A Compositional Look at the Human Gastrointestinal Microbiome and Immune Activation Parameters in HIV Infected Subjects

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Mutlu, Ece A ^a   Keshavarzian, Ali ^a,b,c   Losurdo, John ^a   Swanson, Garth ^a   Siewe, Basile ^a   Forsyth, Christopher ^a,b   French, Audrey ^a   DeMarais, Patricia ^a   Sun, Yan ^d   Koenig, Lars ^d   Cox, Stephen ^d   Engen, Phillip ^a   Chakradeo, Prachi ^a   Abbasi, Rawan ^a   Gorenz, Annika ^a   Burns, Charles ^e   Landay, Alan ^a,c  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

^b RUSH UNIVERSITY   (United States)

^c UTRECHT UNIVERSITY   (Netherlands)

^d Research and Testing Laboratory   (United States)

^e RUSH MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COTRIMOXAZOLE; INTERLEUKIN 6; LIPOTEICHOIC ACID;

ARTICLE; CD4 LYMPHOCYTE COUNT; CLINICAL ARTICLE; COLONOSCOPY; CONTROLLED STUDY; DISEASE COURSE; DRUG USE; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HUMAN TISSUE; IMMUNITY; INTESTINE FLORA; MICROBIAL DIVERSITY; MICROBIOME; PYROSEQUENCING; VIRUS LOAD;

FEMALE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV INFECTIONS; HUMANS; INTESTINAL MUCOSA; MALE; MICROBIOTA; MIDDLE AGED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S;

EID: 84895733084     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003829     Document Type: Article

References (59)

