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Connect between gut microbiome and diseases of the human eye

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Abstract

Implicating dysbiosis of gut microbiome in digestive tract diseases/diet-related diseases (obesity, inflammatory bowel disease, enterocolitis, diabetes, etc.) may be expected. However, when gut microbiome dysbiosis is implicated in extra-intestinal diseases like cancers, muscular dystrophy, mental disorders, vaginosis, etc., it is all the more challenging. An additional challenge would be to ascertain the role of gut microbiome in ocular diseases, which are as remote as the brain. The present review highlights studies that establish the connect between gut microbiome dysbiosis and inflammatory ocular diseases such as uveitis, bacterial keratitis, fungal keratitis, etc.

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References

  • Aas J, Gessert CE and Bakken JS 2003 Recurrent Clostridium difficile colitis: case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin. Infect. Dis. 36 580–585

    Article  PubMed  Google Scholar 

  • Acharya C and Bajaj JS 2017 Gut microbiota and complications of liver disease. Gastroenterol. Clin. North Am. 46 155–169

    Article  PubMed  PubMed Central  Google Scholar 

  • Aly AM, Adel A, El-Gendy AO, Essam TM and Aziz RK 2016 Gut microbiome alterations in patients with stage 4 hepatitis C. Gut Pathol. 8 42

    Article  CAS  Google Scholar 

  • Andriessen EM, Wilson AM, Mawambo G, Dejda A, Miloudi K, Sennlaub F, et al. 2016 Gut microbiota influences pathological angiogenesis in obesity-driven choroidal neovascularization. EMBO Mol. Med. 8 1366–1379

    CAS  Google Scholar 

  • Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. 2013 Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504 451–455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemente JC, Ursell LK, Parfrey LW and Knight R 2012 The impact of the gut microbiota on human health: an integrative view. Cell 148 1258–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dasgupta S, Erturk-Hasdemir D, Ochoa-Reparaz J, Reinecker HC and Kasper DL 2014 Plasmacytoid dendritic cells mediate anti-inflammatory responses to a gut commensal molecule via both innate and adaptive mechanisms. Cell Host Microbe 15 413–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Paiva CS, Jones DB, Stern ME, Bian F, Moore QL, Corbiere S, et al. 2016 Altered mucosal microbiome diversity and disease severity in Sjogren syndrome. Sci. Rep. 6 23561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong Q, Brulc JM, Iovieno A, Bates B, Garoutte A, Miller D, et al. 2011 Diversity of bacteria at healthy human conjunctiva. Investig. Ophthalmol. Vis. Sci. 52 5408–5413

    Article  CAS  Google Scholar 

  • Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, et al. 2013 Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 110 9066–9071

    Article  PubMed  PubMed Central  Google Scholar 

  • Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N and Pace NR 2007 Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc. Natl. Acad. Sci. USA 104 13780–13785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gacias M, Gaspari S, Santos PM, Tamburini S, Andrade M, Zhang F, et al. 2016 Microbiota-driven transcriptional changes in prefrontal cortex override genetic differences in social behavior. Elife https://doi.org/10.7554/eLife.13442

    Article  PubMed  PubMed Central  Google Scholar 

  • Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, et al. 2010 Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe 8 292–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giloteaux L, Goodrich JK, Walters WA, Levine SM, Ley RE and Hanson MR 2016 Reduced diversity and altered composition of the gut microbiome in individuals with myalgic encephalomyelitis/chronic fatigue syndrome. Microbiome 4 30

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodrich JK, Waters JL, Poole AC, Sutter JL, Koren O, Blekhman R, et al. 2014 Human genetics shape the gut microbiome. Cell 159 789–799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horai R, Zarate-Blades CR, Dillenburg-Pilla P, Chen J, Kielczewski JL, Silver PB, et al. 2015 Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site. Immunity 43 343–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, Ye Z, Cao Q, Su G, Wang Q, Deng J, et al. 2018 Gut microbiota composition and fecal metabolic phenotype in patients with acute anterior uveitis. Investig. Ophthalmol. Vis. Sci. 59 1523–1531

    Article  CAS  Google Scholar 

  • Jayasudha R, Chakravarthy SK, Prashanthi GS, Sharma S, Garg P, Murthy SI, et al. 2018 Alterations in gut bacterial and fungal microbiomes are associated with bacterial Keratitis, an inflammatory disease of the human eye. J. Biosci. 43 835–856

