The role of genetic factors in the pathogenesis of primary open-angle glaucoma. Part 1. Connective tissue

Cover Page
Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract


The article presents an analytical review of works devoted to molecular and genetic studies in primary open-angle glaucoma from the perspective of the concept of hereditary inferiority of the connective tissue of the eye (“scleral component”), and the entire body as a whole, as triggers in the development of the disease. The relationship between the main theories of the pathogenesis of glaucoma optical neuropathy and the determining role of molecular and genetic mechanisms of specific changes in the eye tissue is shown. The clinical features of primary open-angle glaucoma in patients with a family history are analyzed. Potentially new directions for preclinical diagnosis of glaucoma and pathogenetically oriented therapy are proposed.


Full Text

Restricted Access

About the authors

Anastasiia N. Zhuravleva

Helmholtz National Medical Research Center of Eye Diseases

Author for correspondence.
Email: zh.eye@mail.ru
ORCID iD: 0000-0001-8381-2124
SPIN-code: 9358-5060
Scopus Author ID: 554 544

Russian Federation, 14/19 Sadovaya-Chernogryazskaya str., Moscow, 105062

PhD, MD of Highest Qualification, Scientific Researcher

Maria O. Kirillova

Helmholtz National Medical Research Center of Eye Diseases

Email: mkirillova.92@mail.ru
ORCID iD: 0000-0002-1813-4408

Russian Federation, 14/19 Sadovaya-Chernogryazskaya str., Moscow, 105062

Postgraduate Student

Marina V. Zueva

Helmholtz National Medical Research Center of Eye Diseases

Email: visionlab@yandex.ru
ORCID iD: 0000-0002-0161-5010

Russian Federation, 14/19 Sadovaya-Chernogryazskaya str., Moscow, 105062

Dr. Sci. (Biol.), Professor

Vitaliy V. Kadyshev

Research Centre for Medical Genetics

Email: vvh.kad@gmail.com
ORCID iD: 0000-0003-3665-982X

Russian Federation, Moscow

Cand. Sci. (Med.), Senior researcher, Associate Professor

References

  1. Zhuravleva AN, Neroyev VV, Andreyeva LD. Investigation of scleral fibronectin in primary open-angle glaucoma: immunohistochemical study. Vestnik Oftalmologii. 2009;125(3):12–14. (In Russ.)
  2. Sennova LG. A retrospective analysis of the role of connective tissue in the pathogenesis of glaucoma. National Journal Glaucoma. 2018;17(1):113–116. (In Russ.)
  3. Zhuravleva AN. Skleral'nyj komponent v glaukomnoj processe [dissertation]. Мoscow, 2010. (In Russ.)
  4. Fuse N. Genetic bases for glaucoma. Tohoku J Exp Med. 2010;221:1–10. doi: 10.1620/tjem.221.1
  5. Astakhov YS, Rakhmanov VV. Heredity and glaucoma. Ophthalmology Journal. 2012;5(4):51–57. (In Russ.)
  6. Nesterov AP. Glaukoma. Мoscow: Medicinskoe informacionnoe agentstvo, 2008. 360 p. (In Russ.)
  7. Ofri R. Intraocular pressure and glaucoma. Vet Clin North Am Exot Anim Pract. 2002;2:391–406. doi: 10.1016/S1094-9194(01)00004-4
  8. Rasmussen CA, Kaufman PL. The trabecular meshwork in normal eyes and in exfoliation glaucoma. J Glaucoma. 2014;23(8): 15–19. doi: 10.1097/ijg.0000000000000106
  9. Zhuravleva AN, Andreeva LD, Neroev VV. Kollagenovaja teorija starenija i geneticheskij kod v patogeneze glaukomy. Clinical gerontology. 2009;25(8–9):78. (In Russ.)
  10. Kwon HS, Lee HS, Ji Y, et al. Myocilin is a modulator of Wnt signaling. Mol Cell Biol. 2009;29(8):2139–2154. doi: 10.1128/mcb.01274-08
  11. Yuan He, Wah, Zhuo J. Ge Pro370Leu mutant myocilin impairs mitochondrial functions in human trabecular meshwork cells. Mol Vis. 2009;15:815–825.
