Functional Genomics of Host–Microbiome Interactions in Humans

Trends in Genetics

Volumn 34, Issue 1, 2018, Pages 30-40

  Luca, Francesca ^a   Kupfer, Sonia S ^b   Knights, Dan ^c,d   Khoruts, Alexander ^c,e   Blekhman, Ran ^c  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d University of Minnesota   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

functional genomics; host microbiome interactions; human genomics; microbiome

Indexed keywords

CAUSALITY; FUNCTIONAL GENOMICS; GENE CONTROL; GENE EXPRESSION; GENETIC VARIABILITY; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HUMAN; MATHEMATICAL ANALYSIS; MICROBIOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS MAPPING; REGULATORY MECHANISM; REVIEW; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; MICROFLORA; PROCEDURES; TRANSLATIONAL RESEARCH;

ANIMALS; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; GENOMICS; HUMANS; MICROBIOTA; TRANSLATIONAL MEDICAL RESEARCH;

EID: 85032284772     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2017.10.001     Document Type: Review

References (100)

1. Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486 (2012), 207–214.
2. Zhernakova, A., et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352 (2016), 565–569.
3. Falony, G., et al. Population-level analysis of gut microbiome variation. Science 352 (2016), 560–564.
4. Tung, J., et al. Social networks predict gut microbiome composition in wild baboons. Elife, 4, 2015, e05224.
5. Lax, S., et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345 (2014), 1048–1052.
6. Gomez, A., et al. Gut microbiome of coexisting BaAka pygmies and Bantu reflects gradients of traditional subsistence patterns. Cell Rep. 14 (2016), 2142–2153.
7. Vangay, P., et al. Antibiotics, pediatric dysbiosis, and disease. Cell Host Microbe 17 (2015), 553–564.
8. Morton, E.R., et al. Variation in rural African Gut microbiota is strongly correlated with colonization by Entamoeba and subsistence. PLoS Genet., 11, 2015, e1005658.
9. David, L.A., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505 (2014), 559–563.
10. Yassour, M., et al. Natural history of the infant gut microbiome and impact of antibiotic treatment on bacterial strain diversity and stability. Sci. Transl. Med., 8, 2016 343ra81.
11. Goodrich, J.K., et al. Cross-species comparisons of host genetic associations with the microbiome. Science 352 (2016), 532–535.
12. Thaiss, C.A., et al. Persistent microbiome alterations modulate the rate of post-dieting weight regain. Nature 540 (2016), 544–551.
13. Kostic, A.D., et al. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology 146 (2014), 1489–1499.
14. Burns, M.B., et al. Virulence genes are a signature of the microbiome in the colorectal tumor microenvironment. Genome Med., 7, 2015, 55.
15. Baxter, N.T., et al. Structure of the gut microbiome following colonization with human feces determines colonic tumor burden. Microbiome, 2, 2014, 20.
16. Qin, J., et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490 (2012), 55–60.
17. Gevers, D., et al. The treatment-naive microbiome in new-onset Crohn's disease. Cell Host Microbe 15 (2014), 382–392.
18. Tong, M., et al. Reprogramming of gut microbiome energy metabolism by the FUT2 Crohn's disease risk polymorphism. ISME J. 8 (2014), 2193–2206.
19. Khachatryan, Z.A., et al. Predominant role of host genetics in controlling the composition of gut microbiota. PLoS One, 3, 2008, e3064.
20. Benson, A.K., The gut microbiome – an emerging complex trait. Nat. Genet. 48 (2016), 1301–1302.
21. Leamy, L.J., et al. Host genetics and diet, but not immunoglobulin A expression, converge to shape compositional features of the gut microbiome in an advanced intercross population of mice. Genome Biol., 15, 2014, 552.
22. Carmody, R.N., et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17 (2015), 72–84.
23. Benson, A.K., et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 18933–18938.
24. McKnite, A.M., et al. Murine gut microbiota is defined by host genetics and modulates variation of metabolic traits. PLoS One, 7, 2012, e39191.
25. Org, E., et al. Genetic and environmental control of host–gut microbiota interactions. Genome Res. 25 (2015), 1558–1569.
26. van Opstal, E.J., Bordenstein, S.R., MICROBIOME. Rethinking heritability of the microbiome. Science 349 (2015), 1172–1173.
27. Goodrich, J.K., et al. Human genetics shape the gut microbiome. Cell 159 (2014), 789–799.
28. Knights, D., et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med., 6, 2014, 107.
29. A framework for human microbiome research. Nature 486, 215–221.
30. Blekhman, R., et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol., 16, 2015, 191.
31. Davenport, E.R., et al. Genome-wide association studies of the human gut microbiota. PLoS One, 10, 2015, e0140301.
32. Igartua, C., et al. Host genetic variation in mucosal immunity pathways influences the upper airway microbiome. Microbiome, 5, 2017, 16.
33. Turpin, W., et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat. Genet. 48 (2016), 1413–1417.
34. Bonder, M.J., et al. The effect of host genetics on the gut microbiome. Nat. Genet. 48 (2016), 1407–1412.
35. Wang, J., et al. Genome-wide association analysis identifies variation in vitamin D receptor and other host factors influencing the gut microbiota. Nat. Genet. 48 (2016), 1396–1406.
36. Forslund, K., et al. Disentangling type 2 diabetes and metformin treatment signatures in the human gut microbiota. Nature 528 (2015), 262–266.
37. Couturier-Maillard, A., et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J. Clin. Invest. 123 (2013), 700–711.
38. Sommer, F., et al. Site-specific programming of the host epithelial transcriptome by the gut microbiota. Genome Biol., 16, 2015, 62.
39. Camp, J.G., et al. Microbiota modulate transcription in the intestinal epithelium without remodeling the accessible chromatin landscape. Genome Res. 24 (2014), 1504–1516.
40. Davison, J.M., et al. Microbiota regulate intestinal epithelial gene expression by suppressing the transcription factor hepatocyte nuclear factor 4 alpha. Genome Res. 27 (2017), 1195–1206.
41. Small, C.M., et al. Host genotype and microbiota contribute asymmetrically to transcriptional variation in the threespine stickleback gut. Genome Biol. Evol. 9 (2017), 504–520.
42. Dobson, A.J., et al. The Drosophila transcriptional network is structured by microbiota. BMC Genomics, 17, 2016, 975.
43. GTEx Consortium, The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348 (2015), 648–660.
44. Knights, D., et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med., 6, 2014, 107.
45. O'Connor, A., et al. Responsiveness of cardiometabolic-related microbiota to diet is influenced by host genetics. Mamm. Genome 25 (2014), 583–599.
46. Guo, C., et al. Population-specific genome-wide mapping of expression quantitative trait loci in the colon of Chinese Han people. J. Dig. Dis. 17 (2016), 600–609.
47. Zeng, C., et al. Identification of susceptibility loci and genes for colorectal cancer risk. Gastroenterology 150 (2016), 1633–1645.
48. Peloquin, J., et al. O-002 genes in IBD-associated risk loci demonstrate genotype-, tissue-, and inflammation-specific patterns of expression in terminal ileum and colon mucosal tissue. Inflamm. Bowel Dis., 22(Suppl. 1), 2016, S1.
49. Hulur, I., et al. Enrichment of inflammatory bowel disease and colorectal cancer risk variants in colon expression quantitative trait loci. BMC Genomics, 16, 2015, 138.
50. Singh, T., et al. Characterization of expression quantitative trait loci in the human colon. Inflamm. Bowel Dis. 21 (2015), 251–256.
51. Ongen, H., et al. Putative cis-regulatory drivers in colorectal cancer. Nature 512 (2014), 87–90.
52. Li, Q., et al. Expression QTL-based analyses reveal candidate causal genes and loci across five tumor types. Hum. Mol. Genet. 23 (2014), 5294–5302.
53. Closa, A., et al. Identification of candidate susceptibility genes for colorectal cancer through eQTL analysis. Carcinogenesis 35 (2014), 2039–2046.
54. Loo, L.W.M., et al. cis-Expression QTL analysis of established colorectal cancer risk variants in colon tumors and adjacent normal tissue. PLoS One, 7, 2012, e30477.
55. Barreiro, L.B., et al. Deciphering the genetic architecture of variation in the immune response to Mycobacterium tuberculosis infection. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 1204–1209.
56. Fairfax, B.P., et al. Innate immune activity conditions the effect of regulatory variants upon monocyte gene expression. Science, 343, 2014 1246949.
57. Nédélec, Y., et al. Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell, 167, 2016 657–669.e21.
58. Çalışkan, M., et al. Host genetic variation influences gene expression response to rhinovirus infection. PLoS Genet., 11, 2015, e1005111.
59. Campbell, J.H., et al. Host genetic and environmental effects on mouse intestinal microbiota. ISME J. 6 (2012), 2033–2044.
60. van Baarlen, P., et al. Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc. Natl. Acad. Sci. U. S. A. 108:Suppl. 1 (2011), 4562–4569.
61. Bron, P.A., et al. Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nat. Rev. Microbiol. 10 (2011), 66–78.
62. Farhana, L., et al. Bile acid: a potential inducer of colon cancer stem cells. Stem Cell Res. Ther., 7, 2016, 181.
63. Tsai, C.-C., et al. Increase in apoptosis by combination of metformin with silibinin in human colorectal cancer cells. World J. Gastroenterol. 21 (2015), 4169–4177.
64. Farhana, L., et al. Role of cancer stem cells in racial disparity in colorectal cancer. Cancer Med. 5 (2016), 1268–1278.
65. Maderer, A., et al. Moguntinones – new selective inhibitors for the treatment of human colorectal cancer. Mol. Cancer Ther. 13 (2014), 1399–1409.
66. Rabineau, M., et al. Contribution of soft substrates to malignancy and tumor suppression during colon cancer cell division. PLoS One, 8, 2013, e78468.
