The influence of the autoimmunity-associated ancestral HLA haplotype AH8.1 on the human gut microbiota: A cross-sectional study

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Hov, Johannes R ^a,b   Zhong, Huanzi ^c   Qin, Bingcai ^c,d   Anmarkrud, Jarl Andreas ^a   Holm, Kristian ^a   Franke, Andre ^e   Lie, Benedicte A ^a,b,f   Karlsen, Tom H ^a,b,g  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

^c BGI SHENZHEN   (China)

^d Division of Cancer Medicine Surgery and Transplantation Section of Gastroenterology Department of Transplantation Medicine Oslo University Hospital Rikshospitalet ^*  (China)

^e UNIVERSITY OF KIEL   (Germany)

^f OSLO UNIVERSITY HOSPITAL   (Norway)

^g UNIVERSITY OF BERGEN   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; HLA ANTIGEN; RNA 16S; HISTOCOMPATIBILITY ANTIGEN; HLA DRB1 ANTIGEN;

ARTICLE; AUTOIMMUNITY; BACTERIUM; CLOSTRIDIUM; CONTROLLED STUDY; COPROCOCCUS; CROSS-SECTIONAL STUDY; ENTERORHABDUS; FECES ANALYSIS; GENETIC ASSOCIATION; GENETIC VARIABILITY; HAPLOTYPE; HOMOZYGOTE; INFLAMMATORY DISEASE; INTESTINE FLORA; MICROBIAL COMMUNITY; NONHUMAN; POPULATION ABUNDANCE; PREVOTELLACEAE; RNA SEQUENCE; SPECIES COMPOSITION; ADULT; CLASSIFICATION; FEMALE; GENETICS; GENOTYPE; HUMAN; IMMUNOLOGY; MALE; METAGENOME; MIDDLE AGED; PHYLOGENY;

ADULT; AUTOIMMUNITY; BACTERIA; CROSS-SECTIONAL STUDIES; FEMALE; GASTROINTESTINAL MICROBIOME; GENOTYPE; HAPLOTYPES; HISTOCOMPATIBILITY ANTIGENS; HLA-DRB1 CHAINS; HUMANS; MALE; METAGENOME; MIDDLE AGED; PHYLOGENY;

EID: 84941618200     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133804     Document Type: Article

References (50)

