Do epigenetic changes caused by commensal microbiota contribute to development of ocular disease? A review of evidence

Ashima Nayyar, Sofya Gindina, Arturo Barron, Yan Hu, John Danias, Ashima Nayyar, Sofya Gindina, Arturo Barron, Yan Hu, John Danias

Abstract

There is evidence that genetic polymorphisms and environmentally induced epigenetic changes play an important role in modifying disease risk. The commensal microbiota has the ability to affect the cellular environment throughout the body without requiring direct contact; for example, through the generation of a pro-inflammatory state. In this review, we discuss evidence that dysbiosis in intestinal, pharyngeal, oral, and ocular microbiome can lead to epigenetic reprogramming and inflammation making the host more susceptible to ocular disease such as autoimmune uveitis, age-related macular degeneration, and open angle glaucoma. Several mechanisms of action have been proposed to explain how changes to commensal microbiota contribute to these diseases. This is an evolving field that has potentially significant implications in the management of these conditions especially from a public health perspective.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Anatomy of eye (adapted from National Eye Institute) [81]
Fig. 2
Fig. 2
Schematic diagram of dry and wet forms of macular degeneration

References

    1. Abbayya K, Puthanakar NY, Naduwinmani S, Chidambar YS. Association between periodontitis and Alzheimer's disease. N Am J Med Sci. 2015;7(6):241. doi: 10.4103/1947-2714.159325.
    1. Acott TS, Kelley MJ. Extracellular matrix in the trabecular meshwork. Exp Eye Res. 2008;86(4):543–561. doi: 10.1016/j.exer.2008.01.013.
    1. Al-Zamil WM, Yassin SA. Recent developments in age-related macular degeneration: a review. Clin Interv Aging. 2017;12:1313–1330. doi: 10.2147/cia.s143508.
    1. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014;146(6):1564–1572. doi: 10.1053/j.gastro.2014.01.058.
    1. Alipour S, Nouri M, Sakhinia E, Samadi N, Roshanravan N, Ghavami A, Khabbazi A. Epigenetic alterations in chronic disease focusing on Behçet’s disease. Biomed Pharmacother. 2017;91:526–533. doi: 10.1016/j.biopha.2017.04.106.
    1. Álvarez-Arellano L, Maldonado-Bernal C. Helicobacter pylori and neurological diseases: married by the laws of inflammation. World J Gastrointest Pathophysiol. 2014;5(4):400.
    1. Ambati J, Fowler BJ. Mechanisms of age-related macular degeneration. Neuron. 2012;75(1):26–39. doi: 10.1016/j.neuron.2012.06.018.
    1. Andriessen EM, Wilson AM, Mawambo G, Dejda A, Miloudi K, Sennlaub F, Sapieha P. Gut microbiota influences pathological angiogenesis in obesity-driven choroidal neovascularization. EMBO Mol Med. 2016;8(12):1366–1379. doi: 10.15252/emmm.201606531.
    1. Astafurov K, Elhawy E, Ren L, Dong CQ, Igboin C, Hyman L, et al. Oral microbiome link to neurodegeneration in glaucoma. PLoS One. 2014;9(9):e104416. doi: 10.1371/journal.pone.0104416.
    1. Barria von BF, Chabouty H, Moreno R, Ortiz F, Barria MF. Microbial flora isolated from patient's conjunctiva previous to cataract surgery. Rev Chilena Infectol. 2015;32(2):150–157. doi: 10.4067/s0716-10182015000300003.
    1. Blum HE. The human microbiome. Adv Med Sci. 2017;62(2):414–420. doi: 10.1016/j.advms.2017.04.005.
    1. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011;108(38):16050–16055. doi: 10.1073/pnas.1102999108.
    1. Bultman SJ. Interplay between diet, gut microbiota, epigenetic events, and colorectal cancer. Mol Nutr Food Res. 2017;61(1):1500902. doi: 10.1002/mnfr.201500902.
    1. Bhutto I, Lutty G. Understanding age-related macular degeneration (AMD): relationships between the photoreceptor/retinal pigment epithelium/Bruch’s membrane/choriocapillaris complex. Mol Aspects Med. 2012;33(4):295–317. doi: 10.1016/j.mam.2012.04.005.
    1. Candido EPM, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell. 1978;14(1):105–113. doi: 10.1016/0092-8674(78)90305-7.
    1. Carding S, Verbeke K, Vipond DT, Corfe BM, Owen LJ. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26:26191. doi: 10.3402/mehd.v26.26191.
    1. Carneiro A, Andrade JP. Nutritional and lifestyle interventions for age-related macular degeneration: a review. Oxid Med Cell Longev. 2017;2017:6469138. doi: 10.1155/2017/6469138.
    1. Caspi RR, Roberge FG, Chan CC, Wiggert B, Chader GJ, Rozenszajn LA, et al. A new model of autoimmune disease. Experimental autoimmune uveoretinitis induced in mice with two different retinal antigens. J Immunol. 1988;140(5):1490–1495.
    1. Casson RJ, Chidlow G, Wood JP, Crowston JG, Goldberg I. Definition of glaucoma: clinical and experimental concepts. Clin Exp Ophthalmol. 2012;40(4):341–349. doi: 10.1111/j.1442-9071.2012.02773.x.
    1. Challa P. Genetics of adult glaucoma. Int Ophthalmol Clin.. 2011;51(3):37–51.
    1. Challa P, Schmidt S, Liu Y, Qin X, Vann RR, Gonzalez P, Hauser MA. Analysis of LOXL1 polymorphisms in a United States population with pseudoexfoliation glaucoma. Mol Vis. 2008;14:146.
    1. Chan CC, Smith JA, Shen D, Ursea R, LeHoang P, Grossniklaus HE. Helicobacter pylori (H. pylori) molecular signature in conjunctival mucosa-associated lymphoid tissue (MALT) lymphoma. Histol Histopathol. 2004;19(4):1219.
    1. Chang PV, Hao L, Offermanns S, Medzhitov R. The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc Natl Acad Sci USA. 2014;111:2247–2252. doi: 10.1073/pnas.1322269111.
    1. Chen H, Cho KS, Vu THK, Shen CH, Kaur M, Chen G, et al. Commensal microflora-induced T cell responses mediate progressive neurodegeneration in glaucoma. Nat Commun. 2018;9(1):3209. doi: 10.1038/s41467-018-05681-9.
    1. Chen J, Qian H, Horai R, Chan CC, Caspi RR. Mouse models of experimental autoimmune uveitis: comparative analysis of adjuvant-induced vs spontaneous models of uveitis. Curr Mol Med. 2015;15(6):550–557. doi: 10.2174/1566524015666150731100318.
    1. Croswell A, Amir E, Teggatz P, Barman M, Salzman NH. Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun. 2009;77(7):2741–2753. doi: 10.1128/IAI.00006-09.
    1. De Haas EN, van der Eijk JAJ. Where in the serotonergic system does it go wrong? Unravelling the route by which the serotonergic system affects feather pecking in chickens. Neurosci Biobehav Rev. 2018;95:170–188. doi: 10.1016/j.neubiorev.2018.07.007.
    1. DeGruttola AK, Low D, Mizoguchi A, Mizoguchi E. Current understanding of dysbiosis in disease in human and animal models. Inflamm Bowel Dis. 2016;22(5):1137–1150. doi: 10.1097/mib.0000000000000750.
    1. Desmettre TJ. Epigenetics in age-related macular degeneration (AMD). J Fr Ophtalmol. 2018.
    1. Donohoe DR, Holley D, Collins LB, Montgomery SA, Whitmore AC, Hillhouse A, et al. A gnotobiotic mouse model demonstrates that dietary fiber protects against colorectal tumorigenesis in a microbiota-and butyrate-dependent manner. Cancer Discov. 2014;4(12):1387–1397. doi: 10.1158/-14-0501.
    1. Erny D, Hrabe de Angelis AL, Jaitin D, Wieghofer P, Staszewski O, David E, Keren-Shaul H, Mahlakoiv T, Jakobshagen K, Buch T, et al. Host microbiota constantly control maturation and function of microglia in the CNS. Nat Neurosci. 2015;18:965–977. doi: 10.1038/nn.4030.
    1. Evertts AG, Zee BM, DiMaggio PA, Gonzales-Cope M, Coller HA, Garcia BA. Quantitative dynamics of the link between cellular metabolism and histone acetylation. J Biol Chem. 2013;288(17):12142–51.
    1. Fang D, Zhu J. Dynamic balance between master transcription factors determines the fates and functions of CD4 T cell and innate lymphoid cell subsets. J Exp Med. 2017;214(7):1861–1876. doi: 10.1084/jem.20170494.
