Advertisement

The microbiome and human disease pathogenesis: how do you do what you do to me …?

  • Edward N. Janoff
    Correspondence
    Reprint requests: Edward N. Janoff, Mucosal and Vaccine Research Program Colorado (MAVRC), Research Complex 2, Room 11-012, Box B-168, Aurora, CO 80045
    Affiliations
    Mucosal and Vaccine Research Program Colorado (MAVRC), Division of Infectious Disease, Department of Medicine, University of Colorado School of Medicine, Aurora, Colo

    Denver, Veterans Affairs Medical Center, Denver, Colo
    Search for articles by this author
Published:October 19, 2016DOI:https://doi.org/10.1016/j.trsl.2016.10.007
      In 1963, the English pop band, Gerry and the Pacemakers, musically inquired of their lover, “How do you do what you do to me? I wish I knew.” Over 50 years later, in the context of our current romance with the microbiome and human disease pathogenesis, we are asking the same question, and we are beginning to get answers. This timely special issue of Translational Research provides evidence that weighs these epidemiologic and mechanistic links in a range of common clinical scenarios affecting multiple organ systems and large populations.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Translational Research
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Pace N.R.
        • Sapp J.
        • Goldenfeld N.
        Phylogeny and beyond: scientific, historical, and conceptual significance of the first tree of life.
        Proc Natl Acad Sci U S A. 2012; 109: 1011-1018
        • Woese C.R.
        • Fox G.E.
        Phylogenetic structure of the prokaryotic domain: the primary kingdoms.
        Proc Natl Acad Sci U S A. 1977; 74: 5088-5090
        • Woese C.R.
        • Kandler O.
        • Wheelis M.L.
        Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya.
        Proc Natl Acad Sci U S A. 1990; 87: 4576-4579
        • Lozupone C.
        • Hamady M.
        • Knight R.
        UniFrac–an online tool for comparing microbial community diversity in a phylogenetic context.
        BMC Bioinformatics. 2006; 7: 371
        • Robertson C.E.
        • Harris J.K.
        • Wagner B.D.
        • et al.
        Explicet: graphical user interface software for metadata-driven management, analysis and visualization of microbiome data.
        Bioinformatics. 2013; 29: 3100-3101
        • Frank D.N.
        • Zhu W.
        • Sartor R.B.
        • Li E.
        Investigating the biological and clinical significance of human dysbioses.
        Trends Microbiol. 2011; 19: 427-434
        • Peterson J.
        • Garges S.
        • Giovanni M.
        • et al.
        • NIH HMP Working Group
        The NIH human microbiome project.
        Genome Res. 2009; 19: 2317-2323
        • McDonald D.
        • Birmingham A.
        • Knight R.
        Context and the human microbiome.
        Microbiome. 2015; 3: 52
        • Backhed F.
        • Ley R.E.
        • Sonnenburg J.L.
        • Peterson D.A.
        • Gordon J.I.
        Host-bacterial mutualism in the human intestine.
        Science. 2005; 307: 1915-1920
        • Huda M.N.
        • Lewis Z.
        • Kalanetra K.M.
        • et al.
        Stool microbiota and vaccine responses of infants.
        Pediatrics. 2014; 134: e362-e372
        • Oh J.Z.
        • Ravindran R.
        • Chassaing B.
        • et al.
        TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination.
        Immunity. 2014; 41: 478-492
        • Uematsu S.
        • Fujimoto K.
        • Jang M.H.
        • et al.
        Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5.
        Nat Immunol. 2008; 9: 769-776
        • Gensollen T.
        • Iyer S.S.
        • Kasper D.L.
        • Blumberg R.S.
        How colonization by microbiota in early life shapes the immune system.
        Science. 2016; 352: 539-544
        • Hooper L.V.
        • Wong M.H.
        • Thelin A.
        • Hansson L.
        • Falk P.G.
        • Gordon J.I.
        Molecular analysis of commensal host-microbial relationships in the intestine.
        Science. 2001; 291: 881-884
        • Janoff E.N.
        • Gustafson C.
        • Frank D.N.
        The world within: living with our microbial guests and guides.
        Transl Res. 2012; 160: 239-245
        • Kau A.L.
        • Ahern P.P.
        • Griffin N.W.
        • Goodman A.L.
        • Gordon J.I.
        Human nutrition, the gut microbiome and the immune system.
        Nature. 2011; 474: 327-336
        • Macpherson A.J.
        • Harris N.L.
        Interactions between commensal intestinal bacteria and the immune system.
        Nat Rev Immunol. 2004; 4: 478-485
        • Planer J.D.
        • Peng Y.
        • Kau A.L.
        • et al.
        Development of the gut microbiota and mucosal IgA responses in twins and gnotobiotic mice.
        Nature. 2016; 534: 263-266
        • Round J.L.
        • Mazmanian S.K.
        The gut microbiota shapes intestinal immune responses during health and disease.
        Nat Rev Immunol. 2009; 9: 313-323
        • Tanoue T.
        • Atarashi K.
        • Honda K.
        Development and maintenance of intestinal regulatory T cells.
        Nat Rev Immunol. 2016; 16: 295-309
        • Atarashi K.
        • Tanoue T.
        • Honda K.
        Induction of lamina propria Th17 cells by intestinal commensal bacteria.
        Vaccine. 2010; 28: 8036-8038
        • Atarashi K.
        • Tanoue T.
        • Oshima K.
        • et al.
        Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota.
        Nature. 2013; 500: 232-236
        • Ivanov I.I.
        • Atarashi K.
        • Manel N.
        • et al.
        Induction of intestinal Th17 cells by segmented filamentous bacteria.
        Cell. 2009; 139: 485-498
        • Yang Y.
        • Torchinsky M.B.
        • Gobert M.
        • et al.
        Focused specificity of intestinal TH17 cells towards commensal bacterial antigens.
        Nature. 2014; 510: 152-156
        • Dominguez-Bello M.G.
        • Costello E.K.
        • Contreras M.
        • et al.
        Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns.
        Proc Natl Acad Sci U S A. 2010; 107: 11971-11975
        • Dominguez-Bello M.G.
        • De Jesus-Laboy K.M.
        • Shen N.
        • et al.
        Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer.
        Nat Med. 2016; 22: 250-253
        • Palmer C.
        • Bik E.M.
        • Digiulio D.B.
        • Relman D.A.
        • Brown P.O.
        Development of the human infant intestinal microbiota.
        PLoS Biol. 2007; 5: e177
        • Brumbaugh D.E.
        • Arruda J.
        • Robbins K.
        • et al.
        Mode of delivery determines neonatal pharyngeal bacterial composition and early intestinal colonization.
        J Pediatr Gastroenterol Nutr. 2016; 63: 320-328
        • Gibbons D.L.
        • Spencer J.
        Mouse and human intestinal immunity: same ballpark, different players; different rules, same score.
        Mucosal Immunol. 2011; 4: 148-157
        • Kau A.L.
        • Planer J.D.
        • Liu J.
        • et al.
        Functional characterization of IgA-targeted bacterial taxa from undernourished Malawian children that produce diet-dependent enteropathy.
        Sci Transl Med. 2015; 7: 276ra24
        • Ardeshir A.
        • Narayan N.R.
        • Mendez-Lagares G.
        • et al.
        Breast-fed and bottle-fed infant rhesus macaques develop distinct gut microbiotas and immune systems.
        Sci Transl Med. 2014; 6: 252ra120
        • Lemas D.J.
        • Young B.E.
        • Baker 2nd, P.R.
        • 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: 1291-1300
        • Bender J.M.
        • Li F.
        • Martelly S.
        • et al.
        Maternal HIV infection influences the microbiome of HIV-uninfected infants.
        Sci Transl Med. 2016; 8: 349ra100
        • Hambidge K.M.
        • Krebs N.F.
        • Westcott J.E.
        • et al.
        Preconception maternal nutrition: a multi-site randomized controlled trial.
        BMC Pregnancy Childbirth. 2014; 14: 111
        • van Nood E.
        • Vrieze A.
        • Nieuwdorp M.
        • et al.
        Duodenal infusion of donor feces for recurrent Clostridium difficile.
        N Engl J Med. 2013; 368: 407-415
        • Khoruts A.
        • Hippen K.L.
        • Lemire A.M.
        • et al.
        Toward Revision of antimicrobial therapies in hematopoietic stem cell transplantation: target the pathogens, but protect the indigenous microbiota.
        Transl Res. 2016;
      1. Djuric. Obesity-associated cancer risk: do intestinal microbiota contribute to the etiology of the systemic pro-inflammatory state?

        • Noecker C.
        • McNally C.P.
        • Eng A.
        • Borenstein E.
        High-Resolution and Accurate Characterization of the human microbiome.
        Transl Res. 2016;
        • Miyoshi J.
        • Chang E.B.
        The gut microbiota and inflammatory bowel diseases.
        Transl Res. 2016;
        • Scott F.W.
        • Pound L.D.
        • Patrick C.
        • Eberhard C.E.
        • Crookshank J.A.
        Where genes meet environment-Integrating the role of gut luminal contents, immunity and pancreas in type 1 diabetes.
        Transl Res. 2016;
      2. Betrapalli. Microbiome and liver disease.

        • Nallu A.
        • Sharma S.
        • Ramezani A.
        • Muralidharan J.
        • Raj D.
        Gut Microbiome in CKD: challenges and opportunities.
        Transl Res. 2016;
        • Tang W.H.
        • Hazen S.L.
        Microbiome, Trimethylamine N-Oxide (TMAO), and Cardiometabolic Disease.
        Transl Res. 2016;
        • Ochoa-Repáraz J.
        • Kasper L.H.
        The influence of gut derived CD39 regulatory T cells in CNS demyelinating disease.
        Transl Res. 2016;
        • Johnson C.C.
        • Ownby D.R.
        The infant gut bacterial microbiota and risk of pediatric asthma and allergic diseases.
        Transl Res. 2016;
        • Cribbs S.K.
        • Beck J.M.
        Microbiome in the pathogenesis of cystic fibrosis and lung transplant-related disease.
        Transl Res. 2016;
        • Huang Y.J.
        • Erb-Downward J.R.
        • Dickson R.P.
        • Curtis J.L.
        • Huffnagle G.B.
        • Han M.K.
        Understanding the role of the microbiome in COPD: principles, challenges and future directions.
        Transl Res. 2016;
        • Blaser M.J.
        Missing Microbes: How the Overuse of Antibiotics Is Fueling Our Modern Plagues.
        Henry Holt and Co., New York2014
        • Schroeder B.O.
        • Backhed F.
        Signals from the gut microbiota to distant organs in physiology and disease.
        Nat Med. 2016; 22: 1079-1089
        • Kyrgiou M.
        • Mitra A.
        • Moscicki A.B.
        Does vaginal microbiota play a role in the development of cervical cancer?.
        Transl Res. 2016;
      3. Pope. Microbiota and cancer: a discordant symphony.

        • Hill A.B.
        The environment and disease: association or causation?.
        Proc R Soc Med. 1965; 58: 295-300
        • Herrera V.
        • Parsonnet J.
        Helicobacter pylori and gastric adenocarcinoma.
        Clin Microbiol Infect. 2009; 15: 971-976
        • Uemura N.
        • Okamoto S.
        • Yamamoto S.
        • et al.
        Helicobacter pylori infection and the development of gastric cancer.
        N Engl J Med. 2001; 345: 784-789
        • Hanage W.P.
        Microbiology: microbiome science needs a healthy dose of scepticism.
        Nature. 2014; 512: 247-248
        • Moon C.
        • Stappenbeck T.S.
        Viral interactions with the host and microbiota in the intestine.
        Curr Opin Immunol. 2012; 24: 405-410
        • Wylie K.M.
        • Weinstock G.M.
        • Storch G.A.
        Emerging view of the human virome.
        Transl Res. 2012; 160: 283-290