67. Marzorati, M., et al. The HMI™ module: a new tool to study the Host–Microbiota Interaction in the human gastrointestinal tract in vitro. BMC Microbiol., 14, 2014, 133.
68. Kim, H.J., et al. Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E7–E15.
69. Richards, A.L., et al. Genetic and transcriptional analysis of human host response to healthy gut microbiota. mSystems 1 (2016), e00067–16.
70. Schweiger, P.J., Jensen, K.B., Modeling human disease using organotypic cultures. Curr. Opin. Cell Biol. 43 (2016), 22–29.
71. Tsilingiri, K., et al. Probiotic and postbiotic activity in health and disease: comparison on a novel polarised ex-vivo organ culture model. Gut 61 (2012), 1007–1015.
72. 2 vitamin D3 in African- and European-Americans. J. Steroid Biochem. Mol. Biol. 168 (2017), 49–59.
73. 2 and 25(OH) vitamin D. Physiol. Genomics 46 (2014), 302–308.
74. Sato, T., et al. Single Lgr5 stem cells build crypt–villus structures in vitro without a mesenchymal niche. Nature 459 (2009), 262–265.
75. Spence, J.R., et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 470 (2011), 105–109.
76. Dedhia, P.H., et al. Organoid models of human gastrointestinal development and disease. Gastroenterology 150 (2016), 1098–1112.
77. Nozaki, K., et al. Co-culture with intestinal epithelial organoids allows efficient expansion and motility analysis of intraepithelial lymphocytes. J. Gastroenterol. 51 (2016), 206–213.
78. Bertaux-Skeirik, N., et al. Co-culture of gastric organoids and immortalized stomach mesenchymal cells. Methods Mol. Biol. 1422 (2016), 23–31.
79. Finkbeiner, S.R., et al. Transcriptome-wide analysis reveals hallmarks of human intestine development and maturation in vitro and in vivo. Stem Cell Rep. 4 (2015), 1140–1155.
80. Wilson, S.S., et al. A small intestinal organoid model of non-invasive enteric pathogen–epithelial cell interactions. Mucosal Immunol. 8 (2015), 352–361.
81. Leslie, J.L., et al. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect. Immun. 83 (2015), 138–145.
82. Karve, S.S., et al. Intestinal organoids model human responses to infection by commensal and Shiga toxin producing Escherichia coli. PLoS One, 12, 2017, e0178966.
83. Lukovac, S., et al. Differential modulation by Akkermansia muciniphila and Faecalibacterium prausnitzii of host peripheral lipid metabolism and histone acetylation in mouse gut organoids. MBio 5 (2014), e01438–14.
84. Goodrich, J.K., et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19 (2016), 731–743.
85. Morgan, X.C., et al. Associations between host gene expression, the mucosal microbiome, and clinical outcome in the pelvic pouch of patients with inflammatory bowel disease. Genome Biol., 16, 2015, 67.
86. Gamazon, E.R., et al. A gene-based association method for mapping traits using reference transcriptome data. Nat. Genet. 47 (2015), 1091–1098.
87. Vikhanski, L., Immunity: How Elie Metchnikoff Changed the Course of Modern Medicine. 2016, Chicago Review Press.
88. Anukam, K.C. and Reid, G. (2007) Probiotics: 100 years (1907–2007) after Elie Metchnikoff's observation. In Communicating Current Research and Educational Topics and Trends in Applied Microbiology (Vol. 2) (Méndez-Vilas, A., ed.), pp. 466–473, Formatex.
89. Eiseman, B., et al. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44 (1958), 854–859.
90. Sonnenburg, E.D., Sonnenburg, J.L., Starving our microbial self: the deleterious consequences of a diet deficient in microbiota-accessible carbohydrates. Cell Metab. 20 (2014), 779–786.
91. Khoruts, A., Sadowsky, M.J., Understanding the mechanisms of faecal microbiota transplantation. Nat. Rev. Gastroenterol. Hepatol. 13 (2016), 508–516.
92. Mangravite, L.M., et al. A statin-dependent QTL for GATM expression is associated with statin-induced myopathy. Nature 502 (2013), 377–380.
93. Maranville, J.C., et al. Interactions between glucocorticoid treatment and cis-regulatory polymorphisms contribute to cellular response phenotypes. PLoS Genet., 7, 2011, e1002162.
94. Maranville, J.C., et al. Genetic mapping with multiple levels of phenotypic information reveals determinants of lymphocyte glucocorticoid sensitivity. Am. J. Hum. Genet. 93 (2013), 735–743.
95. Siddle, K.J., et al. A genomic portrait of the genetic architecture and regulatory impact of microRNA expression in response to infection. Genome Res. 24 (2014), 850–859.
96. Pastinen, T., Genome-wide allele-specific analysis: insights into regulatory variation. Nat. Rev. Genet. 11 (2010), 533–538.
97. Kasowski, M., et al. Variation in transcription factor binding among humans. Science 328 (2010), 232–235.
98. McDaniell, R., et al. Heritable individual-specific and allele-specific chromatin signatures in humans. Science 328 (2010), 235–239.
99. Knowles, D.A., et al. Allele-specific expression reveals interactions between genetic variation and environment. Nat. Methods 14 (2017), 699–702.
100. Moyerbrailean, G.A., et al. High-throughput allele-specific expression across 250 environmental conditions. Genome Res. 26 (2016), 1627–1638.