Matrix Metalloproteinases in Tuberculosis-Immune Reconstitution Inflammatory Syndrome and Impaired Lung Function Among Advanced HIV/TB Co-infected Patients Initiating Antiretroviral Therapy

EBioMedicine

Volumn 3, Issue , 2016, Pages 100-107

  Ravimohan, Shruthi ^a,c   Tamuhla, Neo ^c   Kung, Shiang Ju ^d,e   Nfanyana, Kebatshabile ^c   Steenhoff, Andrew P ^b,c,d   Gross, Robert ^a,b,c   Weissman, Drew ^a,c   Bisson, Gregory P ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c BOTSWANA UPENN PARTNERSHIP   (Botswana)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^e UNIVERSITY OF BOTSWANA   (Botswana)

Author keywords

ART; HIV; Immune recovery; Lung function; Matrix metalloproteinases; TB IRIS

Indexed keywords

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; NEUTROPHIL COLLAGENASE; STROMELYSIN;

ADULT; ARTICLE; BLOOD SAMPLING; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FORCED EXPIRATORY VOLUME; FORCED EXPIRATORY VOLUME FORCED VITAL CAPACITY RATIO; FORCED VITAL CAPACITY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNE RESPONSE; LUNG DISEASE; LUNG FUNCTION TEST; MALE; MIXED INFECTION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROSPECTIVE STUDY; RESPIRATORY TRACT PARAMETERS; TUBERCULOSIS; VIRUS LOAD; CASE CONTROL STUDY; CELLULAR IMMUNITY; COMPLICATION; HIV INFECTIONS; IMMUNOLOGY; LUNG TUBERCULOSIS; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION;

ADULT; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; CASE-CONTROL STUDIES; COINFECTION; FEMALE; HIV INFECTIONS; HUMANS; IMMUNE RECONSTITUTION INFLAMMATORY SYNDROME; IMMUNITY, CELLULAR; MALE; MATRIX METALLOPROTEINASES; MIDDLE AGED; RESPIRATORY FUNCTION TESTS; T-LYMPHOCYTE SUBSETS; TUBERCULOSIS, PULMONARY;

EID: 84958922114     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.11.040     Document Type: Article

References (51)

