The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes

Cell Host and Microbe

Volumn 17, Issue 2, 2015, Pages 260-273

  Kostic, Aleksandar D ^a,b,c   Gevers, Dirk ^a   Siljander, Heli ^d   Vatanen, Tommi ^a,e   Hyötyläinen, Tuulia ^f,i   Hämäläinen, Anu Maaria ^g   Peet, Aleksandr ^h   Tillmann, Vallo ^h   Pöhö, Päivi ^d,i   Mattila, Ismo ^f,i   Lähdesmäki, Harri ^e   Franzosa, Eric A ^c   Vaarala, Outi ^d   De Goffau, Marcus ^j   Harmsen, Hermie ^j   Ilonen, Jorma ^k,l   Virtanen, Suvi M ^m,n,o   Clish, Clary B ^a   Orešič, Matej ^f,i   Huttenhower, Curtis ^a,c   Knip, Mikael ^d,p,q   Xavier, Ramnik J ^a,b,r   more..

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF HELSINKI   (Finland)

^e AALTO UNIVERSITY   (Finland)

^f STENO DIABETES CENTER   (Denmark)

^g JORVI HOSPITAL   (Finland)

^h UNIVERSITY OF TARTU   (Estonia)

ⁱ VTT TECHNICAL RESEARCH CENTRE OF FINLAND   (Finland)

^j UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^k UNIVERSITY OF TURKU   (Finland)

^l UNIVERSITY OF EASTERN FINLAND   (Finland)

^m NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

ⁿ TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^o PIRKANMAA HOSPITAL DISTRICT   (Finland)

^p FOLKHÄLSAN RESEARCH CENTER   (Finland)

^q TAMPERE UNIVERSITY HOSPITAL   (Finland)

^r Massachusetts Institute of Technology Cambridge   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; DNA 16S; GALACTOSE; GLUCOSE; MANNOSE; XYLOSE;

ACIDAMINOCOCCACEAE; ARTICLE; BACTEROIDES; BLAUTIA; CESAREAN SECTION; CHILD DEVELOPMENT; CLADISTICS; COMMENSAL; CONTROLLED STUDY; DIET; DISEASE COURSE; ENVIRONMENTAL FACTOR; ESTONIA; FINLAND; GENE FUNCTION; GENOTYPE; GLYCEMIC CONTROL; HLA SYSTEM; HUMAN; INFANT; INSULIN DEPENDENT DIABETES MELLITUS; INTESTINE FLORA; LACHNOSPIRACEAE; LIPIDOMICS; METABOLOMICS; METAGENOMICS; MICROBIAL COMMUNITY; MICROBIAL GENE; NONHUMAN; PATHOGENESIS; PHYLOGENY; PRIORITY JOURNAL; RUMINOCOCCUS; SEROCONVERSION; STREPTOCOCCUS; COHORT ANALYSIS; GASTROINTESTINAL TRACT; MICROBIOLOGY;

COHORT STUDIES; DIABETES MELLITUS, TYPE 1; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; INFANT;

EID: 84922941772     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.01.001     Document Type: Article

References (53)

1. K. Aagaard, J. Ma, K.M. Antony, R. Ganu, J. Petrosino, and J. Versalovic The placenta harbors a unique microbiome Sci. Transl. Med. 6 2014 237ra65
2. S. Abubucker, N. Segata, J. Goll, A.M. Schubert, J. Izard, B.L. Cantarel, B. Rodriguez-Mueller, J. Zucker, M. Thiagarajan, and B. Henrissat Metabolic reconstruction for metagenomic data and its application to the human microbiome PLoS Comput. Biol. 8 2012 e1002358
3. P. Achenbach, E. Bonifacio, K. Koczwara, and A.-G. Ziegler Natural history of type 1 diabetes Diabetes 54 Suppl 2 2005 S25 S31
4. L.M. Alcantara, N.E. Silveira, J.R. Dantas, P.B. Araujo, M.M. de Oliveira, A. Milech, L. Zajdenverg, M. Rodacki, and J.E. de Oliveira Low triglyceride levels are associated with a better metabolic control in patients with type 1 diabetes Diabetol. Metab. Syndr. 3 2011 22
5. D. An, S.F. Oh, T. Olszak, J.F. Neves, F.Y. Avci, D. Ertürk-Hasdemir, X. Lu, S. Zeissig, R.S. Blumberg, and D.L. Kasper Sphingolipids from a symbiotic microbe regulate homeostasis of host intestinal natural killer T cells Cell 156 2014 123 133
6. C.T. Brown, A.G. Davis-Richardson, A. Giongo, K.A. Gano, D.B. Crabb, N. Mukherjee, G. Casella, J.C. Drew, J. Ilonen, and M. Knip Gut microbiome metagenomics analysis suggests a functional model for the development of autoimmunity for type 1 diabetes PLoS ONE 6 2011 e25792
7. J. Cahenzli, Y. Köller, M. Wyss, M.B. Geuking, and K.D. McCoy Intestinal microbial diversity during early-life colonization shapes long-term IgE levels Cell Host Microbe 14 2013 559 570
8. J.G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F.D. Bushman, E.K. Costello, N. Fierer, A.G. Peña, J.K. Goodrich, and J.I. Gordon QIIME allows analysis of high-throughput community sequencing data Nat. Methods 7 2010 335 336
9. J.G. Caporaso, C.L. Lauber, W.A. Walters, D. Berg-Lyons, J. Huntley, N. Fierer, S.M. Owens, J. Betley, L. Fraser, and M. Bauer Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms ISME J. 6 2012 1621 1624
10. J.Y. Chang, D.A. Antonopoulos, A. Kalra, A. Tonelli, W.T. Khalife, T.M. Schmidt, and V.B. Young Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea J. Infect. Dis. 197 2008 435 438
11. I. Cho, S. Yamanishi, L. Cox, B.A. Methé, J. Zavadil, K. Li, Z. Gao, D. Mahana, K. Raju, and I. Teitler Antibiotics in early life alter the murine colonic microbiome and adiposity Nature 488 2012 621 626
12. J. Chow, and S.K. Mazmanian Getting the bugs out of the immune system: do bacterial microbiota "fix" intestinal T cell responses? Cell Host Microbe 5 2009 8 12
13. L.M. Cox, S. Yamanishi, J. Sohn, A.V. Alekseyenko, J.M. Leung, I. Cho, S.G. Kim, H. Li, Z. Gao, and D. Mahana Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences Cell 158 2014 705 721
14. M. Da Silva, G.K. Jaggers, S.V. Verstraeten, A.G. Erlejman, C.G. Fraga, and P.I. Oteiza Large procyanidins prevent bile-acid-induced oxidant production and membrane-initiated ERK1/2, p38, and Akt activation in Caco-2 cells Free Radic. Biol. Med. 52 2012 151 159
15. M.C. de Goffau, K. Luopajärvi, M. Knip, J. Ilonen, T. Ruohtula, T. Härkönen, L. Orivuori, S. Hakala, G.W. Welling, H.J. Harmsen, and O. Vaarala Fecal microbiota composition differs between children with β-cell autoimmunity and those without Diabetes 62 2013 1238 1244
16. M.G. Dominguez-Bello, E.K. Costello, M. Contreras, M. Magris, G. Hidalgo, N. Fierer, and R. Knight Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns Proc. Natl. Acad. Sci. USA 107 2010 11971 11975
17. J.J. Faith, J.L. Guruge, M. Charbonneau, S. Subramanian, H. Seedorf, A.L. Goodman, J.C. Clemente, R. Knight, A.C. Heath, and R.L. Leibel The long-term stability of the human gut microbiota Science 341 2013 1237439
