammation in tuberculosis. J Clin Invest. 2014 Feb 10.
3. Harding MG, Zhang K, Conly J, Kubes P, Neutrophil Crawling in Capillaries; A Novel Immune Response to Staphylococcus aureus. PLoS Pathog. 2014 Oct;10(10):e1004379. doi: 10.1371/journal.ppat.1004379 25299673
4. Mantovani A, Cassatella MA, Costantini C, Jaillon S, Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011 Aug;11(8):519–31. doi: 10.1038/nri3024 21785456
5. Parks WC, Wilson CL, Lopez-Boado YS, Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol. 2004 Aug;4(8):617–29. 15286728
6. Nagase H, Visse R, Murphy G, Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006 Feb 15;69(3):562–73. 16405877
7. Ong CW, Elkington PT, Friedland JS, Tuberculosis, pulmonary cavitation, and matrix metalloproteinases. Am J Respir Crit Care Med. 2014 Jul 1;190(1):9–18. doi: 10.1164/rccm.201311-2106PP 24713029
8. 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 Jan 22;327(5964):466–9. doi: 10.1126/science.1179663 20007864
9. Elkington P, Shiomi T, Breen R, Nuttall RK, Ugarte-Gil CA, Walker NF, et al. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J Clin Invest. 2011 May;121(5):1827–33. doi: 10.1172/JCI45666 21519144
10. Walker NF, Clark SO, Oni T, Andreu N, Tezera L, Singh S, et al. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am J Respir Crit Care Med. 2012 May 1;185(9):989–97. doi: 10.1164/rccm.201110-1769OC 22345579
11. 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 Mar 15;166(6):4223–30. 11238675
12. Green JA, Tran CT, Farrar JJ, Nguyen MT, Nguyen PH, Dinh SX, et al. Dexamethasone, cerebrospinal fluid matrix metalloproteinase concentrations and clinical outcomes in tuberculous meningitis. PLoS One. 2009;4(9):e7277. doi: 10.1371/journal.pone.0007277 19789647
13. O'Neill LA, Hardie DG, Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature. 2013 Jan 17;493(7432):346–55. doi: 10.1038/nature11862 23325217
14. Finlay D, Cantrell DA, Metabolism, migration and memory in cytotoxic T cells. Nat Rev Immunol. 2011 Feb;11(2):109–17. doi: 10.1038/nri2888 21233853
15. Chan O, Burke JD, Gao DF, Fish EN, The chemokine CCL5 regulates glucose uptake and AMP kinase signaling in activated T cells to facilitate chemotaxis. J Biol Chem. 2012 Aug 24;287(35):29406–16. doi: 10.1074/jbc.M112.348946 22782897
16. Pan H, Yan BS, Rojas M, Shebzukhov YV, Zhou H, Kobzik L, et al. Ipr1 gene mediates innate immunity to tuberculosis. Nature. 2005 Apr 7;434(7034):767–72. 15815631
17. Calderon VE, Valbuena G, Goez Y, Judy BM, Huante MB, Sutjita P, et al. A humanized mouse model of tuberculosis. PLoS One. 2013;8(5):e63331. doi: 10.1371/journal.pone.0063331 23691024
18. Al Shammari B, Shiomi T, Tezera L, Bielecka MK, Workman V, Sathyamoorthy T, et al. The extracellular matrix regulates granuloma necrosis in tuberculosis. J Infect Dis. 2015 Feb 12.
19. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM, Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med. 1993 Dec 1;178(6):2243–7. 8245795
20. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR, An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med. 1993 Dec 1;178(6):2249–54. 7504064
21. Mohan VP, Scanga CA, Yu K, Scott HM, Tanaka KE, Tsang E, et al. Effects of tumor necrosis factor alpha on host immune response in chronic persistent tuberculosis: possible role for limiting pathology. Infect Immun. 2001 Mar;69(3):1847–55. 11179363
22. Davey MS, Tamassia N, Rossato M, Bazzoni F, Calzetti F, Bruderek K, et al. Failure to detect production of IL-10 by activated human neutrophils. Nat Immunol. 2011 Nov;12(11):1017–8; author reply 8–20. doi: 10.1038/ni.2111 22012430
23. Risso A, Leukocyte antimicrobial peptides: multifunctional effector molecules of innate immunity. J Leukoc Biol. 2000 Dec;68(6):785–92. 11129645
24. Condliffe AM, Davidson K, Anderson KE, Ellson CD, Crabbe T, Okkenhaug K, et al. Sequential activation of class IB and class IA PI3K is important for the primed respiratory burst of human but not murine neutrophils. Blood. 2005 Aug 15;106(4):1432–40. 15878979
25. Price B, Dennison C, Tschesche H, Elliott E, Neutrophil tissue inhibitor of matrix metalloproteinases-1 occurs in novel vesicles that do not fuse with the phagosome. J Biol Chem. 2000 Sep 8;275(36):28308–15. 10869345
