Immune response and mortality risk relate to distinct lung microbiomes in patients with HIV and pneumonia

American Journal of Respiratory and Critical Care Medicine

Volumn 195, Issue 1, 2017, Pages 104-114

  Shenoy, Meera K ^a,b   Iwai, Shoko ^a   Lin, Din L ^a   Worodria, William ^c   Ayakaka, Irene ^c   Byanyima, Patrick ^c   Kaswabuli, Sylvia ^c   Fong, Serena ^d   Stone, Stephen ^d   Chang, Emily ^d   Lucian Davis, J ^e,f   Faruqi, Ali Ahmad ^a   Segal, Mark R ^g   Huang, Laurence ^d   Lynch, Susan V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Biomedical Sciences Graduate Program   (United States)

^c MAKERERE UNIVERSITY   (Uganda)

^d SAN FRANCISCO GENERAL HOSPITAL   (United States)

^e YALE UNIVERSITY   (United States)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

HIV; Immune response; Microbiota; Mortality; Pneumonia

Indexed keywords

CEFTRIAXONE; MEMBRANE PROTEIN; RNA 16S; T CELL IMMUNOGLOBULIN AND MUCIN DOMAIN 3 PROTEIN; UNCLASSIFIED DRUG;

AIRWAY; ANTIBIOTIC THERAPY; ARTICLE; ASPERGILLUS; BACTERIAL PNEUMONIA; BLOOD SAMPLING; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOSCOPY; CELLULAR IMMUNITY; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION PROFILING; GENE SEQUENCE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL PROCEDURES; LIQUID CHROMATOGRAPHY; LOWER RESPIRATORY TRACT; LUNG; LUNG LAVAGE; LUNG MYCOSIS; MAJOR CLINICAL STUDY; MALE; MASS FRAGMENTOGRAPHY; METABOLITE; METAGENOME; MICROBIAL COMMUNITY; MICROBIOLOGICAL EXAMINATION; MICROBIOME; MORTALITY RISK; MYCOBACTERIUM; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RNA EXTRACTION; SERUM; TH2 CELL; TREATMENT OUTCOME; UGANDAN; COMPLICATION; GENETICS; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; MIXED INFECTION; MORTALITY; RISK FACTOR;

BRONCHOALVEOLAR LAVAGE FLUID; COINFECTION; FEMALE; HIV INFECTIONS; HUMANS; LUNG; MALE; MICROBIOTA; PNEUMONIA, BACTERIAL; RISK FACTORS; RNA, RIBOSOMAL, 16S;

EID: 85008640881     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201603-0523OC     Document Type: Article

References (45)