18. K. Faust, J.F. Sathirapongsasuti, J. Izard, N. Segata, D. Gevers, J. Raes, and C. Huttenhower Microbial co-occurrence relationships in the human microbiome PLoS Comput. Biol. 8 2012 e1002606
19. D. Gevers, S. Kugathasan, L.A. Denson, Y. Vázquez-Baeza, W. Van Treuren, B. Ren, E. Schwager, D. Knights, S.J. Song, and M. Yassour The treatment-naive microbiome in new-onset Crohn's disease Cell Host Microbe 15 2014 382 392
20. A. Giongo, K.A. Gano, D.B. Crabb, N. Mukherjee, L.L. Novelo, G. Casella, J.C. Drew, J. Ilonen, M. Knip, and H. Hyöty Toward defining the autoimmune microbiome for type 1 diabetes ISME J. 5 2011 82 91
21. V. Harjutsalo, L. Sjöberg, and J. Tuomilehto Time trends in the incidence of type 1 diabetes in Finnish children: a cohort study Lancet 371 2008 1777 1782
22. V. Harjutsalo, R. Sund, M. Knip, and P.-H. Groop Incidence of type 1 diabetes in Finland JAMA 310 2013 427 428
23. Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome Nature 486 2012 207 214
24. N. Kapel, P. Matarazzo, D. Haouchine, N. Abiola, S. Guérin, D. Magne, J.G. Gobert, and C. Dupont Fecal tumor necrosis factor alpha, eosinophil cationic protein and IgE levels in infants with cow's milk allergy and gastrointestinal manifestations Clin. Chem. Lab. Med. 37 1999 29 32
25. M. Knip, R. Veijola, S.M. Virtanen, H. Hyöty, O. Vaarala, and H.K. Akerblom Environmental triggers and determinants of type 1 diabetes Diabetes 54 Suppl 2 2005 S125 S136
26. M. Knip, S. Korhonen, P. Kulmala, R. Veijola, A. Reunanen, O.T. Raitakari, J. Viikari, and H.K. Akerblom Prediction of type 1 diabetes in the general population Diabetes Care 33 2010 1206 1212
27. J.E. Koenig, A. Spor, N. Scalfone, A.D. Fricker, J. Stombaugh, R. Knight, L.T. Angenent, and R.E. Ley Succession of microbial consortia in the developing infant gut microbiome Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4578 4585
28. R.A. Koeth, Z. Wang, B.S. Levison, J.A. Buffa, E. Org, B.T. Sheehy, E.B. Britt, X. Fu, Y. Wu, and L. Li Intestinal microbiota metabolism of L-carnitine, a nutrient in red meat, promotes atherosclerosis Nat. Med. 19 2013 576 585
29. M.G.I. Langille, J. Zaneveld, J.G. Caporaso, D. McDonald, D. Knights, J.A. Reyes, J.C. Clemente, D.E. Burkepile, R.L. Vega Thurber, and R. Knight Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences Nat. Biotechnol. 31 2013 814 821
30. D.K. Lee, S.Y. Park, S.K. Baik, S.O. Kwon, J.M. Chung, E.-S. Oh, and H.S. Kim [Deoxycholic acid-induced signal transduction in HT-29 cells: role of NF-kappa B and interleukin-8] Korean J. Gastroenterol. 43 2004 176 185
31. C. Manichanh, N. Borruel, F. Casellas, and F. Guarner The gut microbiota in IBD Nat. Rev. Gastroenterol. Hepatol. 9 2012 599 608
32. T. Mochida, T. Tanaka, Y. Shiraki, H. Tajiri, S. Matsumoto, K. Shimbo, T. Ando, K. Nakamura, M. Okamoto, and F. Endo Time-dependent changes in the plasma amino acid concentration in diabetes mellitus Mol. Genet. Metab. 103 2011 406 409
33. X.C. Morgan, T.L. Tickle, H. Sokol, D. Gevers, K.L. Devaney, D.V. Ward, J.A. Reyes, S.A. Shah, N. LeLeiko, and S.B. Snapper Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment Genome Biol. 13 2012 R79
34. M. Mühlbauer, B. Allard, A.K. Bosserhoff, S. Kiessling, H. Herfarth, G. Rogler, J. Schölmerich, C. Jobin, and C. Hellerbrand Differential effects of deoxycholic acid and taurodeoxycholic acid on NF-kappa B signal transduction and IL-8 gene expression in colonic epithelial cells Am. J. Physiol. Gastrointest. Liver Physiol. 286 2004 G1000 G1008
35. D.A. O'Neil, E.M. Porter, D. Elewaut, G.M. Anderson, L. Eckmann, T. Ganz, and M.F. Kagnoff Expression and regulation of the human beta-defensins hBD-1 and hBD-2 in intestinal epithelium J. Immunol. 163 1999 6718 6724