1. Horton R, Wilming L, Rand V, Lovering RC, Bruford EA, Khodiyar VK, et al. (2004) Gene map of the extended human MHC. Nat Rev Genet 5: 889-899. PMID: 15573121.
2. Fellay J, Shianna KV, Ge D, Colombo S, Ledergerber B, Weale M, et al. (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317: 944-947. PMID: 17641165.
3. Thorsby E, Lie BA (2005) HLA associated genetic predisposition to autoimmune diseases: Genes involved and possible mechanisms. Transpl Immunol 14: 175-182. PMID: 15982560.
4. Traherne JA (2008) Human MHC architecture and evolution: implications for disease association studies. Int J Immunogenet 35: 179-192. doi:10.1111/j.1744-313X.2008.00765.x PMID: 18397301.
5. Horton R, Gibson R, Coggill P, Miretti M, Allcock RJ, Almeida J, et al. (2008) Variation analysis and gene annotation of eight MHC haplotypes: The MHC Haplotype Project. Immunogenetics 60: 1-18. doi:10.1007/s00251-007-0262-2 PMID: 18193213.
6. Candore G, Lio D, Colonna Romano G, Caruso C (2002) Pathogenesis of autoimmune diseases associated with 8.1 ancestral haplotype: effect of multiple gene interactions. Autoimmun Rev 1: 29-35. PMID: 12849055.
7. Price P, Witt C, Allcock R, Sayer D, Garlepp M, Kok CC, et al. (1999) The genetic basis for the association of the 8.1 ancestral haplotype (A1, B8, DR3) with multiple immunopathological diseases. Immunol Rev 167: 257-274. PMID: 10319267.
8. Morris DL, Taylor KE, Fernando MM, Nititham J, Alarcon-Riquelme ME, Barcellos LF, et al. (2012) Unraveling multiple MHC gene associations with systemic lupus erythematosus: model choice indicates a role for HLA alleles and non-HLA genes in Europeans. Am J Hum Genet 91: 778-793. doi:10.1016/j.ajhg.2012.08.026 PMID: 23084292.
9. Naess S, Lie BA, Melum E, Olsson M, Hov JR, Croucher PJ, et al. (2014) Refinement of the MHC risk map in a scandinavian primary sclerosing cholangitis population. PLoS One 9: e114486. doi:10.1371/journal.pone.0114486 PMID: 25521205.
10. Scher JU, Sczesnak A, Longman RS, Segata N, Ubeda C, Bielski C, et al. (2013) Expansion of intestinal Prevotella copri correlates with enhanced susceptibility to arthritis. Elife 2: e01202doi:10.7554/eLife.01202 PMID: 24192039.
11. Willing BP, Dicksved J, Halfvarson J, Andersson AF, Lucio M, Zheng Z, et al. (2010) A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139: 1844-1854 e1841. doi:10.1053/j.gastro.2010.08.049 PMID: 20816835.
12. Vrieze A, van Nood E, Holleman F, Salojarvi J, Kootte RS, Bartelsman JF, et al. (2012) Transfer of Intestinal Microbiota From Lean Donors Increases Insulin Sensitivity in Subjects With Metabolic Syndrome. Gastroenterology 143: 913-916. doi:10.1053/j.gastro.2012.06.031 PMID: 22728514.
13. David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, et al. (2014) Diet rapidly and reproducibly alters the human gut microbiome. Nature 505: 559-563. doi:10.1038/nature12820 PMID: 24336217.
14. Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. (2014) Human genetics shape the gut microbiome. Cell 159: 789-799doi:10.1016/j.cell.2014.09.053 PMID: 25417156.
15. Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nature reviews Microbiology 9: 279-290doi:10.1038/nrmicro2540 PMID: 21407244.
16. Salzman NH, Hung K, Haribhai D, Chu H, Karlsson-Sjoberg J, Amir E, et al. (2010) Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 11: 76-83doi:10.1038/ni.1825 PMID: 19855381.
17. Suzuki K, Meek B, Doi Y, Muramatsu M, Chiba T, Honjo T, et al. (2004) Aberrant expansion of segmented filamentous bacteria in IgA-deficient gut. Proc Natl Acad Sci U S A 101: 1981-1986. PMID: 14766966.
18. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, et al. (2013) NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest.
19. Rehman A, Sina C, Gavrilova O, Hasler R, Ott S, Baines JF, et al. (2011) Nod2 is essential for temporal development of intestinal microbial communities. Gut 60: 1354-1362. doi:10.1136/gut.2010.216259 PMID: 21421666.
20. Rausch P, Rehman A, Kunzel S, Hasler R, Ott SJ, Schreiber S, et al. (2011) Colonic mucosa-associated microbiota is influenced by an interaction of Crohn disease and FUT2 (Secretor) genotype. Proceedings of the National Academy of Sciences of the United States of America 108: 19030-19035. doi:10.1073/pnas.1106408108 PMID: 22068912.
21. Toivanen P, Vaahtovuo J, Eerola E (2001) Influence of major histocompatibility complex on bacterial composition of fecal flora. Infection and Immunity 69: 2372-2377. PMID: 11254595.
22. Gomez A, Luckey D, Yeoman CJ, Marietta EV, Berg Miller ME, Murray JA, et al. (2012) Loss of sex and age driven differences in the gut microbiome characterize arthritis-susceptible 0401 mice but not arthritis- resistant 0402 mice. PloS one 7: e36095. doi:10.1371/journal.pone.0036095PMID: 22553482.
23. De Palma G, Capilla A, Nadal I, Nova E, Pozo T, Varea V, et al. (2010) Interplay between human leukocyte antigen genes and the microbial colonization process of the newborn intestine. Curr Issues Mol Biol 12: 1-10. PMID: 19478349.
24. Kriegel MA, Sefik E, Hill JA, Wu HJ, Benoist C, Mathis D (2011) Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc Natl Acad Sci U S A 108: 11548-11553. doi:10.1073/pnas.1108924108 PMID: 21709219.
25. Marild K, Ye W, Lebwohl B, Green PH, Blaser MJ, Card T, et al. (2013) Antibiotic exposure and the development of coeliac disease: A nationwide case-control study. BMC Gastroenterol 13: 109. doi:10.1186/1471-230X-13-109 PMID: 23834758.
26. Ahlquist DA, Schwartz S, Isaacson J, Ellefson M (1988) A stool collection device: The first step in occult blood testing. Annals of Internal Medicine 108: 609-612. PMID: 3348567.
27. Wu GD, Lewis JD, Hoffmann C, Chen YY, Knight R, Bittinger K, et al. (2010) Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC microbiology 10: 206. doi:10.1186/1471-2180-10-206 PMID: 20673359.
28. Henderson G, Cox F, Kittelmann S, Miri VH, Zethof M, Noel SJ, et al. (2013) Effect of DNA extraction methods and sampling techniques on the apparent structure of cow and sheep rumen microbial communities. PLoS One 8: e74787. doi:10.1371/journal.pone.0074787 PMID: 24040342.
29. Jumpstart Consortium Human Microbiome Project Data Generation Working G (2012) Evaluation of 16S rDNA-based community profiling for human microbiome research. PLoS One 7: e39315. doi:10.1371/journal.pone.0039315 PMID: 22720093.
30. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75: 7537-7541. doi:10.1128/AEM.01541-09 PMID: 19801464.
31. Quince C, Lanzen A, Davenport RJ, Turnbaugh PJ (2011) Removing noise from pyrosequenced amplicons. BMC Bioinformatics 12: 38. doi:10.1186/1471-2105-12-38 PMID: 21276213.
32. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200. doi:10.1093/bioinformatics/btr381 PMID: 21700674.
33. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nature methods 7: 335-336. doi:10.1038/nmeth.f.303 PMID: 20383131.
34. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180. doi:10.1038/nature09944 PMID: 21508958.
35. Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. (2012) A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490: 55-60. doi:10.1038/nature11450 PMID: 23023125.
36. The Human Microbiome Project Consortium (2012) Structure, function and diversity of the healthy human microbiome. Nature 486: 207-214. doi:10.1038/nature11234 PMID: 22699609.
37. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, Mende DR, et al. (2014) Addendum: Enterotypes of the human gut microbiome. Nature 506: 516.
38. Goyette P, Boucher G, Mallon D, Ellinghaus E, Jostins L, Huang H, et al. (2015) High-density mapping of the MHC identifies a shared role for HLA-DRB1∗01:03 in inflammatory bowel diseases and heterozygous advantage in ulcerative colitis. Nat Genet.
39. Palma GD, Capilla A, Nova E, Castillejo G, Varea V, Pozo T, et al. (2012) Influence of milk-feeding type and genetic risk of developing coeliac disease on intestinal microbiota of infants: The PROFICEL study. PLoS One 7: e30791. doi:10.1371/journal.pone.0030791 PMID: 22319588.
40. Olivares M, Neef A, Castillejo G, Palma GD, Varea V, Capilla A, et al. (2014) The HLA-DQ2 genotype selects for early intestinal microbiota composition in infants at high risk of developing coeliac disease. Gut.
41. Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vazquez-Baeza Y, et al. (2013) Meta-analyses of studies of the human microbiota. Genome Res 23: 1704-1714. doi:10.1101/gr.151803.112 PMID: 23861384.
42. Nava GM, Friedrichsen HJ, Stappenbeck TS (2011) Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 5: 627-638. doi:10.1038/ismej.2010.161 PMID: 20981114.
43. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139: 485-498. doi:10.1016/j.cell.2009.09.033 PMID: 19836068.
44. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. (2011) Induction of colonic regulatory T cells by indigenous Clostridium species. Science 331: 337-341. doi:10.1126/science.1198469 PMID: 21205640.
45. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, et al. (2014) The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15: 382-392. doi:10.1016/j.chom.2014.02.005 PMID: 24629344.
46. La Rosa PS, Brooks JP, Deych E, Boone EL, Edwards DJ, Wang Q, et al. (2012) Hypothesis testing and power calculations for taxonomic-based human microbiome data. PLoS One 7: e52078doi:10.1371/journal.pone.0052078 PMID: 23284876.
47. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. (2009) A core gut microbiome in obese and lean twins. Nature 457: 480-484. doi:10.1038/nature07540 PMID: 19043404.
48. Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, Falony G, et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500: 541-546. doi:10.1038/nature12506 PMID: 23985870.
49. Atarashi K, Tanoue T, Oshima K, Suda W, Nagano Y, Nishikawa H, et al. (2013) Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500: 232-236. doi:10.1038/nature12331 PMID: 23842501.
50. Geiger TL, Tauro S (2012) Nature and nurture in Foxp3(+) regulatory T cell development, stability, and function. Hum Immunol 73: 232-239. doi:10.1016/j.humimm.2011.12.012 PMID: 22240298.