    Article  CAS  PubMed  Google Scholar 

  • Jayasudha R, Chakravarthy SK, Prashanthi SG, Sharma S, Garg P, Murthy SI and Shivaji S Implicating dysbiosis of the gut fungal microbiome in uveitis, an inflammatory disease of the eye. Investig. Ophthalmol. Vis. Sci.2019 (In Press)

    Google Scholar 

  • Jumas-Bilak E, Carlier JP, Jean-Pierre H, Mory F, Teyssier C, Gay B, et al. 2007 Acidaminococcus intestini sp. nov., isolated from human clinical samples. Int. J. Syst. Evol. Microbiol. 57 2314–2319

    Article  CAS  PubMed  Google Scholar 

  • Kalyana Chakravarthy S, Jayasudha R, Ranjith K, Dutta A, Pinna NK, Mande SS, et al. 2018a Alterations in the gut bacterial microbiome in fungal Keratitis patients. PLoS One 13 e0199640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalyana Chakravarthy S, Jayasudha R, Sai Prashanthi G, Ali MH, Sharma S, Tyagi M, et al. 2018b Dysbiosis in the gut bacterial microbiome of patients with uveitis, an inflammatory disease of the eye. Indian J. Microbiol. 58 457–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kugadas A, Christiansen SH, Sankaranarayanan S, Surana NK, Gauguet S, Kunz R, et al. 2016 Impact of microbiota on resistance to ocular Pseudomonas aeruginosa-induced keratitis. PLoS Pathog. 12 e1005855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kugadas A, Wright Q, Geddes-McAlister J and Gadjeva M 2017 Role of microbiota in strengthening ocular mucosal barrier function through secretory IgA. Investig. Ophthalmol. Vis. Sci. 58 4593–4600

    Article  CAS  Google Scholar 

  • Lederberg J and McCray AT 2001 ’Ome Sweet ’Omics—A genealogical treasury of words. Scientist 15 8

    Google Scholar 

  • Leser T, Myling-Petersen D, Wellejus A, Brockmann E, Olsen J, Rehdin S, Chr Hansen AS 2016 Probiotic strains of Bifidobacterium adolescentis Conference Proceeding (PAMIDA International)

  • Levine JS and Burakoff R 2011 Extraintestinal manifestations of inflammatory bowel disease. Gastroenterol. Hepatol. 7 235–241

    Google Scholar 

  • Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD and Gordon JI 2005 Obesity alters gut microbial ecology. Proc. Natl. Acad. Sci. USA 102 11070–11075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin P 2018 The role of the intestinal microbiome in ocular inflammatory disease. Curr. Opin. Ophthalmol. 29 261–266

    Article  PubMed  Google Scholar 

  • Lopetuso LR, Scaldaferri F, Petito V and Gasbarrini A 2013 Commensal Clostridia: leading players in the maintenance of gut homeostasis. Gut Pathog. 5 23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu LJ and Liu J 2016 Human microbiota and ophthalmic disease. Yale J. Biol. Med. 89 325–330

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lukiw WJ 2016 Bacteroides fragilis lipopolysaccharide and inflammatory signaling in Alzheimer’s disease. Front. Microbiol. 7 1544

    Article  PubMed  PubMed Central  Google Scholar 

  • Malan-Muller S, Valles-Colomer M, Raes J, Lowry CA, Seedat S and Hemmings SM J 2018 The gut microbiome and mental health: implications for anxiety- and trauma-related disorders. OMICS 22 90–107

    Article  CAS  PubMed  Google Scholar 

  • Martin R, Chain F, Miquel S, Lu J, Gratadoux JJ, Sokol H, et al. 2014 The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm. Bowel Dis. 20 417–430

    Article  PubMed  Google Scholar 

  • Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, et al. 2012 Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 13 R79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura YK, Metea C, Karstens L, Asquith M, Gruner H, Moscibrocki C, et al. 2016 Gut microbial alterations associated with protection from autoimmune uveitis. Investig. Ophthalmol. Vis. Sci. 57 3747–3758

    Article  CAS  Google Scholar 

  • Ozkan J, Nielsen S, Diez-Vives C, Coroneo M, Thomas T and Willcox M 2017 Temporal stability and composition of the ocular surface microbiome. Sci. Rep. 7 9880

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramezani A and Raj DS 2014 The gut microbiome, kidney disease, and targeted interventions. J. Am. Soc. Nephrol. 25 657–670

    Article  CAS  PubMed  Google Scholar 

  • Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. 2011 Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. USA 108 4680–4687

    Article  PubMed  Google Scholar 

  • Remely M, Aumueller E, Merold C, Dworzak S, Hippe B, Zanner J, et al. 2014 Effects of short chain fatty acid producing bacteria on epigenetic regulation of FFAR3 in type 2 diabetes and obesity. Gene 537 85–92

    Article  CAS  PubMed  Google Scholar 

  • Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. 2013 Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341 1241214

    Article  CAS  PubMed  Google Scholar 

  • Rowan S, Jiang S, Korem T, Szymanski J, Chang ML, Szelog J, et al. 2017 Involvement of a gut-retina axis in protection against dietary glycemia-induced age-related macular degeneration. Proc. Natl. Acad. Sci. USA 114 E4472–E4481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu J, Kubota T, Takada E, Takai K, Fujiwara N, Arimitsu N, et al. 2016 Bifidobacteria abundance-featured gut microbiota compositional change in patients with Behcet’s disease. PLoS One 11 e0153746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaji S 2017 We are not alone: a case for the human microbiome in extra intestinal diseases. Gut Pathog. 9 13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shivaji S, Jayasudha R, Sai Prashanthi G, Kalyana Chakravarthy S and Sharma S 2019 The human ocular surface fungal microbiome. Investig. Ophthalmol. Vis. Sci. 60 451–459

    Article  CAS  Google Scholar 

  • St Leger AJ, Desai JV, Drummond RA, Kugadas A, Almaghrabi F, Silver P, et al. 2017 An ocular commensal protects against corneal infection by driving an interleukin-17 response from mucosal gamma delta T cells. Immunity 47 148–158

    Article  CAS  PubMed  Google Scholar 

  • Sun J and Kato I 2016 Gut microbiota, inflammation and colorectal cancer. Genes Dis. 3 130–143

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang WH, Kitai T and Hazen SL 2017 Gut microbiota in cardiovascular health and disease. Circ. Res. 120 1183–1196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teweldemedhin M, Gebreyesus H, Atsbaha AH, Asgedom SW and Saravanan M 2017 Bacterial profile of ocular infections: a systematic review. BMC Ophthalmol. 17 212

    Article  PubMed  PubMed Central  Google Scholar 

  • Tlaskalova-Hogenova H, Stepankova R, Kozakova H, Hudcovic T, Vannucci L, Tuckova L, et al. 2011 The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer: contribution of germ-free and gnotobiotic animal models of human diseases. Cell. Mol. Immunol. 8 110–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER and Gordon JI 2006 An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444 1027–1031

    Article  PubMed  Google Scholar 

  • Vavricka SR, Schoepfer A, Scharl M, Lakatos PL, Navarini A and Rogler G 2015 Extraintestinal manifestations of inflammatory bowel disease. Inflamm. Bowel Dis. 21 1982–1992

    Article  PubMed  Google Scholar 

  • Vogt NM, Kerby RL, Dill-McFarland KA, Harding SJ, Merluzzi AP, Johnson SC, et al. 2017 Gut microbiome alterations in Alzheimer’s disease. Sci. Rep. 7 13537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, et al. 2009 Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA 106 3698–3703

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang H, Huang X, Fang S, Xin W, Huang L and Chen C 2016 Uncovering the composition of microbial community structure and metagenomics among three gut locations in pigs with distinct fatness. Sci. Rep. 6 27427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zackular JP, Baxter NT, Iverson KD, Sadler WD, Petrosino JF, Chen GY, et al. 2013 The gut microbiome modulates colon tumorigenesis. MBio 4 e00692-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaleski A, Banaszkiewicz A and Walkowiak J 2013 Butyric acid in irritable bowel syndrome. Prz. Gastroenterol. 8 350–353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zinkernagel MS, Zysset-Burri DC, Keller I, Berger LE, Leichtle AB, Largiader CR, et al. 2017 Association of the intestinal microbiome with the development of neovascular age-related macular degeneration. Sci. Rep. 7 40826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The study was supported by grants received from the Hyderabad Eye Research Foundation and the Department of Biotechnology, India. Thanks to Kalyan, Jayasudha and Prashanthi for their help in this work.

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  1. Brien Holden Eye Research Centre, LV Prasad Eye Institute, Hyderabad, 500 034, India

    S Shivaji

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  1. S Shivaji
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Shivaji, S. Connect between gut microbiome and diseases of the human eye. J Biosci 44, 110 (2019). https://doi.org/10.1007/s12038-019-9931-1

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