  12. Fautsch MP, Vrabel AM, Johnson DH. The identification of myocilin-associated proteins in the human trabecular meshwork. Exp Eye Res. 2006;82:1046–1052. doi: 10.1016/j.exer.2005.09.016
  13. Fingert, JH. Primary open-angle glaucoma genes. Eye. 2011;25(5):587–595. doi: 10.1038/eye.2011.97
  14. Nag A, Lu H, Arno M, et al. Evaluation of the Myocilin Mutation Gln368Stop Demonstrates Reduced Penetrance for Glaucoma in European Populations. Ophthalmol. 2017;124(4):547–553. doi: 10.1016/j.ophtha.2016.11.018
  15. Hewitt AW, Mackey DA, Craig JE. Myocilin allele-specific glaucoma phenotype database. Hum Mutat. 2008;29:207–211. doi: 10.1002/humu.20634
  16. Ritch R, Schlotzer-Schrehardt U. Exfoliation syndrome. Surv. Ophthalmol. 2001;45(4):265–315. doi: 10.1016/s0039-6257(00)00196-x
  17. Jeng SM, Karger RA, Hodge DO, et al. The risk of glaucoma in pseudoexfoliation syndrome. J Glaucoma. 2007;16(1):117–121. doi: 10.1097/01.ijg.0000243470.13343.8b
  18. Konstas AG, Hollo G, Astakhov YS, et al. Factors associated with long-term progression or stability in exfoliation glaucoma. Arch ophthalmol. 2004;122(1):29–33. doi: 10.1001/archopht.122.1.29
  19. Aung T, Ozaki M, Lee MC. Genetic association study of exfoliation syndrome identifies a protective rare variant at LOXL1 and five new susceptibility loci. Nat Genet. 2017;49(7):993–1004. doi: 10.1038/ng.3875
  20. Aung T, Chan AS, Khor CC. Genetics of Exfoliation Syndrome. J Glaucoma. 2018;27(1):12–14. doi: 10.1097/IJG.0000000000000928.
  21. Thorleifsson G, Magnusson KP, Sulem P, et al. Common sequence variants in LOXL1 gene confer suspectibility to exfoliation glaucoma. Science. 2007;317(5843):1397–1400. doi: 10.1126/science.1146554
  22. Hewitt AW, Sharma S, Burdon KP, et al. Ancestral LOXL1 variants are associated with pseudoexfoliation in Caucasian Australians but with markedly lower penetrance than in Nordic people. Hum Mol Genet. 2007;17:710–716. doi: 10.1093/hmg/ddm342
  23. Ramprasad VL, George R, Soumittra N, et al. Association of non-synonymous single nucleotide polymorphisms in the LOXL1 gene with pseudoexfoliation syndrome in India. Mol Vis. 2008;14:318–322.
  24. Challa P, Schmidt S, Liu Y, et al. Analysis of LOXL1 polymorphisms in a United States population with pseudoexfoliation glaucoma. Mol Vis. 2008;14:146–149.
  25. Streeten BW, Li ZY, Wallace RN, et al. Pseudoexfoliative fibrillopathy in visceral organs of a patient with pseudoexfoliation syndrome. Arch Ophthalmol. 1992;110:1757–1762. doi: 10.1001/archopht.1992.01080240097039
  26. Wirostko BM, Curtin K, Ritch R, et al. Risk for exfoliation syndrome in women with pelvic organ prolapse: a utah project on exfoliation syndrome (upexs) study. JAMA Ophthalmol. 2016;134(11):1255–1262. doi: 10.1001/jamaophthalmol.2016.3411
  27. Schlotzer-Schrehardt U. Molecular pathology of pseudoexfoliation syndrome/glaucoma – new insights from LOXL1 gene associations. Exp Eye Res. 2009;88:776–785. doi: 10.1016/j.exer.2008.08.012
  28. Taurone S, Ripandelli G, Pacella E, et al. Potential regulatory molecules in the human trabecular meshwork of patients with glaucoma: immunohistochemical profile of a number of inflammatory cytokines. Mol Med Rep. 2015;11(2):1384–1390. doi: 10.3892/mmr.2014.2772
  29. Derakhshan A, Tavakkol AJ, Sadeghi AJ, et al. The Association Between the Transforming Growth Factor Beta-1–509C>T Gene Polymorphism and Primary Open Angle Glaucoma in North Eastern Iran. Rep Biochem Mol Biol. 2019;7(2):167–173.
  30. O'Kane S, Ferguson MW. Transforming growth factor beta s and wound healing. Int J Biochem Cell Biol. 1997;29(1):63–78. doi: 10.1016/s1357-2725(96)00120-3