1. Sandler NG, Wand H, Roque A, Law M, Nason MC, et al. (2011) Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infect Dis 203: 780-790.
2. Ostrowski SR, Piironen T, Hoyer-Hansen G, Gerstoft J, Pedersen BK, et al. (2005) High plasma levels of intact and cleaved soluble urokinase receptor reflect immune activation and are independent predictors of mortality in HIV-1-infected patients. J Acquir Immune Defic Syndr 39: 23-31.
3. Klatt NR, Funderburg NT, Brenchley JM, (2013) Microbial translocation, immune activation, and HIV disease. Trends Microbiol 21: 6-13.
4. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, et al. (2004) CD4+ T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 200: 749-759.
5. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
6. Gori A, Tincati C, Rizzardini G, Torti C, Quirino T, et al. (2008) Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J Clin Microbiol 46: 757-758.
7. Merlini E, Bai F, Bellistri GM, Tincati C, d'Arminio Monforte A, et al. (2011) Evidence for polymicrobic flora translocating in peripheral blood of HIV-infected patients with poor immune response to antiretroviral therapy. PLoS One 6: e18580.
8. Gori A, Rizzardini G, Van't Land B, Amor KB, van Schaik J, et al. (2011) Specific prebiotics modulate gut microbiota and immune activation in HAART-naive HIV-infected adults: results of the "COPA" pilot randomized trial. Mucosal Immunol 4: 554-563.
9. Handley SA, Thackray LB, Zhao G, Presti R, Miller AD, et al. (2012) Pathogenic simian immunodeficiency virus infection is associated with expansion of the enteric virome. Cell 151: 253-266.
10. McKenna P, Hoffmann C, Minkah N, Aye PP, Lackner A, et al. (2008) The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4: e20.
11. Bray JR, Curtis CT, (1957) An ordination of upland forest communities of southern Wisconsin. Ecological Monographs 27: 325-349.
12. Lozupone C, Knight R, (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235.
13. Vaziri ND, Wong J, Pahl M, Piceno YM, Yuan J, et al. (2013) Chronic kidney disease alters intestinal microbial flora. Kidney Int 83: 308-315.
14. Cheung MK, Lam WY, Fung WY, Law PT, Au CH, et al. (2013) Sputum Microbiota in Tuberculosis as Revealed by 16S rRNA Pyrosequencing. PLoS One 8: e54574.
15. Colombo AP, Boches SK, Cotton SL, Goodson JM, Kent R, et al. (2009) Comparisons of subgingival microbial profiles of refractory periodontitis, severe periodontitis, and periodontal health using the human oral microbe identification microarray. J Periodontol 80: 1421-1432.
16. Sato T, Yamaki K, Ishida N, Hashimoto K, Takeuchi Y, et al. (2012) Cultivable anaerobic microbiota of infected root canals. Int J Dent 2012: 609689.
17. Rolph HJ, Lennon A, Riggio MP, Saunders WP, MacKenzie D, et al. (2001) Molecular identification of microorganisms from endodontic infections. J Clin Microbiol 39: 3282-3289.
18. Rammaert B, Borand L, Goyet S, Te V, Hem S, et al. (2010) Ralstonia pickettii community-acquired pneumonia in Cambodia. Int J Tuberc Lung Dis 14: 1653-1654.
19. Pan W, Zhao Z, Dong M, (2011) Lobar pneumonia caused by Ralstonia pickettii in a sixty-five-year-old Han Chinese man: a case report. J Med Case Rep 5: 377.
20. Davies JC, Rubin BK, (2007) Emerging and unusual gram-negative infections in cystic fibrosis. Semin Respir Crit Care Med 28: 312-321.
21. Barbut F, Kosmann MJ, Lalande V, Neyme D, Coppo P, et al. (2006) Outbreak of Ralstonia pickettii pseudobacteremia among patients with hematological malignancies. Infect Control Hosp Epidemiol 27: 642-644.
22. Xu J, Moore JE, Millar BC, Alexander HD, McClurg R, et al. (2004) Improved laboratory diagnosis of bacterial and fungal infections in patients with hematological malignancies using PCR and ribosomal RNA sequence analysis. Leuk Lymphoma 45: 1637-1641.
23. Ryan MP, Pembroke JT, Adley CC, (2006) Ralstonia pickettii: a persistent gram-negative nosocomial infectious organism. J Hosp Infect 62: 278-284.
24. Ena J, Simon-Aylon A, Pasquau F, (2009) Intestinal spirochetosis as a cause of chronic diarrhoea in patients with HIV infection: case report and review of the literature. Int J STD AIDS 20: 803-805.
25. Watts DH, (2012) Mother to child transmission of HIV-another complication of bacterial vaginosis? J Acquir Immune Defic Syndr 60: 221-224.
26. Frank DN, Manigart O, Leroy V, Meda N, Valea D, et al. (2012) Altered vaginal microbiota are associated with perinatal mother-to-child transmission of HIV in African women from Burkina Faso. J Acquir Immune Defic Syndr 60: 299-306.
27. Saxena D, Li Y, Yang L, Pei Z, Poles M, et al. (2012) Human microbiome and HIV/AIDS. Curr HIV/AIDS Rep 9: 44-51.
28. Spear GT, Gilbert D, Landay AL, Zariffard R, French AL, et al. (2011) Pyrosequencing of the genital microbiotas of HIV-seropositive and-seronegative women reveals Lactobacillus iners as the predominant Lactobacillus Species. Appl Environ Microbiol 77: 378-381.
29. Hummelen R, Fernandes AD, Macklaim JM, Dickson RJ, Changalucha J, et al. (2010) Deep sequencing of the vaginal microbiota of women with HIV. PLoS One 5: e12078.
