Altered metabolism of gut microbiota contributes to chronic immune activation in HIV-infected individuals

Mucosal Immunology

Volumn 8, Issue 4, 2015, Pages 760-772

  Vazquez Castellanos J F ^a,b   Serrano Villar, S ^c   Latorre, A ^a,b   Artacho, A ^a   Ferrus M L ^a   Madrid, N ^c   Vallejo, A ^c   Sainz, T ^d,e   Martinez Botas J ^c,f   Ferrando Martinez S ^d,e,g   Vera, M ^h   Dronda, F ^c   Leal, M ^g   Del Romero, J ^h   Moreno, S ^c   Estrada, V ⁱ   Gosalbes, M J ^a,b   Moya, A ^a,b  

^a UNIVERSITY OF VALENCIA   (Spain)

^b CIBER EPIDEMIOLOGÍA Y SALUD PÚBLICA CIBERESP   (Spain)

^c HOSPITAL RAMÓN Y CAJAL   (Spain)

^d HOSPITAL GENERAL UNIVERSITARIO GREGORIO MARAÑÓN   (Spain)

^e BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^f Instituto de Salud Carlos III   (Spain)

^g HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^h CENTRO SANITARIO SANDOVAL   (Spain)

ⁱ HOSPITAL CLÍNICO SAN CARLOS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

16S RRNA GENE; ADAPTIVE IMMUNITY; ADULT; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BACTERIAL TRANSLOCATION; BAYES THEOREM; CHRONIC IMMUNE ACTIVATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC ANALYSIS; HOST PATHOGEN INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; INNATE IMMUNITY; INTESTINE FLORA; METAGENOME; MICROBIAL COMMUNITY; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SPECIES COMPOSITION; BIODIVERSITY; CASE CONTROL STUDY; CLUSTER ANALYSIS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HIV INFECTIONS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOLOGY; MARKOV CHAIN; METABOLISM; METABOLOME; METABOLOMICS; MICROBIOLOGY;

ADAPTIVE IMMUNITY; ANTIRETROVIRAL THERAPY, HIGHLY ACTIVE; BAYES THEOREM; BIODIVERSITY; CASE-CONTROL STUDIES; CLUSTER ANALYSIS; DISEASE PROGRESSION; GASTROINTESTINAL MICROBIOME; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; MARKOV CHAINS; METABOLOME; METABOLOMICS; METAGENOME; RNA, RIBOSOMAL, 16S;

EID: 84932619244     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.107     Document Type: Article

References (53)

