Early microbes modify immune system development and metabolic homeostasis-the "Restaurant" hypothesis revisited

Frontiers in Endocrinology

Volumn 8, Issue DEC, 2017, Pages

  Nash, Michael J ^a   Frank, Daniel N ^b   Friedman, Jacob E ^a,c  

^a University of Colorado Denver and Children s Hospital Colorado   (United States)

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

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

Innate immunity; Microbiome; Non alcoholic fatty liver disease; Pregnancy; Proteobacteria

Indexed keywords

CELL PROLIFERATION; CHEMOTAXIS; DYSBIOSIS; GENE EXPRESSION; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; INTESTINE FLORA; MATERNAL OBESITY; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; NONALCOHOLIC FATTY LIVER; NONHUMAN; SHORT SURVEY;

EID: 85037824673     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2017.00349     Document Type: Short Survey

References (76)

1. Russell SL, Gold MJ, Hartmann M, Willing BP, Thorson L, Wlodarska M, et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep (2012) 13:440-7. doi:10.1038/embor.2012.32
2. Ma J, Prince AL, Bader D, Hu M, Ganu R, Baquero K, et al. High-fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nat Commun (2014) 5:3889. doi:10.1038/ncomms4889
3. Dabelea D, Hanson RL, Lindsay RS, Pettitt DJ, Imperatore G, Gabir MM, et al. Intrauterine exposure to diabetes conveys risks for type 2 diabetes and obesity: a study of discordant sibships. Diabetes (2000) 49:2208-11. doi:10.2337/diabetes.49.12.2208
4. Friedman JE. Obesity and gestational diabetes mellitus pathways for programming in mouse, monkey, and man-where do we go next? The 2014 Norbert Freinkel award lecture. Diabetes Care (2015) 38:1402-11. doi:10.2337/dc15-0628
5. Derraik JG, Ahlsson F, Diderholm B, Lundgren M. Obesity rates in two generations of Swedish women entering pregnancy, and associated obesity risk among adult daughters. Sci Rep (2015) 5:16692. doi:10.1038/srep16692
6. Arrieta MC, Stiemsma LT, Dimitriu PA, Thorson L, Russell S, Yurist-Doutsch S, et al. Early infancy microbial and metabolic alterations affect risk of childhood asthma. Sci Transl Med (2015) 7:307ra152. doi:10.1126/scitranslmed.aab2271
7. Cho I, Yamanishi S, Cox L, Methe BA, Zavadil J, Li K, et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature (2012) 488:621-6. doi:10.1038/nature11400
8. Vijay-Kumar M, Aitken JD, Carvalho FA, Cullender TC, Mwangi S, Srinivasan S, et al. Metabolic syndrome and altered gut microbiota in mice lacking toll-like receptor 5. Science (2010) 328:228-31. doi:10.1126/science.1179721
9. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature (2008) 455:1109-13. doi:10.1038/nature07336
10. Perry RJ, Peng L, Barry NA, Cline GW, Zhang D, Cardone RL, et al. Acetate mediates a microbiome-brain-beta-cell axis to promote metabolic syndrome. Nature (2016) 534:213-7. doi:10.1038/nature18309
11. Ellekilde M, Selfjord E, Larsen CS, Jakesevic M, Rune I, Tranberg B, et al. Transfer of gut microbiota from lean and obese mice to antibiotic-treated mice. Sci Rep (2014) 4:5922. doi:10.1038/srep05922
12. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science (2013) 341:1241214. doi:10.1126/science.1241214
13. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature (2006) 444:1027-31. doi:10.1038/nature05414
14. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A (2005) 102:11070-5. doi:10.1073/pnas.0504978102
15. Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature (2006) 444:1022-3. doi:10.1038/4441022a
16. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med (2009) 1:6ra14. doi:10.1126/scitranslmed.3000322
17. Khosravi A, Yáñez A, Price JG, Chow A, Merad M, Goodridge HS, et al. Gut microbiota promotes hematopoiesis tocontrol bacterial infection. Cell Host Microbe (2014) 15:374-81. doi:10.1016/j.chom.2014.02.006
18. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J. The placenta harbors a unique microbiome. Sci Transl Med (2014) 6:237ra65. doi:10.1126/scitranslmed.3008599
19. DiGiulio DB, Romero R, Amogan HP, Kusanovic JP, Bik EM, Gotsch F, et al. Microbial prevalence, diversity and abundance in amniotic fluid during preterm labor: a molecular and culture-based investigation. PLoS One (2008) 3:e3056. doi:10.1371/journal.pone.0003056