26. Cuadrado E, Ortega L, Hernandez-Guillamon M, Penalba A, Fernandez-Cadenas I, Rosell A, et al. Tissue plasminogen activator (t-PA) promotes neutrophil degranulation and MMP-9 release. J Leukoc Biol. 2008 Jul;84(1):207–14. doi: 10.1189/jlb.0907606 18390930
27. Natarajan K, Singh S, Burke TR, Jr.Grunberger D, Aggarwal BB, Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9090–5. 8799159
28. Ward C, Chilvers ER, Lawson MF, Pryde JG, Fujihara S, Farrow SN, et al. NF-kappaB activation is a critical regulator of human granulocyte apoptosis in vitro. J Biol Chem. 1999 Feb 12;274(7):4309–18. 9933632
29. Kang DD, Lin Y, Moreno JR, Randall TD, Khader SA, Profiling early lung immune responses in the mouse model of tuberculosis. PLoS One. 2011;6(1):e16161. doi: 10.1371/journal.pone.0016161 21249199
30. Soehnlein O, Zernecke A, Eriksson EE, Rothfuchs AG, Pham CT, Herwald H, et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008 Aug 15;112(4):1461–71. doi: 10.1182/blood-2008-02-139634 18490516
31. Seyer JM, Hutcheson ET, Kang AH, Collagen polymorphism in idiopathic chronic pulmonary fibrosis. J Clin Invest. 1976 Jun;57(6):1498–507. 777026
32. Gapski R, Hasturk H, Van Dyke TE, Oringer RJ, Wang S, Braun TM, et al. Systemic MMP inhibition for periodontal wound repair: results of a multi-centre randomized-controlled clinical trial. J Clin Periodontol. 2009 Feb;36(2):149–56. doi: 10.1111/j.1600-051X.2008.01351.x 19207891
33. Ugarte-Gil CA, Elkington P, Gilman RH, Coronel J, Tezera LB, Bernabe-Ortiz A, et al. Induced Sputum MMP-1, -3 & -8 Concentrations during Treatment of Tuberculosis. PLoS One. 2013;8(4):e61333. doi: 10.1371/journal.pone.0061333 23613834
34. Neeli I, Radic M, Knotting the NETs: analyzing histone modifications in neutrophil extracellular traps. Arthritis Res Ther. 2012;14(2):115. doi: 10.1186/ar3773 22524286
35. Brill A, Fuchs TA, Savchenko AS, Thomas GM, Martinod K, De Meyer SF, et al. Neutrophil extracellular traps promote deep vein thrombosis in mice. J Thromb Haemost. 2012 Jan;10(1):136–44. doi: 10.1111/j.1538-7836.2011.04544.x 22044575
36. Alfakry H, Sinisalo J, Paju S, Nieminen MS, Valtonen V, Tervahartiala T, et al. The association of serum neutrophil markers and acute coronary syndrome. Scand J Immunol. 2012 Aug;76(2):181–7. doi: 10.1111/j.1365-3083.2012.02718.x 22537345
37. Carlson M, Raab Y, Seveus L, Xu S, Hallgren R, Venge P, Human neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis. Gut. 2002 Apr;50(4):501–6. 11889070
38. Ramos-DeSimone N, Moll UM, Quigley JP, French DL, Inhibition of matrix metalloproteinase 9 activation by a specific monoclonal antibody. Hybridoma. 1993 Aug;12(4):349–63. 8244415
39. Berry MP, Graham CM, McNab FW, Xu Z, Bloch SA, Oni T, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010 Aug 19;466(7309):973–7. doi: 10.1038/nature09247 20725040
40. Danelishvili L, McGarvey J, Li YJ, Bermudez LE, Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in human macrophages and alveolar epithelial cells. Cell Microbiol. 2003 Sep;5(9):649–60. 12925134
41. Karim AF, Chandra P, Chopra A, Siddiqui Z, Bhaskar A, Singh A, et al. Express path analysis identifies a tyrosine kinase Src-centric network regulating divergent host responses to Mycobacterium tuberculosis infection. J Biol Chem. 2011 Nov 18;286(46):40307–19. doi: 10.1074/jbc.M111.266239 21953458
42. Hahn-Windgassen A, Nogueira V, Chen CC, Skeen JE, Sonenberg N, Hay N, Akt activates the mammalian target of rapamycin by regulating cellular ATP level and AMPK activity. J Biol Chem. 2005 Sep 16;280(37):32081–9. 16027121
43. Zou MH, Hou XY, Shi CM, Kirkpatick S, Liu F, Goldman MH, et al. Activation of 5'-AMP-activated kinase is mediated through c-Src and phosphoinositide 3-kinase activity during hypoxia-reoxygenation of bovine aortic endothelial cells. Role of peroxynitrite. J Biol Chem. 2003 Sep 5;278(36):34003–10. 12824177
44. Singh S, Saraiva L, Elkington PT, Friedland JS. Regulation of matrix metalloproteinase-1, -3, and -9 in Mycobacterium tuberculosis-dependent respiratory networks by the rapamycin-sensitive PI3K/p70S6K cascade. FASEB J. 2013 Oct 4.