1. Pasipanodya J.G., McNabb S.J., Hilsenrath P., et al. Pulmonary impairment after tuberculosis and its contribution to TB burden. BMC Public Health 2010, 10:259.
2. Hnizdo E., Singh T., Churchyard G. Chronic pulmonary function impairment caused by initial and recurrent pulmonary tuberculosis following treatment. Thorax 2000, 55:32-38.
3. Ralph A.P., Kenangalem E., Waramori G., et al. High morbidity during treatment and residual pulmonary disability in pulmonary tuberculosis: under-recognised phenomena. PLoS One 2013, 8.
4. Van Zyl Smit R.N., Pai M., Yew W.W., et al. Global lung health: the colliding epidemics of tuberculosis, tobacco smoking, HIV and COPD. Eur. Respir. J. 2010, 35:27-33.
5. World Health Organization WHO. Global Tuberculosis Report 2014 (Available: Accessed Dec 15, 2014). http://www.who.int/tb/publications/global_report/gtbr14_executive_summary.pdf?ua=1.
6. Plit M.L., Anderson R., Van Rensburg C.E., et al. Influence of antimicrobial chemotherapy on spirometric parameters and pro-inflammatory indices in severe pulmonary tuberculosis. Eur. Respir. J. 1998, 12:351-356.
7. Kwan C.K., Ernst J.D. HIV and tuberculosis: a deadly human syndemic. Clin. Microbiol. Rev. 2011, 24:351-376.
8. Post F.A., Wood R., Pillay G.P. Pulmonary tuberculosis in HIV infection: radiographic appearance is related to CD4+ T-lymphocyte count. Tuber. Lung Dis. 1995, 76:518-521.
9. Flynn J.L., Chan J., Triebold K.J., Dalton D.K., Stewart T.A., Bloom B.R. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993, 178:2249-2254.
10. Schluger N.W., Perez D., Liu Y.M. Reconstitution of immune responses to tuberculosis in patients with HIV infection who receive antiretroviral therapy. Chest 2002, 122:597-602.
11. Greenlee K.J., Werb Z., Kheradmand F. Matrix metalloproteinases in lung: multiple, multifarious, and multifaceted. Physiol. Rev. 2007, 87:69-98.
12. Ong C.W., Elkington P.T., Friedland J.S. Tuberculosis, pulmonary cavitation, and matrix metalloproteinases. Am. J. Respir. Crit. Care Med. 2014, 190:9-18.
13. Elkington P., Shiomi T., Breen R., et al. MMP-1 drives immunopathology in human tuberculosis and transgenic mice. J. Clin. Invest. 2011, 121:1827-1833.
14. Walker N.F., Clark S.O., Oni T., et al. Doxycycline and HIV infection suppress tuberculosis-induced matrix metalloproteinases. Am. J. Respir. Crit. Care Med. 2012, 185:989-997.
15. Abdool Karim S.S., Naidoo K., Grobler A., et al. Integration of antiretroviral therapy with tuberculosis treatment. N. Engl. J. Med. 2011, 365:1492-1501.
16. Abdool Karim S.S., Naidoo K., Grobler A., et al. Timing of initiation of antiretroviral drugs during tuberculosis therapy. N. Engl. J. Med. 2010, 362:697-706.
17. George M.P., Kannass M., Huang L., Sciurba F.C., Morris A. Respiratory symptoms and airway obstruction in HIV-infected subjects in the HAART era. PLoS One 2009, 4.
18. Meintjes G., Lawn S.D., Scano F., et al. Tuberculosis-associated immune reconstitution inflammatory syndrome: case definitions for use in resource-limited settings. Lancet Infect. Dis. 2008, 8:516-523.
19. Lawn S.D., Wainwright H., Orrell C. Fatal unmasking tuberculosis immune reconstitution disease with bronchiolitis obliterans organizing pneumonia: the role of macrophages. AIDS 2009, 23:143-145.
20. Tadokera R., Meintjes G.A., Wilkinson K.A., et al. Matrix metalloproteinases and tissue damage in HIV-tuberculosis immune reconstitution inflammatory syndrome. Eur. J. Immunol. 2014, 44:127-136.
21. Ravimohan S., Tamuhla N., Steenhoff A.P., et al. Early immunologic failure is associated with early mortality among advanced HIV-infected adults initiating antiretroviral therapy with active tuberculosis. J. Infect. Dis. 2013, 208:1784-1793.
22. Ravimohan S., Tamuhla N., Steenhoff A.P., et al. Immunological profiling of tuberculosis-associated immune reconstitution inflammatory syndrome and non-immune reconstitution inflammatory syndrome death in HIV-infected adults with pulmonary tuberculosis starting antiretroviral therapy: a prospective observational cohort study. Lancet Infect. Dis. 2015, 15:p429-p438.
23. Elkington P.T., Emerson J.E., Lopez-Pascua L.D., et al. Mycobacterium tuberculosis up-regulates matrix metalloproteinase-1 secretion from human airway epithelial cells via a p38 MAPK switch. J. Immunol. 2005, 175:5333-5340.
24. Elkington P.T., Friedland J.S. Matrix metalloproteinases in destructive pulmonary pathology. Thorax 2006, 61:259-266.
25. Ong C.W., Elkington P.T., Brilha S., et al. Neutrophil-derived MMP-8 drives AMPK-dependent matrix destruction in human pulmonary tuberculosis. PLoS Pathog. 2015, 11.