20. Ardissone AN, de la Cruz DM, Davis-Richardson AG, Rechcigl KT, Li N, Drew JC, et al. Meconium microbiome analysis identifies bacteria correlated with premature birth. PLoS One (2014) 9:e90784. doi:10.1371/journal.pone.0090784
21. Brumbaugh DE, Arruda J, Robbins K, Ir D, Santorico SA, Robertson CE, et al. Mode of delivery determines neonatal pharyngeal bacterial composition and early intestinal colonization. J Pediatr Gastroenterol Nutr (2016) 63:320-8. doi:10.1097/MPG.0000000000001124
22. Perez-Muñoz ME, Arrieta MC, Ramer-Tait AE, Walter J. A critical assessment of the 'sterile womb' and 'in utero colonization' hypotheses: implications for research on the pioneer infant microbiome. Microbiome (2017) 5:48. doi:10.1186/s40168-017-0268-4
23. Leatham-Jensen MP, Frimodt-Moller J, Adediran J, Mokszycki ME, Banner ME, Caughron JE, et al. The streptomycin-treated mouse intestine selects Escherichia coli envZ missense mutants that interact with dense and diverse intestinal microbiota. Infect Immun (2012) 80:1716-27. doi:10.1128/IAI.06193-11
24. Conway T, Cohen PS. Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol Spectr (2015) 3. doi:10.1128/microbiolspec.MBP-0006-2014
25. Freter R, Brickner H, Fekete J, Vickerman MM, Carey KE. Survival and implantation of Escherichia coli in the intestinal tract. Infect Immun (1983) 39:686-703
26. Bäckhed F, Roswall J, Peng Y, Feng Q, Jia H, Kovatcheva-Datchary P, et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe (2015) 17:690-703. doi:10.1016/j.chom.2015.04.004
27. Bradley PH, Pollard KS. Proteobacteria explain significant functional variability in the human gut microbiome. Microbiome (2017) 5:36. doi:10.1186/s40168-017-0244-z
28. Cahenzli J, Koller Y, Wyss M, Geuking MB, McCoy KD. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe (2013) 14:559-70. doi:10.1016/j.chom.2013.10.004
29. Bokulich NA, Chung J, Battaglia T, Henderson N, Jay M, Li H, et al. Antibiotics, birth mode, and diet shape microbiome maturation during early life. Sci Transl Med (2016) 8:343ra82. doi:10.1126/scitranslmed.aad7121
30. Chu DM, Antony KM, Ma J, Prince AL, Showalter L, Moller M, et al. The early infant gut microbiome varies in association with a maternal high-fat diet. Genome Med (2016) 8:77. doi:10.1186/s13073-016-0330-z
31. Myles IA, Fontecilla NM, Janelsins BM, Vithayathil PJ, Segre JA, Datta SK. Parental dietary fat intake alters offspring microbiome and immunity. J Immunol (2013) 191:3200-9. doi:10.4049/jimmunol.1301057
32. Thompson JR, Valleau JC, Barling AN, Franco JG, DeCapo M, Bagley JL, et al. Exposure to a high-fat diet during early development programs behavior and impairs the central serotonergic system in juvenile non-human primates. Front Endocrinol (2017) 8:164. doi:10.3389/fendo.2017.00164
33. Lemas DJ, Young BE, Baker PR II, Tomczik AC, Soderborg TK, Hernandez TL, et al. Alterations in human milk leptin and insulin are associated with early changes in the infant intestinal microbiome. Am J Clin Nutr (2016) 103:1291-300. doi:10.3945/ajcn.115.126375
34. Mueller NT, Shin H, Pizoni A, Werlang IC, Matte U, Goldani MZ, et al. Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci Rep (2016) 6:23133. doi:10.1038/srep23133
35. Cerdo T, Ruiz A, Jauregui R, Azaryah H, Torres-Espinola FJ, Garcia-Valdes L, et al. Maternal obesity is associated with gut microbial metabolic potential in offspring during infancy. J Physiol Biochem (2017). doi:10.1007/s13105-017-0577-x
36. Galley JD, Bailey M, Kamp Dush C, Schoppe-Sullivan S, Christian LM. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS One (2014) 9:e113026. doi:10.1371/journal.pone.0113026
37. De Leoz ML, Kalanetra KM, Bokulich NA, Strum JS, Underwood MA, German JB, et al. Human milk glycomics and gut microbial genomics in infant feces show a correlation between human milk oligosaccharides and gut microbiota: a proof-of-concept study. J Proteome Res (2015) 14:491-502. doi:10.1021/pr500759e