45. Hardie DG, Ross FA, Hawley SA, AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol. 2012 Apr;13(4):251–62. doi: 10.1038/nrm3311 22436748
46. Kodiha M, Rassi JG, Brown CM, Stochaj U, Localization of AMP kinase is regulated by stress, cell density, and signaling through the MEK—>ERK1/2 pathway. Am J Physiol Cell Physiol. 2007 Nov;293(5):C1427–36. 17728396
47. Arad M, Seidman CE, Seidman JG, AMP-activated protein kinase in the heart: role during health and disease. Circ Res. 2007 Mar 2;100(4):474–88. 17332438
48. Scott JW, Hawley SA, Green KA, Anis M, Stewart G, Scullion GA, et al. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest. 2004 Jan;113(2):274–84. 14722619
49. Condos R, Rom WN, Liu YM, Schluger NW, Local immune responses correlate with presentation and outcome in tuberculosis. Am J Respir Crit Care Med. 1998 Mar;157(3 Pt 1):729–35. 9517583
50. Sathyamoorthy T, Sandhu G, Tezera LB, Thomas R, Singhania A, Woelk CH, et al. Gender-dependent differences in plasma matrix metalloproteinase-8 elevated in pulmonary tuberculosis. PLoS One. 2015;10(1):e0117605. doi: 10.1371/journal.pone.0117605 25635689
51. Desvignes L, Ernst JD, Interferon-gamma-responsive nonhematopoietic cells regulate the immune response to Mycobacterium tuberculosis. Immunity. 2009 Dec 18;31(6):974–85. doi: 10.1016/j.immuni.2009.10.007 20064452
52. Nandi B, Behar SM, Regulation of neutrophils by interferon-gamma limits lung inflammation during tuberculosis infection. J Exp Med. 2011 Oct 24;208(11):2251–62. doi: 10.1084/jem.20110919 21967766
53. Kozakiewicz L, Chen Y, Xu J, Wang Y, Dunussi-Joannopoulos K, Ou Q, et al. B cells regulate neutrophilia during Mycobacterium tuberculosis infection and BCG vaccination by modulating the interleukin-17 response. PLoS Pathog. 2013;9(7):e1003472. doi: 10.1371/journal.ppat.1003472 23853593
54. Xu J, Zhang X, Pelayo R, Monestier M, Ammollo CT, Semeraro F, et al. Extracellular histones are major mediators of death in sepsis. Nat Med. 2009 Nov;15(11):1318–21. doi: 10.1038/nm.2053 19855397
55. Saffarzadeh M, Juenemann C, Queisser MA, Lochnit G, Barreto G, Galuska SP, et al. Neutrophil extracellular traps directly induce epithelial and endothelial cell death: a predominant role of histones. PLoS One. 2012;7(2):e32366. doi: 10.1371/journal.pone.0032366 22389696
56. Graham SA, Antonopoulos A, Hitchen PG, Haslam SM, Dell A, Drickamer K, et al. Identification of neutrophil granule glycoproteins as Lewis(x)-containing ligands cleared by the scavenger receptor C-type lectin. J Biol Chem. 2011 Jul 8;286(27):24336–49. doi: 10.1074/jbc.M111.244772 21561871
57. 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 Mar;117(3):684–94. 10712992
58. Albaiceta GM, Gutierrez-Fernandez A, Garcia-Prieto E, Puente XS, Parra D, Astudillo A, et al. Absence or inhibition of matrix metalloproteinase-8 decreases ventilator-induced lung injury. Am J Respir Cell Mol Biol. 2010 Nov;43(5):555–63. doi: 10.1165/rcmb.2009-0034OC 19995943
59. Guo L, Stripay JL, Zhang X, Collage RD, Hulver M, Carchman EH, et al. CaMKIalpha regulates AMP kinase-dependent, TORC-1-independent autophagy during lipopolysaccharide-induced acute lung neutrophilic inflammation. J Immunol. 2013 Apr 1;190(7):3620–8. doi: 10.4049/jimmunol.1102975 23447692
60. Hoogendijk AJ, Pinhancos SS, van der Poll T, Wieland CW, AMP-activated protein kinase activation by 5-aminoimidazole-4-carbox-amide-1-beta-D-ribofuranoside (AICAR) reduces lipoteichoic acid-induced lung inflammation. J Biol Chem. 2013 Mar 8;288(10):7047–52. doi: 10.1074/jbc.M112.413138 23322781
61. Wang S, Zhang C, Zhang M, Liang B, Zhu H, Lee J, et al. Activation of AMP-activated protein kinase alpha2 by nicotine instigates formation of abdominal aortic aneurysms in mice in vivo. Nat Med. 2012 Jun;18(6):902–10. doi: 10.1038/nm.2711 22561688
62. Mihaylova MM, Shaw RJ, The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 2011 Sep;13(9):1016–23. doi: 10.1038/ncb2329 21892142
63. Wejse C, Gustafson P, Nielsen J, Gomes VF, Aaby P, Andersen PL, et al. TBscore: Signs and symptoms from tuberculosis patients in a low-resource setting have predictive value and may be used to assess clinical course. Scand J Infect Dis. 2008;40(2):111–20. 17852907