30. Spear GT, Sikaroodi M, Zariffard MR, Landay AL, French AL, et al. (2008) Comparison of the diversity of the vaginal microbiota in HIV-infected and HIV-uninfected women with or without bacterial vaginosis. J Infect Dis 198: 1131-1140.
31. Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214.
32. Sanapareddy N, Legge RM, Jovov B, McCoy A, Burcal L, et al. (2012) Increased rectal microbial richness is associated with the presence of colorectal adenomas in humans. ISME J 6: 1858-1868.
33. Hansen R, Russell RK, Reiff C, Louis P, McIntosh F, et al. (2012) Microbiota of de-novo pediatric IBD: increased Faecalibacterium prausnitzii and reduced bacterial diversity in Crohn's but not in ulcerative colitis. Am J Gastroenterol 107: 1913-1922.
34. Manichanh C, Rigottier-Gois L, Bonnaud E, Gloux K, Pelletier E, et al. (2006) Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55: 205-211.
35. Ellis CL, Ma ZM, Mann SK, Li CS, Wu J, et al. (2011) 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.
36. Vujkovic-Cvijin I, Dunham RM, Iwai S, Maher MC, Albright RG, et al. (2013) Dysbiosis of the Gut Microbiota Is Associated with HIV Disease Progression and Tryptophan Catabolism. Sci Transl Med 5: 193ra191.
37. Sankaran S, George MD, Reay E, Guadalupe M, Flamm J, et al. (2008) Rapid onset of intestinal epithelial barrier dysfunction in primary human immunodeficiency virus infection is driven by an imbalance between immune response and mucosal repair and regeneration. J Virol 82: 538-545.
38. Epple HJ, Schneider T, Troeger H, Kunkel D, Allers K, et al. (2009) Impairment of the intestinal barrier is evident in untreated but absent in suppressively treated HIV-infected patients. Gut 58: 220-227.
39. Smith AJ, Schacker TW, Reilly CS, Haase AT, (2010) A role for syndecan-1 and claudin-2 in microbial translocation during HIV-1 infection. J Acquir Immune Defic Syndr 55: 306-315.
40. Costiniuk CT, Angel JB, (2012) Human immunodeficiency virus and the gastrointestinal immune system: does highly active antiretroviral therapy restore gut immunity? Mucosal Immunol 5: 596-604.
41. Ahmed S, Macfarlane GT, Fite A, McBain AJ, Gilbert P, et al. (2007) Mucosa-associated bacterial diversity in relation to human terminal ileum and colonic biopsy samples. Appl Environ Microbiol 73: 7435-7442.
42. Nava GM, Stappenbeck TS, (2011) Diversity of the autochthonous colonic microbiota. Gut Microbes 2: 99-104.
43. Wilson NL, Moneyham LD, Alexandrov AW, (2013) A Systematic Review of Probiotics as a Potential Intervention to Restore Gut Health in HIV Infection. J Assoc Nurses AIDS Care 24: 98-111.
44. Schunter M, Chu H, Hayes TL, McConnell D, Crawford SS, et al. (2012) Randomized pilot trial of a synbiotic dietary supplement in chronic HIV-1 infection. BMC Complement Altern Med 12: 84.
45. Gonzalez-Hernandez LA, Jave-Suarez LF, Fafutis-Morris M, Montes-Salcedo KE, Valle-Gutierrez LG, et al. (2012) Synbiotic therapy decreases microbial translocation and inflammation and improves immunological status in HIV-infected patients: a double-blind randomized controlled pilot trial. Nutr J 11: 90.
46. Smith DM, Snow DE, Rees E, Zischkau AM, Hanson JD, et al. (2010) Evaluation of the bacterial diversity of pressure ulcers using bTEFAP pyrosequencing. BMC Med Genomics 3: 41.
47. Wolcott RD, Gontcharova V, Sun Y, Dowd SE, (2009) Evaluation of the bacterial diversity among and within individual venous leg ulcers using bacterial tag-encoded FLX and titanium amplicon pyrosequencing and metagenomic approaches. BMC Microbiol 9: 226.
48. Sen R, Ishak HD, Estrada D, Dowd SE, Hong E, et al. (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci U S A 106: 17805-17810.
49. Ishak HD, Plowes R, Sen R, Kellner K, Meyer E, et al. (2011) Bacterial diversity in Solenopsis invicta and Solenopsis geminata ant colonies characterized by 16S amplicon 454 pyrosequencing. Microb Ecol 61: 821-831.
50. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335-336.
51. Edgar RC, (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
52. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R, (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
53. Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, et al. (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res 21: 494-504.
54. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, et al. (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266-267.
55. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, et al. (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6: 610-618.
56. Werner JJ, Koren O, Hugenholtz P, DeSantis TZ, Walters WA, et al. (2012) Impact of training sets on classification of high-throughput bacterial 16s rRNA gene surveys. ISME J 6: 94-103.
57. Wang Q, Garrity GM, Tiedje JM, Cole JR, (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73: 5261-5267.
58. Price MN, Dehal PS, Arkin AP, (2010) FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5: e9490.
59. Dufrene M, Legendre P, (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345-366.