38. Mirpuri J, Raetz M, Sturge CR, Wilhelm CL, Benson A, Savani RC, et al. Proteobacteria-specific IgA regulates maturation of the intestinal microbiota. Gut Microbes (2014) 5:28-39. doi:10.4161/gmic.26489
39. Yuan C, Gaskins AJ, Blaine AI, Zhang C, Gillman MW, Missmer SA, et al. Association between cesarean birth and risk of obesity in offspring in childhood, adolescence, and early adulthood. JAMA Pediatr (2016) 170:e162385. doi:10.1001/jamapediatrics.2016.2385
40. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell (2014) 158:705-21. doi:10.1016/j.cell.2014.05.052
41. O'Sullivan A, He X, McNiven EM, Haggarty NW, Lonnerdal B, Slupsky CM. Early diet impacts infant rhesus gut microbiome, immunity, and metabolism. J Proteome Res (2013) 12:2833-45. doi:10.1021/pr4001702
42. O'Sullivan A, Farver M, Smilowitz JT. The influence of early infant-feeding practices on the intestinal microbiome and body composition in infants. Nutr Metab Insights (2015) 8:1-9. doi:10.4137/NMI.S29530
43. Madan JC, Hoen AG, Lundgren SN, Farzan SF, Cottingham KL, Morrison HG, et al. Association of cesarean delivery and formula supplementation with the intestinal microbiome of 6-week-old infants. JAMA Pediatr (2016) 170:212-9. doi:10.1001/jamapediatrics.2015.3732
44. Cabrera-Rubio R, Collado MC, Laitinen K, Salminen S, Isolauri E, Mira A. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am J Clin Nutr (2012) 96:544-51. doi:10.3945/ajcn.112.037382
45. Luo Y, Chen GL, Hannemann N, Ipseiz N, Kronke G, Bauerle T, et al. Microbiota from obese mice regulate hematopoietic stem cell differentiation by altering the bone niche. Cell Metab (2015) 22:886-94. doi:10.1016/j.cmet.2015.08.020
46. Sureshchandra S, Wilson RM, Rais M, Marshall NE, Purnell JQ, Thornburg KL, et al. Maternal pregravid obesity remodels the DNA methylation landscape of cord blood monocytes disrupting their inflammatory program. J Immunol (2017) 199:2729-44. doi:10.4049/jimmunol.1700434
47. Park J, Kim M, Kang SG, Jannasch AH, Cooper B, Patterson J, et al. Short chain fatty acids induce both effector and regulatory T cells by suppression of histone deacetylases and regulation of the mTOR-S6K pathway. Mucosal Immunol (2015) 8:80-93. doi:10.1038/mi.2014.44
48. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci U S A (2014) 111:2247-52. doi:10.1073/pnas.1322269111
49. Vinolo MA, Rodrigues HG, Hatanaka E, Hebeda CB, Farsky SH, Curi R. Short-chain fatty acids stimulate the migration of neutrophils to inflammatory sites. Clin Sci (Lond) (2009) 117:331-8. doi:10.1042/CS20080642
50. Thorburn AN, McKenzie CI, Shen S, Stanley D, Macia L, Mason LJ, et al. Evidence that asthma is a developmental origin disease influenced by maternal diet and bacterial metabolites. Nat Commun (2015) 6:7320. doi:10.1038/ncomms8320
51. Macpherson AJ, de Aguero MG, Ganal-Vonarburg SC. How nutrition and the maternal microbiota shape the neonatal immune system. Nat Rev Immunol (2017) 17:508-17. doi:10.1038/nri.2017.58
52. Thaiss CA, Zmora N, Levy M, Elinav E. The microbiome and innate immunity. Nature (2016) 535:65-74. doi:10.1038/nature18847
53. Lotz M, Gutle D, Walther S, Menard S, Bogdan C, Hornef MW. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J Exp Med (2006) 203:973-84. doi:10.1084/jem.20050625
54. Gomez de Aguero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y, Li H, et al. The maternal microbiota drives early postnatal innate immune development. Science (2016) 351:1296-302. doi:10.1126/science.aad2571
55. Kamimae-Lanning AN, Krasnow SM, Goloviznina NA, Zhu X, Roth-Carter QR, Levasseur PR, et al. Maternal high-fat diet and obesity compromise fetal hematopoiesis. Mol Metab (2015) 4:25-38. doi:10.1016/j.molmet.2014.11.001
56. Wieland A, Frank DN, Harnke B, Bambha K. Systematic review: microbial dysbiosis and nonalcoholic fatty liver disease. Aliment Pharmacol Ther (2015) 42:1051-63. doi:10.1111/apt.13376
57. Boursier J, Mueller O, Barret M, Machado M, Fizanne L, Araujo-Perez F, et al. The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota. Hepatology (2016) 63:764-75. doi:10.1002/hep.28356
58. Schnabl B, Brenner DA. Interactions between the intestinal microbiome and liver diseases. Gastroenterology (2014) 146:1513-24. doi:10.1053/j.gastro.2014.01.020