26. Ravimohan S., Tamuhla N., Nfanyana K., et al. Robust reconstitution of TB-specific polyfunctional CD4+ T-cell responses and rising systemic IL-6 in paradoxical TB-IRIS. Clinical infectious diseases : an official publicationof the Infectious Diseases Society of America 2015, 10.1093/cid/civ978.
27. Grant P.M., Komarow L., Andersen J., et al. Risk factor analyses for immune reconstitution inflammatory syndrome in a randomized study of early vs. deferred ART during an opportunistic infection. PloS one 2010, 5.
28. American Thoracic Society Standardization of spirometry, 1994 update. Am. J. Respir. Crit. Care Med. 1995, 152:1107-1136.
29. American Thoracic Society Lung function testing: selection of reference values and interpretative strategies. Am. Rev. Respir. Dis. 1991, 144:1202-1218.
30. Pellegrino R., Viegi G., Brusasco V., et al. Interpretative strategies for lung function tests. Eur. Respir. J. 2005, 26:948-968.
31. Quanjer P.H., Tammeling G.J., Cotes J.E., et al. Lung volumes and forced ventilatory flows. Report working party standardization of lung function tests, European Community for Steel and Coal. Official Statement of the European Respiratory Society. Eur. Respir. J. Suppl. 1993, 16:5-40.
32. White N., Ehrlich R., Rees D. A guide to spirometry as applied to occupational health. S. Afr. Med. J. 1996, 86:807-813.
33. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser 1995, B 57:289-300.
34. Salgame P. MMPs in tuberculosis: granuloma creators and tissue destroyers. J. Clin. Invest. 2011, 121:1686-1688.
35. Dutta N.K., Karakousis P.C. Latent tuberculosis infection: myths, models, and molecular mechanisms. Microbiol. Mol. Biol. Rev. 2014, 78:343-371.
36. Naidoo K., Yende-Zuma N., Padayatchi N., et al. The immune reconstitution inflammatory syndrome after antiretroviral therapy initiation in patients with tuberculosis: findings from the SAPiT trial. Ann. Intern. Med. 2012, 157:313-324.
37. Luetkemeyer A.F., Kendall M.A., Nyirenda M., et al. Tuberculosis immune reconstitution inflammatory syndrome in A5221 STRIDE: timing, severity, and implications for HIV-TB programs. J. Acquir. Immune Defic. Syndr. 2014, 65:423-428.
38. Hoheisel G., Sack U., Hui D.S., et al. Occurrence of matrix metalloproteinases and tissue inhibitors of metalloproteinases in tuberculous pleuritis. Tuberculosis (Edinb.) 2001, 81:203-209.
39. Singh S., Kubler A., Singh U.K., et al. Antimycobacterial drugs modulate immunopathogenic matrix metalloproteinases in a cellular model of pulmonary tuberculosis. Antimicrob. Agents Chemother. 2014, 58:4657-4665.
40. Hasty K.A., Hibbs M.S., Kang A.H., Mainardi C.L. Secreted forms of human neutrophil collagenase. J. Biol. Chem. 1986, 261:5645-5650.
41. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 2004, 4:617-629.
42. Ugarte-Gil C.A., Elkington P., Gilman R.H., et al. Induced sputum MMP-1, -3 & -8 concentrations during treatment of tuberculosis. PLoS One 2013, 8.
43. Barber D.L., Mayer-Barber K.D., Antonelli L.R., et al. Th1-driven immune reconstitution disease in Mycobacterium avium-infected mice. Blood 2010, 116:3485-3493.
44. Marais S., Wilkinson K.A., Lesosky M., et al. Neutrophil-associated central nervous system inflammation in tuberculous meningitis immune reconstitution inflammatory syndrome. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America 2014, 59:1638-1647.
45. Zhang M., Gong J., Iyer D.V., et al. T cell cytokine responses in persons with tuberculosis and human immunodeficiency virus infection. J. Clin. Invest. 1994, 94:2435-2442.
46. Law K.F., Jagirdar J., Weiden M.D., et al. Tuberculosis in HIV-positive patients: cellular response and immune activation in the lung. Am. J. Respir. Crit. Care Med. 1996, 153:1377-1384.
47. Eum S.Y., Kong J.H., Hong M.S., et al. Neutrophils are the predominant infected phagocytic cells in the airways of patients with active pulmonary TB. Chest 2010, 137:122-128.
48. Appelberg R. CD4+ T cells are required for antigen-specific recruitment of neutrophils by BCG-immune spleen cells. Immunology 1992, 75:414-419.
49. Zhang J.H., Ferrante A., Arrigo A.P., Dayer J.M. Neutrophil stimulation and priming by direct contact with activated human T lymphocytes. J. Immunol. 1992, 148:177-181.
50. Marais S., Meintjes G., Pepper D.J., et al. Frequency, severity, and prediction of tuberculous meningitis immune reconstitution inflammatory syndrome. Clinical infectious diseases: An Official Publication of the Infectious Diseases Society of America 2013, 56:450-460.
51. Weiss S.J., Peppin G., Ortiz X., et al. Oxidative autoactivation of latent collagenase by human neutrophils. Science 1985, 227:747-749.