1. Sandler N.G. & Douek D.C. Microbial translocation in HIV infection: causes, consequences and treatment opportunities. Nat. Rev. Microbiol. 10, 655-666 (2012
2. Brenchley J.M., et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat. Med. 12, 1365-1371 (2006
3. Deeks S.G., Tracy R. & Douek D.C. Systemic effects of inflammation on health during chronic HIV infection. Immunity 39, 633-645 (2013
4. Jiang W., et al. Plasma levels of bacterial DNA correlate with immune activation and the magnitude of immune restoration in persons with antiretroviral-treated HIV infection. J. Infect. Dis. 199, 1177-1185 (2009
5. Mavigner M., et al. Altered CD4+ Tcell homing to the gut impairs mucosal immune reconstitution in treated HIV-infected individuals. J. Clin. Invest. 122, 62-69 (2012
6. Neuhaus J., et al. Markers of inflammation, coagulation, and renal function are elevated in adults with HIV infection. J. Infect. Dis. 201, 1788-1795 (2010
7. Sandler N.G., et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J. Infect. Dis. 203, 780-790 (2011
8. Appay V. & Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. J. Pathol. 214, 231-241 (2008
9. Deeks S., Lewin S. & Havlir D. The end of AIDS: HIV infection as a chronic disease. Lancet 382, 1525-1533 (2013
10. Cebula A., et al. Thymus-derived regulatory Tcells contribute to tolerance to commensal microbiota. Nature 497, 258-262 (2013
11. Cho I. & Blaser M.J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260-270 (2012
12. Morgan X.C., et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 13, R79 (2012
13. Presley L.L., et al. Host-microbe relationships in inflammatory bowel disease detected by bacterial and metaproteomic analysis of the mucosalluminal interface. Inflamm. Bowel Dis. 18, 409-417 (2012
14. Qin J., et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59-65 (2010
15. McHardy I.H., et al. HIV Infection is associated with compositional and functional shifts in the rectal mucosal microbiota. Microbiome 1, 26 (2013
16. Kanehisa M., Goto S., Kawashima S., Okuno Y. & Hattori M. The KEGG resource for deciphering the genome.Nucleic Acids Res. 32, 277-280 (2004
17. Pearl J. Probabilistic Reasoning in Intelligent Systems: Networks of Plausible Inference, 2nd edn (Morgan Kaufmann Publishers Inc, San Francisco California USA, 1988
18. Su C., Andrew A., Karagas M.R. & Borsuk M.E. Using Bayesian networks to discover relations between genes, environment, and disease. BioData Min. 6, 6 (2013
19. Yu G., Fadrosh D., Ma B., Ravel J. & Goedert J.J. Anal microbiota profiles in HIV-positive and HIV-negative MSM. AIDS 28, 753-760 (2013
20. Dillon S., Lee E., Kotter C. & Austin G. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol. 7, 983-994 (2014
21. Ellis C., Ma Z., Mann S. & Li C. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-Level 16S Ribosomal DNA (rDNA) quantification and correlations with immune activation. J. Acquir. Immune Defic. Syndr. 57, 363-370 (2011
22. Pérez-Santiago J., Gianella S. & Massanella M. Gut lactobacillales are associated with higher CD4 and less microbial translocation during HIV infection. AIDS 27, 1921-1931 (2013
23. Vujkovic-Cvijin I., et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci. Transl. Med. 5, 193ra91 (2013
24. Lozupone C.A., et al. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 14, 329-339 (2013
25. Mutlu E.A., et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog. 10, e1003829 (2014
26. Durbán, A., et al. Assessing gut microbial diversity from feces and rectal mucosa. Microb. Ecol. 61, 123-133 (2011
27. Winter S.E., et al. Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708-711 (2013
28. Mukhopadhya I., Hansen R., El-Omar E.M. & Hold G.L. IBD-what role do Proteobacteria play?. Nat. Rev. Gastroenterol. Hepatol. 9, 219-230 (2012
29. Serrano-Villar S., et al. HIV-infected individuals with low CD4/CD8 ratio despite effective antiretroviral therapy exhibit altered T cell subsets, heightened CD8+ T cell activation, and increased risk of non-AIDS morbidity and mortality. PLoS Pathog. 10, e1004078 (2014
30. De Filippo C., et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc. Natl Acad. Sci. USA 107, 14691-14696 (2010
31. Yatsunenko T., et al. Human gut microbiome viewed across age and geography. Nature 486, 222-227 (2012
32. Wu G.D., et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105-108 (2011
33. Ou J. & Carbonero F. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am. J. Clin. Nutr. 98, 111-120 (2013
34. Louis P., Scott K.P., Duncan S.H. & Flint H.J. Understanding the effects of diet on bacterial metabolism in the large intestine. J. Appl. Microbiol. 102, 1197-1208 (2007
35. Vinolo M.R., Rodrigues H.G., Nachbar R.T. & Curi R. Regulation of inflammation by short chain fatty acids. Nutrients 3, 858-876 (2011
36. Carvalho B.M. & Saad M.J.A. Influence of gut microbiota on subclinical inflammation and insulin resistance. Mediators Inflamm. 2013, 13 (2013
37. Rook G. Regulation of the immune system by biodiversity from the natural environment: An ecosystem service essential to health. Proc. Natl Acad. Sci. USA 110, 1-8 (2013
38. Sokol H., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl Acad. Sci. USA 105, 16731-16736 (2008
39. Biagi E., et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS ONE 5, e10667 (2010
40. Ivanov I.I., et al. Specific microbiota direct the differentiation of IL-17- producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349 (2008
41. Deeks S.G., Verdin E.& cCune J.M. Immunosenescence andHIV. Curr. Opin. Immunol. 24, 501-506 (2012
42. Arumugam M., et al. Enterotypes of the human gut microbiome. Nature 473, 174-180 (2011
43. Verhasselt V., et al. Bacterial lipopolysaccharide stimulates the production of cytokines and the expression of costimulatory molecules by human peripheral blood dendritic cells. J. Immunol. 158, 2919-2925 (1997
44. Karlsson F.H., et al. Symptomatic atherosclerosis is associated with an altered gut metagenome. Nat. Commun. 3, 1245 (2012
45. Naik S.R., Rupawalla E.N. & Sheth U.K. Anti-inflammatory activity of thiamine and nicotinic acid. Biochem. Pharmacol. 19, 2867-2873 (1970
46. Moallem S., Hosseinzadeh H. & Farahi S. A study of acute and chronic anti-nociceptive and anti-inflammatory effects of thiamine in mice. Iran Biomed. J. 12, 173-178 (2008
47. Kuroki F., et al. Multiple vitamin status in Crohn's disease. Dig. Dis. Sci. 38, 1614-1618 (1993
48. Pérez-Cobas A.E., et al. Gut microbiota disturbance during antibiotic therapy: a multi-omic approach. Gut 62, 1591-1601 (2013
49. Caporaso J., et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010
50. Meyer F., et al. The metagenomics RASTserver-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9, 386 (2008
51. Segata N., et al. Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011
52. Ferrando-Martínez S., et al. A reliable and simplified sj/beta-TREC ratio quantification method for human thymic output measurement. J. Immunol. Methods 352, 111-117 (2010
53. Scutari M. Learning Bayesian Networks with the bnlearn R Package. J. Stat. Softw. 35, 1-22 (2010