59. Cholankeril G, Perumpail RB, Pham EA, Ahmed A, Harrison SA. Nonalcoholic fatty liver disease: epidemiology, natural history, and diagnostic challenges. Hepatology (2016) 64:954. doi:10.1002/hep.28719
60. Anderson EL, Howe LD, Jones HE, Higgins JP, Lawlor DA, Fraser A. The Prevalence of non-alcoholic fatty liver disease in children and adolescents: a systematic review and meta-analysis. PLoS One (2015) 10:e0140908. doi:10.1371/journal.pone.0140908
61. Goyal NP, Schwimmer JB. The progression and natural history of pediatric nonalcoholic fatty liver disease. Clin Liver Dis (2016) 20:325-38. doi:10.1016/j.cld.2015.10.003
62. Brumbaugh DE, Friedman JE. Developmental origins of nonalcoholic fatty liver disease. Pediatr Res (2014) 75:140-7. doi:10.1038/pr.2013.193
63. Mittal S, El-Serag HB, Sada YH, Kanwal F, Duan Z, Temple S, et al. Hepatocellular carcinoma in the absence of cirrhosis in United States veterans is associated with nonalcoholic fatty liver disease. Clin Gastroenterol Hepatol (2016) 14:124-31.e1. doi:10.1016/j.cgh.2015.07.019
64. Ayonrinde OT, Oddy WH, Adams LA, Mori TA, Beilin LJ, de Klerk N, et al. Infant nutrition and maternal obesity influence the risk of non-alcoholic fatty liver disease in adolescents. J Hepatol (2017) 67(3):568-76. doi:10.1016/j.jhep.2017.03.029
65. Nobili V, Alkhouri N, Alisi A, Della Corte C, Fitzpatrick E, Raponi M, et al. Nonalcoholic fatty liver disease: a challenge for pediatricians. JAMA Pediatr (2015) 169:170-6. doi:10.1001/jamapediatrics.2014.2702
66. Brumbaugh DE, Tearse P, Cree-Green M, Fenton LZ, Brown M, Scherzinger A, et al. Intrahepatic fat is increased in the neonatal offspring of obese women with gestational diabetes. J Pediatr (2013) 162:930-6.e1. doi:10.1016/j.jpeds.2012.11.017
67. Modi N, Murgasova D, Ruager-Martin R, Thomas EL, Hyde MJ, Gale C, et al. The influence of maternal body mass index on infant adiposity and hepatic lipid content. Pediatr Res (2011) 70:287-91. doi:10.1203/PDR.0b013e318225f9b1
68. Wesolowski SR, Hay WW Jr. Role of placental insufficiency and intrauterine growth restriction on the activation of fetal hepatic glucose production. Mol Cell Endocrinol (2016) 435:61-8. doi:10.1016/j.mce.2015.12.016
69. Wankhade UD, Zhong Y, Kang P, Alfaro M, Chintapalli SV, Thakali KM, et al. Enhanced offspring predisposition to steatohepatitis with maternal high-fat diet is associated with epigenetic and microbiome alterations. PLoS One (2017) 12:e0175675. doi:10.1371/journal.pone.0175675
70. Zhou D, Pan Q, Shen F, Cao HX, Ding WJ, Chen YW, et al. Total fecal microbiota transplantation alleviates high-fat diet-induced steatohepatitis in mice via beneficial regulation of gut microbiota. Sci Rep (2017) 7:1529. doi:10.1038/s41598-017-01751-y
71. Kim DH, Kim H, Jeong D, Kang IB, Chon JW, Kim HS, et al. Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: targeted and untargeted community analysis with correlation of biomarkers. J Nutr Biochem (2017) 44:35-43. doi:10.1016/j.jnutbio.2017.02.014
72. Xue L, He J, Gao N, Lu X, Li M, Wu X, et al. Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia. Sci Rep (2017) 7:45176. doi:10.1038/srep45176
73. Lelouvier B, Servant F, Paisse S, Brunet AC, Benyahya S, Serino M, et al. Changes in blood microbiota profiles associated with liver fibrosis in obese patients: a pilot analysis. Hepatology (2016) 64:2015-27. doi:10.1002/hep.28829
74. Hamilton MK, Ronveaux CC, Rust BM, Newman JW, Hawley M, Barile D, et al. Prebiotic milk oligosaccharides prevent development of obese phenotype, impairment of gut permeability, and microbial dysbiosis in high fat-fed mice. Am J Physiol Gastrointest Liver Physiol (2017) 312:G474-87. doi:10.1152/ajpgi.00427.2016
75. Buffington SA, Di Prisco GV, Auchtung TA, Ajami NJ, Petrosino JF, Costa-Mattioli M. Microbial reconstitution reverses maternal diet-induced social and synaptic deficits in offspring. Cell (2016) 165:1762-75. doi:10.1016/j.cell.2016.06.001
76. Murphy EA, Velazquez KT, Herbert KM. Influence of high-fat-diet on gut microbiota: a driving force for chronic disease risk. Curr Opin Clin Nutr Metab Care (2015) 18:515-20. doi:10.1097/mco.0000000000000209