1. World Health Organization. The gap report. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS; 2014.
2. World Health Organization. UNAIDS report on the global AIDS epidemic 2013. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS; 2013.
3. Badri M, Ehrlich R, Wood R, Pulerwitz T, Maartens G. Association between tuberculosis and HIV disease progression in a high tuberculosis prevalence area. Int J Tuberc Lung Dis 2001;5: 225-232.
4. Chaisson RE, Martinson NA. Tuberculosis in Africa: combating an HIV-driven crisis. N Engl J Med 2008;358:1089-1092.
5. French N, Gordon SB, Mwalukomo T, White SA, Mwafulirwa G, Longwe H, Mwaiponya M, Zijlstra EE, Molyneux ME, Gilks CF. A trial of a 7-valent pneumococcal conjugate vaccine in HIV-infected adults. N Engl J Med 2010;362:812-822.
6. Marshall CS, Curtis AJ, Spelman T, O'Brien DP, Greig J, Shanks L, du Cros P, Casas EC, da Fonseca MS, Athan E, et al. Impact of HIV-associated conditions on mortality in people commencing anti-retroviral therapy in resource limited settings. PLoS One 2013;8:e68445.
7. Twigg III HL, Knox KS, Zhou J, Crothers KA, Nelson DE, Toh E, Day RB, Lin H, Gao X, Dong Q, et al. Effect of advanced HIV infection on the respiratory microbiome. Am J Respir Crit Care Med 2016;194:226-235.
8. Flanagan JL, Brodie EL, Weng L, Lynch SV, Garcia O, Brown R, Hugenholtz P, DeSantis TZ, Andersen GL, Wiener-Kronish JP, et al. Loss of bacterial diversity during antibiotic treatment of intubated patients colonized with Pseudomonas aeruginosa. J Clin Microbiol 2007;45:1954-1962.
9. Iwai S, Huang D, Fong S, Jarlsberg LG, Worodria W, Yoo S, Cattamanchi A, Davis JL, Kaswabuli S, Segal M, et al. The lung microbiome of Ugandan HIV-infected pneumonia patients is compositionally and functionally distinct from that of San Franciscan patients. PLoS One 2014;9:e95726.
10. Shenoy M, Iwai S, Lin D, Worodria W, Ayakaka I, Byanyima P, Kaswabuli S, Fong S, Stone SA, Chang E, et al. Functionally and immunologically distinct lung microbiomes of HIV-infected pneumonia patients are significantly related to mortality outcomes [abstract]. Am J Respir Crit Care Med 2015;191:A4699.
11. Iwai S, Fei M, Huang D, Fong S, Subramanian A, Grieco K, Lynch SV, Huang L. Oral and airway microbiota in HIV-infected pneumonia patients. J Clin Microbiol 2012;50:2995-3002.
12. Magoc T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 2011;27: 2957-2963.
13. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, FiererN, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010;7:335-336.
14. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, et al.; Human Microbiome Consortium. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 2011;21:494-504.
15. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing;2008.
16. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006;72:5069-5072.
17. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008;3:1101-1108.
18. Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience 2013;2:16.
19. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 2013;31:814-821.
20. Bray JR, Curtis JT. An ordination of upland forest communities of southern Wisconsin. Ecol Monogr 1957;27:325-349.
21. Holmes I, Harris K, Quince C. Dirichlet multinomial mixtures: generative models for microbial metagenomics. PLoS One 2012; 7:e30126.
22. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol 2001;26:32-46.
23. Lozupone C, Hamady M, Knight R. UniFrac: an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics 2006;7:371.
24. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005;71: 8228-8235.
25. Rutherford ST, Bassler BL. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harb Perspect Med 2012;2:a012427.
26. Antonic V, Stojadinovic A, Zhang B, Izadjoo MJ, Alavi M. Pseudomonas aeruginosa induces pigment production and enhances virulence in a white phenotypic variant of Staphylococcus aureus. Infect Drug Resist 2013;6:175-186.
27. Kanehisa M, Goto S. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 2000;28:27-30.
28. Kanehisa M, Goto S, Sato Y, Kawashima M, Furumichi M, Tanabe M. Data, information, knowledge and principle: back to metabolism in KEGG. Nucleic Acids Res 2014;42: D199-D205.
29. Rahman AN, Clayton K, Mujib S, Fong IW, Ostrowski MA. TIM-3 and its immunoregulatory role in HIV infection. J Clin Cell Immunol 2012; S7:007.
30. Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, Long BR, Wong JC, Satkunarajah M, Schweneker M, Chapman JM, et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 2008;205:2763-2779.
31. Golden-Mason L, Palmer BE, Kassam N, Townshend-Bulson L, Livingston S, McMahon BJ, Castelblanco N, Kuchroo V, Gretch DR, Rosen HR. Negative immune regulator Tim-3 is overexpressed on T cells in hepatitis C virus infection and its blockade rescues dysfunctional CD4+ and CD8+ T cells. J Virol 2009;83: 9122-9130.
32. Muller S, Radic M. Citrullinated autoantigens: from diagnostic markers to pathogenetic mechanisms. Clin Rev Allergy Immunol 2015;49: 232-239.
33. Cha L, Berry CM, Nolan D, Castley A, Fernandez S, French MA. Interferon-alpha, immune activation and immune dysfunction in treated HIV infection. Clin Transl Immunology 2014; 3:e10.
34. Burhop KE, Selig WM, Malik AB. Monohydroxyeicosatetraenoic acids (5-HETE and 15-HETE) induce pulmonary vasoconstriction and edema. Circ Res 1988;62:687-698.
35. Mobraten K, Haugbro T, Karlstrom E, Kleiveland CR, Lea T. Activation of the bile acid receptor TGR5 enhances LPS-induced inflammatory responses in a human monocytic cell line. J Recept Signal Transduct Res 2015;35:402-409.
36. Gower JC. Generalized procrustes analysis. Psychometrika 1975;40: 33-51.
37. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res 1967;27:209-220.
38. Cribbs SK, Uppal K, Li S, Jones DP, Huang L, Tipton L, Fitch A, Greenblatt RM, Kingsley L, Guidot DM, et al. Correlation of the lung microbiota with metabolic profiles in bronchoalveolar lavage fluid in HIV infection. Microbiome 2016;4:3.
39. Segal LN, Clemente JC, Tsay J-CJ, Koralov SB, Keller BC, Wu BG, Li Y, Shen N, Ghedin E, Morris A, et al. Enrichment of the lung microbiome with oral taxa is associated with lung inflammation of a Th17 phenotype. Nature Microbiology 2016;1: 16031.
40. Kolwijck E, van de Veerdonk FL. The potential impact of the pulmonary microbiome on immunopathogenesis of Aspergillus-related lung disease. Eur J Immunol 2014;44:3156-3165.
41. Cui L, Lucht L, Tipton L, Rogers MB, Fitch A, Kessinger C, Camp D, Kingsley L, Leo N, Greenblatt RM, et al. Topographic diversity of the respiratory tract mycobiome and alteration in HIV and lung disease. Am J Respir Crit Care Med 2015;191:932-942.
42. Homma T, Kato A, Bhushan B, Norton JE, Suh LA, Carter RG, Gupta DS, Schleimer RP. Role of Aspergillus fumigatus in triggering protease-activated receptor-2 in airway epithelial cells and skewing the cells toward a T-helper 2 bias. Am J Respir Cell Mol Biol 2015; 54:60-70.
43. Urb M, Snarr BD, Wojewodka G, Lehoux M, Lee MJ, Ralph B, Divangahi M, King IL, McGovern TK, Martin JG, et al. Evolution of the immune response to chronic airway colonization with Aspergillus fumigatus hyphae. Infect Immun 2015;83:3590-3600.
44. Sada-Ovalle I, Chávez-Galán L, Torre-Bouscoulet L, Nava-Gamiño L, Barrera L, Jayaraman P, Torres-Rojas M, Salazar-Lezama MA, Behar SM. The Tim3-galectin 9 pathway induces antibacterial activity in human macrophages infected with Mycobacterium tuberculosis. J Immunol 2012;189: 5896-5902.
45. Kilsgard O, Andersson P, Malmsten M, Nordin SL, Linge HM, Eliasson M, Sorenson E, Erjefalt JS, Bylund J, Olin AI, et al. Peptidylarginine deiminases present in the airways during tobacco smoking and inflammation can citrullinate the host defense peptide LL-37, resulting in altered activities. Am J Respir Cell Mol Biol 2012;46: 240-248.