    1. Forrester JV, Kuffova L, Dick AD. Autoimmunity, autoinflammation, and infection in uveitis. Am J Ophthalmol. 2018;189:77–85. doi: 10.1016/j.ajo.2018.02.019.
    1. Fuchshofer R, Welge-Lussen U, Lutjen-Drecoll E, Birke M. Biochemical and morphological analysis of basement membrane component expression in corneoscleral and cribriform human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2006;47(3):794–801. doi: 10.1167/iovs.05-0292.
    1. Ganal SC, Sanos SL, Kallfass C, Oberle K, Johner C, Kirschning C, Lienenklaus S, Weiss S, Staeheli P, Aichele P, et al. Priming of natural killer cells by nonmucosal mononuclear phagocytes requires instructive signals from commensal microbiota. Immunity. 2012;37:171–186. doi: 10.1016/j.immuni.2012.05.020.
    1. Gemenetzi M, Lotery AJ. The role of epigenetics in age-related macular degeneration. Eye. 2014;28(12):1407. doi: 10.1038/eye.2014.225.
    1. González MM, Solano MM, Porco TC, Oldenburg CE, Acharya NR, Lin SC, Chan MF. Epidemiology of uveitis in a US population-based study. J Ophthal inflamm Infect. 2018;8(1):6.
    1. Grossniklaus HE, Geisert EE, Nickerson JM. Introduction to the Retina. Prog Mol Biol Transl Sci. 2015;134:383–396. doi: 10.1016/bs.pmbts.2015.06.001.
    1. Hallak JA, Tibrewal S, Mohindra N, Gao X, Jain S. Single nucleotide polymorphisms in the BDNF, VDR, and DNASE 1 genes in dry eye disease patients: A casecontrol study. Invest Ophthalmol Vis Sci. 2015;56(10):5990–6.
    1. He C, Cheng D, Peng C, Li Y, Zhu Y, Lu N. High-fat diet induces dysbiosis of gastric microbiota prior to gut microbiota in association with metabolic disorders in mice. Front Microbiol. 2018;9:639. doi: 10.3389/fmicb.2018.00639.
    1. Heissigerova J, Seidler Stangova P, Klimova A, Svozilkova P, Hrncir T, Stepankova R, et al. The microbiota determines susceptibility to experimental autoimmune uveoretinitis. J Immunol Res. 2016;2016.
    1. Ho EXP, Cheung CMG, Sim S, Chu CW, Wilm A, Lin CB, et al. Human pharyngeal microbiota in age-related macular degeneration. PLoS One. 2018;13(8):e0201768. doi: 10.1371/journal.pone.0201768.
    1. Holzapfel WH, Haberer P, Snel J, Schillinger U, Huisin’t Veld JH. Overview of gut flora and probiotics. Int J Food Microbiol. 1998;41(2):85–101. doi: 10.1016/S0168-1605(98)00044-0.
    1. Hoon M, Okawa H, Della Santina L, Wong RO. Functional architecture of the retina: development and disease. Prog Retin Eye Res. 2014;42:44–84. doi: 10.1016/j.preteyeres.2014.06.003.
    1. Horai R, Sen HN, Caspi RR. Commensal microbiota as a potential trigger of autoimmune uveitis. Expert Rev Clin Immunol. 2017;13(4):291–293. doi: 10.1080/1744666x.2017.1288098.
    1. Horai R, Zarate-Blades CR, Dillenburg-Pilla P, Chen J, Kielczewski JL, Silver PB, et al. Microbiota-dependent activation of an autoreactive T cell receptor provokes autoimmunity in an immunologically privileged site. Immunity. 2015;43(2):343–353. doi: 10.1016/j.immuni.2015.07.014.
    1. Horie-Inoue K, Inoue S. Genomic aspects of age-related macular degeneration. Biochem Biophys Res Commun. 2014;452(2):263–275. doi: 10.1016/j.bbrc.2014.08.013.
    1. Huang X, Ye Z, Cao Q, Su G, Wang Q, Deng J, et al. Gut microbiota composition and fecal metabolic phenotype in patients with acute anterior uveitis. Invest Ophthalmol Vis Sci. 2018;59(3):1523–1531. doi: 10.1167/iovs.17-22677.
    1. Janowitz C, Nakamura YK, Metea C, Gligor A, Yu W, Karstens L, et al. Disruption of intestinal homeostasis and intestinal microbiota during experimental autoimmune uveitis. Invest Ophthalmol Vis Sci. 2019;60(1):420–429. doi: 10.1167/iovs.18-24813.
    1. Joachim SC, Wuenschig D, Pfeiffer N, Grus FH. IgG antibody patterns in aqueous humor of patients with primary open angle glaucoma and pseudoexfoliation glaucoma. Mol Vis. 2007;13(175):1573–1579.
    1. Kamer AR, Dasanayake AP, Craig RG, Glodzik-Sobanska L, Bry M, de Leon MJ. Alzheimer's disease and peripheral infections: the possible contribution from periodontal infections, model and hypothesis. J Alzheimers Dis. 2008;13(4):437–449. doi: 10.3233/JAD-2008-13408.
    1. Kaisar MM, Pelgrom LR, van der Ham AJ, Yazdanbakhsh M, Everts B. Butyrate conditions human dendritic cells to prime Type 1 regulatory T cells via both histone deacetylase inhibition and G protein-coupled receptor 109A signaling. Front Immunol. 2017;8:1429. doi: 10.3389/fimmu.2017.01429.
    1. Kiel JW. Integrated systems physiology: from molecule to function to disease the ocular circulation. San Rafael: Morgan & Claypool Life Sciences; 2010.
    1. Klein R, Klein BE, Linton KL. Prevalence of age-related maculopathy. The Beaver Dam Eye Study. Ophthalmology. 1992;99(6):933–943. doi: 10.1016/S0161-6420(92)31871-8.
    1. Kountouras J, Mylopoulos N, Boura P, Bessas C, Chatzopoulos D, Venizelos J, Zavos C. Relationship between Helicobacter pylori infection and glaucoma. Ophthalmology. 2001;108(3):599–604. doi: 10.1016/S0161-6420(00)00598-4.
    1. Kountouras J, Zavos C, Chatzopoulos D. Immunomodulatory benefits of cyclosporine A in inflammatory bowel disease. J Cell Mol Med. 2004;8(3):317–328. doi: 10.1111/j.1582-4934.2004.tb00321.x.
    1. Kountouras J, Zavos C, Zeglinas C, Polyzos SA, Katsinelos P. Helicobacter pylori-related impact on glaucoma pathophysiology. Invest Ophthalmol Vis Sci. 2015;56(13):8029–8030. doi: 10.1167/iovs.15-17969.
    1. Kozarov EV, Dorn BR, Shelburne CE, Dunn WA, Jr, Progulske-Fox A. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol. 2005;25(3):e17–e18. doi: 10.1161/01.ATV.0000155018.67835.1a.
    1. Lazarevic V, Chen X, Shim JH, Hwang ES, Jang E, Bolm AN, et al. T-bet represses T H 17 differentiation by preventing Runx1-mediated activation of the gene encoding RORγt. Nat Immunol. 2011;12(1):96. doi: 10.1038/ni.1969.
    1. Lee D, Albenberg L, Compher C, Baldassano R, Piccoli D, Lewis JD, Wu GD. Diet in the pathogenesis and treatment of inflammatory bowel diseases. Gastroenterology. 2015;148(6):1087–1106. doi: 10.1053/j.gastro.2015.01.007.
    1. Leger AJ, Caspi RR. Visions of eye commensals: the known and the unknown about how the microbiome affects eye disease. Bioessays. 2018;40(11):1800046.
    1. Li H, Cao Y. Lactic acid bacterial cell factories for gamma-aminobutyric acid. Amino Acids. 2010;39(5):1107–1116. doi: 10.1007/s00726-010-0582-7.
    1. Li L, Michel R, Cohen J, Decarlo A, Kozarov E. Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol. 2008;8:26. doi: 10.1186/1471-2180-8-26.
    1. Lin L, Zhang J. Role of intestinal microbiota and metabolites on gut homeostasis and human diseases. BMC Immunol. 2017;18(1):2. doi: 10.1186/s12865-016-0187-3.
    1. Lin P. The role of the intestinal microbiome in ocular inflammatory disease. Curr Opin Ophthalmol. 2018;29(3):261–266. doi: 10.1097/icu.0000000000000465.
    1. Lin P, Metea C, Asquith M, Gruner H, Rosenbaum JT, Nakamura YK. The role of the gut microbiota in immune-mediated uveitis. Invest Ophthalmol Visual Sci. 2015;56(7):870–0 Retrieved from .
    1. Liu MM, Chan CC, Tuo J. Epigenetics in ocular diseases. Curr Genomics. 2013;14(3):166–172. doi: 10.2174/1389202911314030002.
    1. Lloyd-Price J, Mahurkar A, Rahnavard G, Crabtree J, Orvis J, Hall AB, et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature. 2017;550(7674):61–66. doi: 10.1038/nature23889.
    1. Lu LJ, Liu J. Human microbiota and ophthalmic disease. Yale J Biol Med. 2016;89(3):325–330.
    1. Lu Y, Fan C, Liang A, Fan X, Wang R, Li P, Qi K. Effects of SCFA on the DNA methylation pattern of adiponectin and resistin in high-fat-diet-induced obese male mice. Br J Nutr. 2018;120(4):385–392. doi: 10.1017/S0007114518001526.
    1. Luo A, Leach ST, Barres R, Hesson LB, Grimm MC, Simar D. The microbiota and epigenetic regulation of T helper 17/regulatory T cells: in search of a balanced immune system. Front Immunol. 2017;8:417. doi: 10.3389/fimmu.2017.00417.
    1. Luo X, Shen YM, Jiang MN, Lou XF, Shen Y. Ocular blood flow autoregulation mechanisms and methods. J Ophthalmol. 2015;2015.
    1. Lyte M. Probiotics function mechanistically as delivery vehicles for neuroactive compounds: Microbial endocrinology in the design and use of probiotics. Bioessays. 2011;33(8):574–581. doi: 10.1002/bies.201100024.
    1. Mazzitello KI, Arizmendi CM, Family F, Grossniklaus HE. Formation and growth of lipofuscin in the retinal pigment epithelium cells. Phys Rev E. 2009;80(5):051908. doi: 10.1103/PhysRevE.80.051908.
    1. McDermott AM. Antimicrobial compounds in tears. Exp Eye Res. 2013;117:53–61. doi: 10.1016/j.exer.2013.07.014.
    1. McKay GJ, Patterson CC, Chakravarthy U, Dasari S, Klaver CC, Vingerling JR, et al. Evidence of association of APOE with age-related macular degeneration: a pooled analysis of 15 studies. Hum Mutat. 2011;32(12):1407–1416. doi: 10.1002/humu.21577.
    1. Miller D, Iovieno A. The role of microbial flora on the ocular surface. Curr Opin Allergy Clin Immunol. 2009;9(5):466–470. doi: 10.1097/ACI.0b013e3283303e1b.
    1. Motulsky AG. Genetics of complex diseases. J Zhejiang Univ Sci B. 2006;7(2):167–8.
    1. Nakamura YK, Metea C, Karstens L, Asquith M, Gruner H, Moscibrocki C, et al. Gut microbial alterations associated with protection from autoimmune uveitis. Invest Ophthalmol Vis Sci. 2016;57(8):3747–3758. doi: 10.1167/iovs.16-19733.
    1. National Eye institute. (2015). Facts about glaucoma (Article). Retrieved from .
    1. Neufeld AH. Microglia in the optic nerve head and the region of parapapillary chorioretinal atrophy in glaucoma. Arch Ophthalmol. 1999;117(8):1050–1056. doi: 10.1001/archopht.117.8.1050.
    1. Nomura A, Stemmermann GN, Chyou PH, Perez-Perez GI, Blaser MJ. Helicobacter pylori infection and the risk for duodenal and gastric ulceration. Ann Intern Med. 1994;120(12):977–981. doi: 10.7326/0003-4819-120-12-199406150-00001.
    1. Pascolini D, Mariotti SP. Global estimates of visual impairment: 2010. Br J Ophthalmol. 2012;96(5):614–618. doi: 10.1136/bjophthalmol-2011-300539.
    1. Pasquale LR, Hyman L, Wiggs JL, Rosner BA, Joshipura K, McEvoy M, et al. Prospective study of oral health and risk of primary open-angle glaucoma in men: data from the health professionals follow-up study. Ophthalmology. 2016;123(11):2318–2327. doi: 10.1016/j.ophtha.2016.07.014.
    1. Pelzel HR, Schlamp CL, Nickells RW. Histone H4 deacetylation plays a critical role in early gene silencing during neuronal apoptosis. BMC Neurosci. 2010;11(1):62. doi: 10.1186/1471-2202-11-62.
    1. Pennington KL, DeAngelis MM. Epidemiology of age-related macular degeneration (AMD): associations with cardiovascular disease phenotypes and lipid factors. Eye and vision. 2016;3(1):34. doi: 10.1186/s40662-016-0063-5.
    1. Polla D, Astafurov K, Hawy E, Hyman L, Hou W, Danias J. A pilot study to evaluate the oral microbiome and dental health in primary open-angle glaucoma. J Glaucoma. 2017;26(4):320–327. doi: 10.1097/ijg.0000000000000465.
    1. Qin Y, Wade PA. Crosstalk between the microbiome and epigenome: messages from bugs. J Biochem. 2017;163(2):105–112. doi: 10.1093/jb/mvx080.
    1. Qiu Y, Zhu Y, Yu H, Zhou C, Kijlstra A, Yang P. Dynamic DNA methylation changes of Tbx21 and Rorc during experimental autoimmune uveitis in mice. Mediators Inflamm. 2018;2018:9129163. doi: 10.1155/2018/9129163.
    1. Quigley HA, Broman AT. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006;90(3):262–267. doi: 10.1136/bjo.2005.081224.
    1. Rickman CB, Farsiu S, Toth CA, Klingeborn M. Dry age-related macular degeneration: mechanisms, therapeutic targets, and imaging. Invest Ophthalmol Vis Sci. 2013;54(14):ORSF68-80.
    1. Rinninella E, Mele MC, Merendino N, Cintoni M, Anselmi G, Caporossi A, et al. The role of diet, micronutrients and the gut microbiota in age-related macular degeneration: new perspectives from the gut(-)retina axis. Nutrients. 2018;10(11). 10.3390/nu10111677.
    1. Rohen JW, Witmer R. Electrn microscopic studies on the trabecular meshwork in glaucoma simplex. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1972;183(4):251–266. doi: 10.1007/BF00496153.
    1. Rosenbaum JT, Asquith M. The microbiome and HLA-B27-associated acute anterior uveitis. Nat Rev Rheumatol. 2018;14(12):704–713. doi: 10.1038/s41584-018-0097-2.
    1. Rosenbaum JT, Davey MP. Time for a gut check: evidence for the hypothesis that HLA-B27 predisposes to ankylosing spondylitis by altering the microbiome. Arthritis Rheum. 2011;63(11):3195–3198. doi: 10.1002/art.30558.
    1. Rosenbaum JT, Lin P, Asquith M. The microbiome, HLA, and the pathogenesis of uveitis. Jpn J Ophthalmol. 2016;60(1):1–6. doi: 10.1007/s10384-015-0416-y.
    1. Runkle EA, Antonetti DA. The blood-retinal barrier: structure and functional significance. Methods Mol Biol. 2011;686:133–148. doi: 10.1007/978-1-60761-938-3_5.
    1. Saito T, Shimazaki Y. Metabolic disorders related to obesity and periodontal disease. Periodontol. 2007;2000(43):254–266. doi: 10.1111/j.1600-0757.2006.00186.x.
    1. Sankaridurg PR, Sharma S, Willcox M, Naduvilath TJ, Sweeney DF, Holden BA, Rao GN. Bacterial colonization of disposable soft contact lenses is greater during corneal infiltrative events than during asymptomatic extended lens wear. J Clin Microbiol. 2000;38(12):4420–4424. doi: 10.1128/JCM.38.12.4420-4424.2000.
    1. Scannapieco FA, Cantos A. Oral inflammation and infection, and chronic medical diseases: implications for the elderly. Periodontol 2000. 2016;72(1):153–175. doi: 10.1111/prd.12129.
    1. Sete MR, Figueredo CM, Sztajnbok F. Periodontitis and systemic lupus erythematosus. Rev Bras Reumatol Engl Ed. 2016;56(2):165–170. doi: 10.1016/j.rbre.2015.09.001.
    1. Shaik MM, Ahmad S, Gan SH, Abuzenadah AM, Ahmad E, Tabrez S, et al. How do periodontal infections affect the onset and progression of Alzheimer’s disease? CNS Neurol Disord Drug Targets. 2014;13(3):460–466. doi: 10.2174/18715273113126660152.
    1. Sng CC, Ang M, Barton K. Uveitis and glaucoma: new insights in the pathogenesis and treatment. Prog Brain Res. 2015;221:243–269. doi: 10.1016/bs.pbr.2015.06.008.
    1. Sohn JH, Bora PS, Jha P, Tezel TH, Kaplan HJ, Bora NS. Complement, innate immunity and ocular disease. Chem Immunol Allergy. 2007;92:105–114. doi: 10.1159/000099261.
    1. Strauss O. The retinal pigment epithelium in visual function. Physiol Rev. 2005;85(3):845–881. doi: 10.1152/physrev.00021.2004.
    1. Tadayoni R. Choroidal neovascularization induces retinal edema and its treatment addresses this problem. J Ophthalmic Vision Res. 2014;9(4):405. doi: 10.4103/2008-322X.150799.
    1. Takahashi K, Sugi Y, Nakano K, Tsuda M, Kurihara K, Hosono A, Kaminogawa S. Epigenetic control of the host gene by commensal bacteria in large intestinal epithelial cells. J Biol Chem. 2011;286:35755–35762. doi: 10.1074/jbc.M111.271007.
    1. Tham YC, Li X, Wong TY, Quigley HA, Aung T, Cheng CY. Global prevalence of glaucoma and projections of glaucoma burden through 2040: a systematic review and meta-analysis. Ophthalmology. 2014;121(11):2081–2090. doi: 10.1016/j.ophtha.2014.05.01.
    1. Topouzis F, Anastasopoulos E, Augood C, Bentham GC, Chakravarthy U, de Jong PT, et al. Association of diabetes with age-related macular degeneration in the EUREYE study. Br J Ophthalmol. 2009;93(8):1037–1041. doi: 10.1136/bjo.2008.146316.
    1. Verhagen FH, Bekker CP, Rossato M, Hiddingh S, de Vries L, Devaprasad A, et al. A disease-associated microRNA cluster links inflammatory pathways and an altered composition of leukocyte subsets to noninfectious uveitis. Invest Ophthalmol Visual Sci. 2018;59(2):878–888. doi: 10.1167/iovs.17-23643.
    1. Wall R, Cryan JF, Ross RP, Fitzgerald GF, Dinan TG, Stanton C. Microbial endocrinology: The microbiota-gut-brain axis in health and disease. New York: Springer; 2014. Bacterial neuroactive compounds produced by psychobiotics; pp. 221–239.
    1. Wang B, Yao M, Lv L, Ling Z, Li L. The Human Microbiota in Health and Disease. Engineering. 2017;3(1):71–82. doi: 10.1016/J.ENG.2017.01.008.
    1. Wen X, Hu X, Miao L, Ge X, Deng Y, Bible PW, Wei L. Epigenetics, microbiota, and intraocular inflammation: New paradigms of immune regulation in the eye. Prog Retin Eye Res. 2018;64:84–95. doi: 10.1016/j.preteyeres.2018.01.001.
    1. Wiggs JL. Genetic etiologies of glaucoma. Arch Ophthalmol. 2007;125(1):30–37. doi: 10.1001/archopht.125.1.30.
    1. Wong WL, Su X, Li X, Cheung CM, Klein R, Cheng CY, Wong TY. Global prevalence of age-related macular degeneration and disease burden projection for 2020 and 2040: a systematic review and meta-analysis. Lancet Glob Health. 2014;2(2):e106–e116. doi: 10.1016/s2214-109x(13)70145-1.
    1. Xie L, Zhai H, Zhao J, Sun S, Shi W, Dong X. Antifungal susceptibility for common pathogens of fungal keratitis in Shandong Province, China. Am J Ophthalmol. 2008;146(2):260–265. doi: 10.1016/j.ajo.2008.04.019.
    1. Xu L, Wang H, Wang Y, Jonas JB. Intraocular pressure correlated with arterial blood pressure: the beijing eye study. Am J Ophthalmol. 2007;144(3):461–462. doi: 10.1016/j.ajo.2007.05.013.
    1. Yucel YH, Johnston MG, Ly T, et al. Identification of lymphatics in the ciliary body of the human eye: a novel “uveolymphatic” outflow pathway. Exp Eye Res. 2009;89:810–819. doi: 10.1016/j.exer.2009.08.010.
    1. Zinkernagel MS, Zysset-Burri DC, Keller I, Berger LE, Leichtle AB, Largiader CR, et al. Association of the intestinal microbiome with the development of neovascular age-related macular degeneration. Sci Rep. 2017;7:40826. doi: 10.1038/srep40826.
    1. Zoellner H. Dental infection and vascular disease. Semin Thromb Hemost. 2011;37(3):181–192. doi: 10.1055/s-0031-1273082.

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner