HIV-induced alteration in gut Microbiota: Driving factors, consequences, and effects of antiretroviral therapy

Gut Microbes

Volumn 5, Issue 4, 2014, Pages 562-570

  Lozupone, Catherine A ^a   Rhodes, Matthew E ^a   Neff, Charles P ^a   Fontenot, Andrew P ^a   Campbell, Thomas B ^a   Palmer, Brent E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

Bacteria; Bacteroides; CD4+ T cells; Gastrointestinal tract; Inflammation; Metabolic disease; Microbiome; Prevotella; Regulatory T cells

Indexed keywords

RNA 16S; TRIMETHYLAMINE; ANTIRETROVIRUS AGENT;

ADAPTIVE IMMUNITY; ARTICLE; BACTERIAL COLONIZATION; BACTEROIDES; CD4+ T LYMPHOCYTE; CHRONIC INFLAMMATION; DESULFOVIBRIO; HELICOBACTER HEPATICUS; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE DEFICIENCY; INTESTINE FLORA; INTESTINE LYMPHATIC TISSUE; NONHUMAN; POLYMERASE CHAIN REACTION; PREVOTELLA; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; VIRUS LOAD; VIRUS PATHOGENESIS; ADULT; COHORT ANALYSIS; FEMALE; GASTROINTESTINAL TRACT; HIV INFECTIONS; IMMUNOLOGY; MALE; MICROBIOLOGY; MICROFLORA; MIDDLE AGED; PATHOLOGY;

ADULT; ANTI-RETROVIRAL AGENTS; COHORT STUDIES; FEMALE; GASTROINTESTINAL TRACT; HIV INFECTIONS; HUMANS; MALE; MICROBIOTA; MIDDLE AGED;

EID: 84924375353     PISSN: 19490976     EISSN: 19490984     Source Type: Journal    
DOI: 10.4161/gmic.32132     Document Type: Article

References (58)

1. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, Nguyen PL, Khoruts A, Larson M, Haase AT, et al. CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-59 PMID:15365096; http://dx.doi.org/10.1084/jem.20040874
2. Dillon SM, Lee EJ, Kotter CV, Austin GL, Dong Z, Hecht DK, Gianella S, Siewe B, Smith DM, Landay AL, et al. An altered intestinal mucosal microbiome in HIV-1 infection is associated with mucosal and systemic immune activation and endotoxemia. Mucosal Immunol 2014; 7:983-94 PMID:24399150; http://dx.doi.org/10.1038/mi.2013.116
3. McHardy IH, Li X, Tong M, Ruegger P, Jacobs J, Borneman J, Anton P, Braun J. HIV Infection is associated with compositional and functional shifts in the rectal mucosal microbiota. Microbiome 2013; 1:26 PMID:24451087; http://dx.doi.org/10.1186/2049-2618-1-26
4. Mutlu EA, Keshavarzian A, Losurdo J, Swanson G, Siewe B, Forsyth C, French A, Demarais P, Sun Y, Koenig L, et al. A compositional look at the human gastrointestinal microbiome and immune activation parameters in HIV infected subjects. PLoS Pathog 2014; 10:e1003829 PMID:24586144; http://dx.doi.org/10.1371/journal.ppat.1003829
5. Vujkovic-Cvijin I, Dunham RM, Iwai S, Maher MC, Albright RG, Broadhurst MJ, Hernandez RD, Lederman MM, Huang Y, Somsouk M, et al. Dysbiosis of the gut microbiota is associated with HIV disease progression and tryptophan catabolism. Sci Transl Med 2013; 5:93ra91 PMID:23843452; http://dx.doi.org/10.1126/scitranslmed.3006438
6. Lozupone CA, Li M, Campbell TB, Flores SC, Linderman D, Gebert MJ, Knight R, Fontenot AP, Palmer BE. Alterations in the gut microbiota associated with HIV-1 infection. Cell Host Microbe 2013; 14:329-39 PMID:24034618; http://dx.doi.org/10.1016/j.chom.2013.08.006
7. Brenchley JM, Douek DC. HIV infection and the gastrointestinal immune system. Mucosal Immunol 2008; 1:23-30 PMID:19079157; http://dx.doi.org/10.1038/mi.2007.1
8. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, Kazzaz Z, Bornstein E, Lambotte O, Altmann D, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365-71 PMID:17115046; http://dx.doi.org/10.1038/nm1511
9. Moriyama K, Ando C, Tashiro K, Kuhara S, Okamura S, Nakano S, Takagi Y, Miki T, Nakashima Y, Hirakawa H. Polymerase chain reaction detection of bacterial 16S rRNA gene in human blood. Microbiol Immunol 2008; 52:375-82 PMID:18667036; http://dx.doi.org/10.1111/j.1348-0421.2008.00048.x
10. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, et al. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc Natl Acad Sci U S A 2013; 110:9066-71 PMID:23671105; http://dx.doi.org/10.1073/pnas.1219451110
11. Gauffin Cano P, Santacruz A, Moya Á, Sanz Y. Bacteroides uniformis CECT 7771 ameliorates metabolic and immunological dysfunction in mice with high-fat-diet induced obesity. PLoS One 2012; 7:e41079 PMID:22844426; http://dx.doi.org/10.1371/journal.pone.0041079
12. Koeth RA, Wang Z, Levison BS, Buffa JA, Org E, Sheehy BT, Britt EB, Fu X, Wu Y, Li L, et al. Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis. Nat Med 2013; 19:576-85 PMID:23563705; http://dx.doi.org/10.1038/nm.3145
13. Mukhopadhya I, Hansen R, El-Omar EM, Hold GL. IBD-what role do Proteobacteria play? Nat Rev Gastroenterol Hepatol 2012; 9:219-30 PMID:22349170; http://dx.doi.org/10.1038/nrgastro.2012.14
14. de Souza HL, de Carvalho VR, Romeiro FG, Sassaki LY, Keller R, Rodrigues J. Mucosa-associated but not luminal Escherichia coli is augmented in Crohn’s disease and ulcerative colitis. Gut Pathog 2012; 4.
15. Stackebrandt E, Goebal BM. Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int Syst Bacteriol 1994; 44:846-9; http://dx.doi.org/10.1099/00207713-44-4-846
16. Namavar F, Theunissen EB, Verweij-Van Vught AM, Peerbooms PG, Bal M, Hoitsma HF, MacLaren DM. Epidemiology of the Bacteroides fragilis group in the colonic flora in 10 patients with colonic cancer. J Med Microbiol 1989; 29:171-6 PMID:2746627; http://dx.doi.org/10.1099/00222615-29-3-171
17. Max B, Sherer R. Management of the adverse effects of antiretroviral therapy and medication adherence. Clin Infect Dis 2000; 30(Suppl 2):S96-116 PMID:10860894; http://dx.doi.org/10.1086/313859
18. Kartalija M, Sande MA. Diarrhea and AIDS in the era of highly active antiretroviral therapy. Clin Infect Dis 1999; 28:701-5, quiz 706-7 PMID:10825021; http://dx.doi.org/10.1086/515191
19. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008; 197:435-8 PMID:18199029; http://dx.doi.org/10.1086/525047
20. Maynard CL, Elson CO, Hatton RD, Weaver CT. Reciprocal interactions of the intestinal microbiota and immune system. Nature 2012; 489:231-41 PMID:22972296; http://dx.doi.org/10.1038/nature11551
21. Round JL, Lee SM, Li J, Tran G, Jabri B, Chatila TA, Mazmanian SK. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011; 332:974-7 PMID:21512004; http://dx.doi.org/10.1126/science.1206095
22. Tzianabos AO, Onderdonk AB, Rosner B, Cisneros RL, Kasper DL. Structural features of polysaccharides that induce intra-abdominal abscesses. Science 1993; 262:416-9 PMID:8211161; http://dx.doi.org/10.1126/science.8211161
23. Avci FY, Kasper DL. How bacterial carbohydrates influence the adaptive immune system. Annu Rev Immunol 2010; 28:107-30 PMID:19968562; http://dx.doi.org/10.1146/annurev-immunol-030409-101159
24. Kverka M, Zakostelska Z, Klimesova K, Sokol D, Hudcovic T, Hrncir T, Rossmann P, Mrazek J, Kopecny J, Verdu EF, et al. Oral administration of Parabacteroides distasonis antigens attenuates experimental murine colitis through modulation of immunity and microbiota composition. Clin Exp Immunol 2011; 163:250-9 PMID:21087444; http://dx.doi.org/10.1111/j.1365-2249.2010.04286.x
25. Lathrop SK, Bloom SM, Rao SM, Nutsch K, Lio CW, Santacruz N, Peterson DA, Stappenbeck TS, Hsieh CS. Peripheral education of the immune system by colonic commensal microbiota. Nature 2011; 478:250-4 PMID:21937990; http://dx.doi.org/10.1038/nature10434
26. Faith JJ, Ahern PP, Ridaura VK, Cheng J, Gordon JI. Identifying gut microbe-host phenotype relationships using combinatorial communities in gnotobiotic mice. Sci Transl Med 2014; 6:20ra11 PMID:24452263; http://dx.doi.org/10.1126/scitranslmed.3008051
27. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, Fukuda S, Saito T, Narushima S, Hase K, et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013; 500:232-6 PMID:23842501; http://dx.doi.org/10.1038/nature12331
28. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, Shih R, Lewis J, Wiley DJ, Phair JP, et al. Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 1999; 179:859-70 PMID:10068581; http://dx.doi.org/10.1086/314660
29. Hunt PW, Brenchley J, Sinclair E, McCune JM, Roland M, Page-Shafer K, Hsue P, Emu B, Krone M, Lampiris H, et al. Relationship between T cell activation and CD4+ T cell count in HIV-seropositive individuals with undetectable plasma HIV RNA levels in the absence of therapy. J Infect Dis 2008; 197:126-33 PMID:18171295; http://dx.doi.org/10.1086/524143
30. Salazar-Gonzalez JF, Martinez-Maza O, Nishanian P, Aziz N, Shen LP, Grosser S, Taylor J, Detels R, Fahey JL. Increased immune activation precedes the inflection point of CD4 T cells and the increased serum virus load in human immunodeficiency virus infection. J Infect Dis 1998; 178:423-30 PMID:9697722; http://dx.doi.org/10.1086/515629
31. De Lorenzo F, Collot-Teixeira S, Boffito M, Feher M, Gazzard B, McGregor JL. Metabolic-inflammatory changes, and accelerated atherosclerosis in HIV patients: rationale for preventative measures. Curr Med Chem 2008; 15:2991-9 PMID:19075647; http://dx.doi.org/10.2174/092986708786848668
32. Madge S, Kinloch-de-Loes S, Mercey D, Johnson MA, Weller IVD. Lipodystrophy in patients naive to HIV protease inhibitors. AIDS 1999; 13:735-7 PMID:10397574; http://dx.doi.org/10.1097/00002030-199904160-00020
33. Mutimura E, Stewart A, Rheeder P, Crowther NJ. Metabolic function and the prevalence of lipodystrophy in a population of HIV-infected African subjects receiving highly active antiretroviral therapy. J Acquir Immune Defic Syndr 2007; 46:451-5 PMID:18077834; http://dx.doi.org/10.1097/QAI.0b013e318158c0a6
34. Shevitz A, Wanke CA, Falutz J, Kotler DP. Clinical perspectives on HIV-associated lipodystrophy syndrome: an update. AIDS 2001; 15:1917-30 PMID:11600819; http://dx.doi.org/10.1097/00002030-200110190-00003
35. Trøseid M, Manner IW, Pedersen KK, Haissman JM, Kvale D, Nielsen SD. Microbial translocation and cardiometabolic risk factors in HIV infection. AIDS Res Hum Retroviruses 2014; 30:514-22 PMID:24521167; http://dx.doi.org/10.1089/aid.2013.0280
36. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008; 453:620-5 PMID:18509436; http://dx.doi.org/10.1038/nature07008
37. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 2010; 107:12204-9 PMID:20566854; http://dx.doi.org/10.1073/pnas.0909122107
38. Dillon SM, Manuzak JA, Leone AK, Lee EJ, Rogers LM, McCarter MD, Wilson CC. HIV-1 infection of human intestinal lamina propria CD4+ T cells in vitro is enhanced by exposure to commensal Escherichia coli. J Immunol 2012; 189:885-96 PMID:22689879; http://dx.doi.org/10.4049/jimmunol.1200681
39. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, Rostron T, Cerundolo V, Pamer EG, Abramson SB, et al. Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife (Cambridge) 2013; 2:e01202 PMID:24192039; http://dx.doi.org/10.7554/eLife.01202
40. Elinav E, Strowig T, Kau AL, Henao-Mejia J, Thaiss CA, Booth CJ, Peaper DR, Bertin J, Eisenbarth SC, Gordon JI, et al. NLRP6 inflammasome regulates colonic microbial ecology and risk for colitis. Cell 2011; 145:745-57 PMID:21565393; http://dx.doi.org/10.1016/j.cell.2011.04.022
41. Larsen JM, Steen-Jensen DB, Laursen JM, Søndergaard JN, Musavian HS, Butt TM, Brix S. Divergent pro-inflammatory profile of human dendritic cells in response to commensal and pathogenic bacteria associated with the airway microbiota. PLoS One 2012; 7:e31976 PMID:22363778; http://dx.doi.org/10.1371/journal.pone.0031976
42. Elinav E, Henao-Mejia J, Flavell RA. Integrative inflammasome activity in the regulation of intestinal mucosal immune responses. Mucosal Immunol 2013; 6:4-13 PMID:23212196; http://dx.doi.org/10.1038/mi.2012.115
43. Benjdia A, Martens EC, Gordon JI, Berteau O. Sulfatases and a radical S-adenosyl-L-methionine (AdoMet) enzyme are key for mucosal foraging and fitness of the prominent human gut symbiont, Bacteroides thetaiotaomicron. J Biol Chem 2011; 286:25973-82 PMID:21507958; http://dx.doi.org/10.1074/jbc.M111.228841
44. De Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, Collini S, Pieraccini G, Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A 2010; 107:14691-6 PMID:20679230; http://dx.doi.org/10.1073/pnas.1005963107
45. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, et al. Human gut microbiome viewed across age and geography. Nature 2012; 486:222-7 PMID:22699611
46. Ruengsomwong S, Korenori Y, Sakamoto N, Wannissorn B, Nakayama J, Nitisinprasert S. Senior Thai fecal microbiota comparison between vegetarians and non-vegetarians using PCR-DGGE and real-time PCR. J Microbiol Biotechnol 2014 PMID:24743571
47. Wu GD, Chen J, Hoffmann C, Bittinger K, Chen YY, Keilbaugh SA, Bewtra M, Knights D, Walters WA, Knight R, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011; 334:105-8 PMID:21885731; http://dx.doi.org/10.1126/science.1208344
48. Cabrero E, Griffa L, Burgos A; HIV Body Physical Changes Study Group. Prevalence and impact of body physical changes in HIV patients treated with highly active antiretroviral therapy: results from a study on patient and physician perceptions. AIDS Patient Care STDS 2010; 24:5-13 PMID:20095903; http://dx.doi.org/10.1089/apc.2009.0191
49. Galescu O, Bhangoo A, Ten S. Insulin resistance, lipodystrophy and cardiometabolic syndrome in HIV/AIDS. Rev Endocr Metab Disord 2013; 14:133-40 PMID:23700046; http://dx.doi.org/10.1007/s11154-013-9247-7
50. Leclercq P, Goujard C, Duracinsky M, Allaert F, L’henaff M, Hellet M, Meunier JP, Carret S, Thevenon J, Ngo Van P, et al. High prevalence and impact on the quality of life of facial lipoatrophy and other abnormalities in fat tissue distribution in HIV-infected patients treated with antiretroviral therapy. AIDS Res Hum Retroviruses 2013; 29:761-8 PMID:23268562; http://dx.doi.org/10.1089/aid.2012.0214
51. Hadigan C, Jeste S, Anderson EJ, Tsay R, Cyr H, Grinspoon S. Modifiable dietary habits and their relation to metabolic abnormalities in men and women with human immunodeficiency virus infection and fat redistribution. Clin Infect Dis 2001; 33:710-7 PMID:11486294; http://dx.doi.org/10.1086/322680
52. Hendricks KM, Dong KR, Tang AM, Ding B, Spiegelman D, Woods MN, Wanke CA. High-fiber diet in HIV-positive men is associated with lower risk of developing fat deposition. Am J Clin Nutr 2003; 78:790-5 PMID:14522738
53. Craciun S, Balskus EP. Microbial conversion of choline to trimethylamine requires a glycyl radical enzyme. Proc Natl Acad Sci U S A 2012; 109:21307-12 PMID:23151509; http://dx.doi.org/10.1073/pnas.1215689109
54. Mansfield KG, Carville A, Wachtman L, Goldin BR, Yearley J, Li W, Woods M, Gualtieri L, Shannon R, Wanke C. A diet high in saturated fat and cholesterol accelerates simian immunodeficiency virus disease progression. J Infect Dis 2007; 196:1202-10 PMID:17955439; http://dx.doi.org/10.1086/521680
55. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010; 7:335-6 PMID:20383131; http://dx.doi.org/10.1038/nmeth.f.303
56. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26:2460-1 PMID:20709691; http://dx.doi.org/10.1093/bioinformatics/btq461
57. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 2012; 6:610-8 PMID:22134646; http://dx.doi.org/10.1038/ismej.2011.139
58. Benjamini Y, Hochberg Y. Controlling the False Discovery Rate-a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met 1995; 57:289-300