36. M. Orešič, S. Simell, M. Sysi-Aho, K. Näntö-Salonen, T. Seppänen-Laakso, V. Parikka, M. Katajamaa, A. Hekkala, I. Mattila, and P. Keskinen Dysregulation of lipid and amino acid metabolism precedes islet autoimmunity in children who later progress to type 1 diabetes J. Exp. Med. 205 2008 2975 2984
37. C. Palmer, E.M. Bik, D.B. DiGiulio, D.A. Relman, and P.O. Brown Development of the human infant intestinal microbiota PLoS Biol. 5 2007 e177
38. C.M. Payne, C. Weber, C. Crowley-Skillicorn, K. Dvorak, H. Bernstein, C. Bernstein, H. Holubec, B. Dvorakova, and H. Garewal Deoxycholate induces mitochondrial oxidative stress and activates NF-kappaB through multiple mechanisms in HCT-116 colon epithelial cells Carcinogenesis 28 2007 215 222
39. M. Sailer, C. Dahlhoff, P. Giesbertz, M.K. Eidens, N. de Wit, I. Rubio-Aliaga, M.V. Boekschoten, M. Müller, and H. Daniel Increased plasma citrulline in mice marks diet-induced obesity and may predict the development of the metabolic syndrome PLoS ONE 8 2013 e63950
40. C.L. Sears, and W.S. Garrett Microbes, microbiota, and colon cancer Cell Host Microbe 15 2014 317 328
41. N. Segata, L. Waldron, A. Ballarini, V. Narasimhan, O. Jousson, and C. Huttenhower Metagenomic microbial community profiling using unique clade-specific marker genes Nat. Methods 9 2012 811 814
42. P.M. Smith, M.R. Howitt, N. Panikov, M. Michaud, C.A. Gallini, M. Bohlooly-Y, J.N. Glickman, and W.S. Garrett The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis Science 341 2013 569 573
43. S. Subramanian, S. Huq, T. Yatsunenko, R. Haque, M. Mahfuz, M.A. Alam, A. Benezra, J. DeStefano, M.F. Meier, and B.D. Muegge Persistent gut microbiota immaturity in malnourished Bangladeshi children Nature 510 2014 417 421
44. P.J. Turnbaugh, M. Hamady, T. Yatsunenko, B.L. Cantarel, A. Duncan, R.E. Ley, M.L. Sogin, W.J. Jones, B.A. Roe, and J.P. Affourtit A core gut microbiome in obese and lean twins Nature 457 2009 480 484
45. O. Vaarala, M.A. Atkinson, and J. Neu The "perfect storm" for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity Diabetes 57 2008 2555 2562
46. P. Vannini, G. Marchesini, G. Forlani, A. Angiolini, A. Ciavarella, M. Zoli, and E. Pisi Branched-chain amino acids and alanine as indices of the metabolic control in type 1 (insulin-dependent) and type 2 (non-insulin-dependent) diabetic patients Diabetologia 22 1982 217 219
47. V.R. Velagapudi, R. Hezaveh, C.S. Reigstad, P. Gopalacharyulu, L. Yetukuri, S. Islam, J. Felin, R. Perkins, J. Borén, M. Oresic, and F. Bäckhed The gut microbiota modulates host energy and lipid metabolism in mice J. Lipid Res. 51 2010 1101 1112
48. B. Vergès Lipid disorders in type 1 diabetes Diabetes Metab. 35 2009 353 360
49. Z. Wang, E. Klipfell, B.J. Bennett, R. Koeth, B.S. Levison, B. Dugar, A.E. Feldstein, E.B. Britt, X. Fu, and Y.-M. Chung Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease Nature 472 2011 57 63
50. J. Wehkamp, M. Schmid, K. Fellermann, and E.F. Stange Defensin deficiency, intestinal microbes, and the clinical phenotypes of Crohn's disease J. Leukoc. Biol. 77 2005 460 465
51. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, A.C. Stonebraker, C. Hu, F.S. Wong, G.L. Szot, and J.A. Bluestone Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
52. T. Yatsunenko, F.E. Rey, M.J. Manary, I. Trehan, M.G. Dominguez-Bello, M. Contreras, M. Magris, G. Hidalgo, R.N. Baldassano, and A.P. Anokhin Human gut microbiome viewed across age and geography Nature 486 2012 222 227
53. A.G. Ziegler, M. Rewers, O. Simell, T. Simell, J. Lempainen, A. Steck, C. Winkler, J. Ilonen, R. Veijola, and M. Knip Seroconversion to multiple islet autoantibodies and risk of progression to diabetes in children JAMA 309 2013 2473 2479