  31. Jampel HD, Roche N, Stark WJ, Roberts AB. Transforming growth factor-beta in human aqueous humor. Curr Eye Res. 1990;9(10):963–969. doi: 10.3109/02713689009069932
  32. Wiggs JL. Glaucoma Genes and Mechanisms. Prog Mol Biol Transl Sci. 2015;134:315–342. doi: 10.1016/bs.pmbts.2015.04.008
  33. Takano Y, Shi D, Shimizu A, et al. Association of Toll-like receptor 4 gene polymorphisms in Japanese subjects with primary open-angle, normal-tension, and exfoliation glaucoma. Am J Ophthalmol. 2012;154(5):825–832. doi: 10.1016/j.ajo.2012.03.050
  34. Hernandez H, Medina-Ortiz WE, Luan T, et al. Crosstalk Between Transforming Growth Factor Beta-2 and Toll-Like Receptor 4 in the Trabecular Meshwork. Invest Ophthalmol Vis Sci. 2017;58(3): 1811–1823. doi: 10.1167/iovs.16-21331
  35. Fukuchi T, Ueda J, Hanyu T, et al. Distribution and expression of transforming growth factor-beta and platelet-derived growth factor in the normal and glaucomatous monkey optic nerve heads. Jpn J Ophthalmol. 2001;45(6):592–599. doi: 10.1016/s0021-5155(01)00414-2
  36. Izhevskaja VL, Kiseleva, OA, Zhuravleva AN, Halilov SA. Polimorfizmy genov kollagena I i III tipov i ih svjaz' s razvitiem POUG. Russian Journal of Genetics. 2013;12(6):33–37. (In Russ.)
  37. Welge-Lussen U, May CA. Induction of tissue transglutaminase in the trabecular meshwork by TGF-beta l and TGF-beta 2. Invest. Ophthal. Vis. Sci. 2000;41(8): 2229–2238.
  38. Albon J. Age related changes in the non-collagenous components of the extracellular matrix of the human lamina cribrosa. Br J Ophthalmol. 2000;84:311–317. doi: 10.1136/bjo.84.3.311
  39. Agapova, OA, Ricard CS, Salvador-Silva M, Hernandez MR. Expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human optic nerve head astrocytes. Glia. 2001;33(3):205–216. doi: 10.1002/1098-1136(200103)33:3<205:: aid-glia1019>3.0.co;2-d
  40. Kirwan RP, Fenerty CH, Crean J, et al. Influence of cyclical mechanical strain on extracellular matrix gene expression in human lamina cribrosa cells in vitro. Mol Vis. 2005;11:798–810. doi: 10.1016/s0021-9290(06)84552-5
  41. Beletskaya IS, Astakhov SY. The role of matrix metalloproteinases in glaucoma pathogenesis. Ophthalmology Journal. 2015;8(3): 28–43. (In Russ.) doi: 10.17816/OV2015328-43
  42. Hernandez MR, Pena J, Selvidge JA, et al. Hydrostatic pressure stimulates synthesis of elastin in cultured optic nerve head astrocytes. Glia. 2000;32:122–136. doi: 10.1002/1098-1136(200011)32:2<122::aid-glia20>3.0.co;2-j
  43. Реnа I, Agapova О. Increased elastin expression in astrocytes of the lamina cribrosa in response to elevated intraocular pressure. Invest Ophtalmol. 2001;42:2303–2314.
  44. Xu SL, Gao ZZ, Wang Y, Chen J. Expression of matrix metalloproteinases and inhibitors on the scleral tissue of lamina cribrosa in rat with experimental chronic ocular hypertension. Zhonghua Yan Ke Za Zhi. 2009;45(3):260–265.
  45. Fountoulakis N, Labiris G, Aristeidu A, et al. Tissue inhibitor of metalloproteinase 4 in aqueous humor of patients with primary open angle glaucoma, pseudoexfoliation syndrome and pseudoexfoliative glaucoma and its role in proteolysis imbalance. BMC Ophthalmology. 2013;13:69. doi: 10.1186/1471-2415-13-69
  46. Bradley JM, Kelley MJ, Zhu XH, et al. Effect of mechanical stretching on trabecular matrix metalloproteinases. Invest Ophthalmol Vis Sci. 2001;42(7):1505–1513.
  47. Golubnitschaja O, Flammer J. What are the biomarkers for glaucoma? Surv Ophthalmol. 2007;52(2):155–161. doi: 10.1016/j.survophthal.2007.08.011
  48. Fiotti N, Calvagna C, Sgorlon G, et al. Multiple sites of vascular dilation or aneurysmal disease and matrix metalloproteinase genetic variants in patients with abdominal aortic aneurysm. J Vasc Surg. 2017;67(6):1727–1735. doi: 10.1016/j.jvs.2017.09.047
  49. Ji M-L, Jia J. Correlations of TIMP2 and TIMP3 gene polymorphisms with primary open-angle glaucoma. Eur Rev Med Pharmacol Sci. 2019;23(13):5542–5547. doi: 10.26355/eurrev_201907_18287
  50. He M, Wang W, Han X, Huang W. Matrix metalloproteinase-1 rs1799750 polymorphism and glaucoma: A meta-analysis. Ophthalmic Genet. 2017;38(3):211–216. doi: 10.1080/13816810.2016.1193877
  51. Tsironi EE, Pefkianaki M, Tsezou A, et al. Evaluation of MMP1 and MMP3 gene polymorphisms in exfoliation syndrome and exfoliation glaucoma. Mol Vis. 2009;15:2890–2895.
  52. Tezel G. Oxidative stress in glaucomatous neurodegeneration: mechanisms and conseguences. Prog Retin Eye Res. 2006;25: 490–513. doi: 10.1016/j.preteyeres.2006.07.003
  53. Mabuchi F, Tang SA, Kashiwagi K, et al. The OPA1 gene polymorphism is associated with normal tension and high tension glaucoma. Am J Ophthal. 2007;143:125–130. doi: 10.1016/j.ajo.2006. 09.028
  54. Kunal R, Suddhasil M. Molecular complexity of primary open angle glaucoma: current concepts. J Genet. 2009;88(4):451–467. doi: 10.1007/s12041-009-0065-3
  55. Bunin AJ. Patologicheskie faktory destruktivnogo processa v trabekuljarnyh tkanjah pri pervichnoj otkrytougol’noj glaukome. Vestnik Oftalmologii. 2000;116(5):24–27. (In Russ.)
  56. Ferreira SM, Lerner SF, Brunzini R, et al. Antioxidant status in the aqueous humour of patients with glaucoma associated with exfoliation syndrome. Eye. 2009;23(8):1691–1697. doi: 10.1038/eye.2008.352
  57. Metlapally R, Li YJ, Tran-Viet KN, et al. COL1A1 and COL2A1 genes and myopia susceptibility: evidence of association and suggestive linkage to the COL2A1 locus. Invest Ophthalmol Vis Sci. 2009;50(9):4080–4086. doi: 10.1167/iovs.08-3346
  58. Kluivers KB, Dijkstra JR, Hendriks JC, et al. COL3A1 2209G>A is a predictor of pelvic organ prolapse. Int Urogynecol J Pelvic Floor Dysfunct. 2009;20(9):1113–1118. doi: 10.1007/s00192-009-0913-y
  59. Chen HY, Chung YW, Lin WY, et al. Collagen type 3 alpha 1 polymorphism and risk of pelvic organ prolapse. Int J Gynecol Obst. 2008;103(1):55–58. doi: 10.1016/j.ijgo.2008.05.031
  60. Mann V, Ralston SH. Meta-analysis of COL1A1 Sp1 polymorphism in relation to bone mineral density and osteoporotic fracture. Bone. 2003;32(6):711–717. doi: 10.1016/s8756-3282(03)00087-5
  61. Kuleshova ON, Dikovskaja MA, Zajdman AM, Luksha EB. Nasledstvennye narushenija soedinitel'noĭ tkani kak prediktory razvitija pervichnoĭ juvenil'noĭ glaukomy. Fyodorov Journal of Ophthalmic Surgery. 2012;(4):52–55. (In Russ.)
  62. Satybalduev A, Zhuravleva A. Joint hypermobility syndrome and primary open-angle glaucoma. Annals of the rheumatic diseases. BMJ. 2020;79:1819. doi: 10.1136/annrheumdis-2020-eular.1004
  63. Hoffmann EM, Zangwill LM, Crowston JG, Weinreb RN. Optic disk size and glaucoma. Surv Ophthalmol. 2007;52:32–49. doi: 10.1016/j.survophthal.2006.10.002
  64. Chang TC, Congdon NG, Wojciechowski R. Determinants and heritability of intraocular pressure and cup-to-disc ratio in a defined older population. Ophthalmol. 2005;112:1186–1191. doi: 10.1016/j.ophtha.2005.03.006
  65. van Koolwijk LM, Despriet DD, van Duijn CM. Genetic contributions to glaucoma: heritability of intraocular pressure, retinal nerve fiber layer thickness, and optic disc morphology. Invest Ophthalmol Vis Sci. 2007;48:3669–3676. doi: 10.1167/iovs.06-1519
  66. Fan BJ, Wang DY, Pasquale LR, et al. Genetic variants associated with optic nerve vertical cup-to-disc ratio are risk factors for primary open angle glaucoma in a US Caucasian population. Invest Ophthalmol Vis Sci. 2011;52(3):1788–1792. doi: 10.1167/iovs.10-6339
  67. Macgregor S, Hewitt AW, Hysi PG. Genome-wide association identifies ATOH7 as a major gene determining human optic disc size. Hum Mol Genet. 2010;19:2716–2724. doi: 10.1093/hmg/ddq144
  68. Herndon LW, Weizer JS, Stinnett SS. Central corneal thickness as a risk factor for advanced glaucoma damage. Arch Ophthalmol. 2004;122:17–21. doi: 10.1001/archopht.122.1.17
  69. Gaspar R, Pinto LA, Sousa DC. Corneal properties and glauсoma: a review of the literature and meta-analysis. Arq Bras Oftalmol. 2017;80(3):202–206. doi: 10.5935/0004-2749.20170050
  70. Medeiros FA, Sample PA, Weinreb RN. Corneal thickness measurements and visual function abnormalities in ocular hypertensive patients. Am J Ophthalmol. 2003;135:131–137. doi: 10.1016/s0002-9394(02)01886-x
  71. Vithana EN. Collagen-related genes influence the glaucoma risk factor, central corneal thickness. Hum Mol Genet. 2011;20(4): 649–658. doi: 10.1093/hmg/ddq511
  72. Desronvil T, Logan-Wyatt D, Abdrabou W, et al. Distribution of COL8A2 and COL8A1 gene variants in Caucasian primary open angle glaucoma patients with thin central corneal thickness. Mol Vis. 2010;16:2185–2191.
  73. Volkov VV. Glaukoma pri psevdonormal'nom davlenii. Moscow: Medicina, 2001. (In Russ.)
  74. Schmidl D, Garhofer G, Schmetterer L. The complex interaction between ocular perfusion pressure and ocular blood flow-relevance for glaucoma. Exp Eye Res. 2011;93(2):141–155. doi: 10.1016/j.exer.2010.09.002
  75. Chung HS, Harris A, Halter PJ. Regional differences in retinal vascular reactivity. Invest Ophthalmol Vis Sci. 1999;40(10):2448–2453.
  76. Golubnitschaja, O, Yeghiazaryan K, Liu R. Increased expression of matrix metalloproteinases in mononuclear blood cells of normal-tension glaucoma patients. J Glaucoma. 2004;13(1):66–72. doi: 10.1097/00061198-200402000-00013
  77. Zhang X, Chintala SK. Influence of interleukin-1 beta induction and mitogen-activated protein kinase phosphorylation on optic nerve ligation-induced matrix metalloproteinase- 9 activation in the retina. Experimental Eye Research. 2004;78(4):849–860. doi: 10.1016/j.exer.2003.10.018
  78. Agarwal R, Gupta SK. Current concepts in the pathophysiology of glaucoma. J Ophthalmol. 2009;(57)4:257–266. doi: 10.4103/0301-4738.53049
  79. Stewart WF. Familial risk of migraine: Variation by proband age at onset and headache severity. Neurology. 2006;66:344–348. doi: 10.1212/01.wnl.0000196640.71600.00
  80. Neroev VV, Zueva MV, Zhuravleva AN, Tsapenko IV. Structural and Functional Disorders in Glaucoma: the Prospects for Preclinical Diagnosis. Part 1. Is the Search for what Comes First Relevant? Ophthalmology in Russia. 2020;17(3):336–343. (In Russ.) doi: 10.18008/1816-5095-2020-3-336-343
  81. Campuzano V, Segura-Puimedon M, Terrado V, et al. Reduction of NADPH-oxidase activity ameliorates the cardiovascular phenotype in a mouse model of Williams-Beuren Syndrome. PLoS Genet. 2012;8(2): e1002458. doi: 10.1371/journal.pgen.1002458
  82. Zhuravleva AN, Kiseleva OA, Kirillova MO. Personalized medicine in glaucoma management. Russian Ophthalmological Journal. 2019;12(3):95–100. (In Russ.) doi: 10.21516/2072-0076-2019-12-3-95-100

Supplementary files

There are no supplementary files to display.

Statistics

Views

Abstract - 77

PDF (Russian) - 5

Cited-By


Article Metrics

Metrics Loading ...

PlumX

Dimensions


Copyright (c) 2021 Zhuravleva A.N., Kirillova M.O., Zueva M.V., Kadyshev V.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies