Skip to main content
SpringerLink
Log in

Molecular mechanisms of the interaction between the processes of the cell response to mechanical stress and neuronal apoptosis in primary open-angle glaucoma

  • Published:
Russian Journal of Genetics: Applied Research

Abstract

Glaucoma is a chronic progressive disease. It involves more than 60 million people worldwide. Primary open-angle glaucoma (POAG) is one of its commonest forms. About 2.71 million people in the United States suffered from POAG in 2011. Currently, POAG is a major cause of irreversible vision loss. The risk of blindness in patients with treated open-angle glaucoma is 27%. It is known that the death of optic nerve cells can be triggered by mechanical stress caused by ocular hypertension, which induces neuronal apoptosis and occurs in patients with POAG. Many scientific publications are dedicated to proteins and genes involved in the development of POAG, including neuronal apoptosis and the cell response to mechanical stress (CRMS). However, the molecular mechanisms underlying the pathophysiology of POAG are still poorly understood. The reconstruction of associative networks describing the functional interactions between these genes/proteins, including biochemical reactions, regulatory interactions, and transport, requires automated knowledge extraction from scientific publications. This work aims to analyze the associative networks describing molecular interactions between proteins and genes involved in CRMS, neuronal apoptosis, and the development of POAG. It has been shown that genes associated with POAG are statistically significantly overrepresented among the genes involved in the interactions between CRMS and neuronal apoptosis in comparison to what is expected on a random basis. This finding may explain how POAG causes the death of the retinal ganglion cell.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abu-Amero, K.K., Kondkar, A.A., Mousa, A., Azad, T.A., Sultan, T., Osman, E.A., and Al-Obeidan, S.A., Analysis of toll-like receptor rs4986790 polymorphism in Saudi patients with primary open angle glaucoma, Ophthalmic Genet., 2016, vol. 1–5. doi 10.3109/13816810.2016.1151900

  • Almasieh, M., Wilson, A.M., Morquette, B., Vargas, J.L., and Di Polo, A., The molecular basis of retinal ganglion cell death in glaucoma, Prog. Retinal Eye Res., 2012, vol. 31, no. 2, pp. 152–181. preteyeres.2011.11.002 doi 10.1016/j

    Article  CAS  Google Scholar 

  • Au, C.W., Siu, M.K., Liao, X., Wong, E.S., Ngan, H.Y., Tam, K.F., Chan, D.C., Chan, Q.K., and Cheung, A.N., Tyrosine kinase B receptor and BDNF expression in ovarian cancers—effect on cell migration, angiogenesis and clinical outcome, Cancer Lett., 2009, vol. 281, no. 2, pp. 151–161. doi 10.1016/j.canlet.2009.02.025

    CAS  Google Scholar 

  • Badorff, C., Ruetten, H., Mueller, S., Stahmer, M., Gehring, D., Jung, F., Ihling, C., Zeiher, A.M., and Dimmeler, S., Fas receptor signaling inhibits glycogen synthase kinase 3ß and induces cardiac hypertrophy following pressure overload, J. Clin. Invest., 2002, vol. 109, no. 3, pp. 373–381. doi 10.1172/JCI13779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baroni, A., Perfetto, B., Ruocco, E., and Rossano, F., Lipoteichoic acid and protein-A from Staphylococcus aureus stimulate release of hepatocyte growth factor (HGF) by human dermal fibroblasts, Arch. Dermatol. Res., 1998, vol. 290, no. 4, pp. 211–214.

    Article  CAS  PubMed  Google Scholar 

  • Borg, L.A., Cagliero, E.N., Sandler, S.T., Welsh, N., and Eizirik, D.L., Interleukin-1 beta increases the activity of superoxide dismutase in rat pancreatic islets, Endocrinology, 1992, vol. 130, no. 5, pp. 2851–2857. doi 10.1210/endo.130.5.1533363

    Article  CAS  PubMed  Google Scholar 

  • Calandrella, N., Scarsella, G., Pescosolido, N., and Risuleo, G., Degenerative and apoptotic events at retinal and optic nerve level after experimental induction of ocular hypertension, Mol. Cell. Biochem., 2007, vol. 301, nos. 1–2, pp. 155–163. doi 10.1007/s11010-006-9407-0

    Article  CAS  PubMed  Google Scholar 

  • Chu, S.H., Feng, D.F., Ma, Y.B., Zhu, Z.A., Zhang, H., and Qiu, J.H., Stabilization of hepatocyte growth factor mRNA by hypoxia-inducible factor 1, Mol. Biol. Rep., 2009, vol. 36, no. 7, pp. 1967–1975. doi 10.1007/s11033-008-9406-1

    Article  CAS  PubMed  Google Scholar 

  • Demenkov, P.S., Ivanisenko, T.V., Kolchanov, N.A., and Ivanisenko, V.A., ANDVisio: A new tool for graphic visualization and analysis of literature mined associative gene networks in the ANDSystem, In Silico Biol., 2012, vol. 11, nos. 3–4, pp. 149–161. doi 10.3233/ISB-2012-0449

    CAS  Google Scholar 

  • Dorn, G.W. and Kirshenbaum, L.A., Cardiac reanimation: Targeting cardiomyocyte death by BNIP3 and NIX/BNIP3L, Oncogene, 2008, vol. 27, pp. 158–167. doi 10.1038/onc.2009.53

    Article  Google Scholar 

  • Egea, J. and Klein, R., Bidirectional Eph–ephrin signaling during axon guidance, Trends Cell Biol., 2007, vol. 17, no. 5, pp. 230–238. tcb.2007.03.004 doi 10.1016/j

    Article  CAS  PubMed  Google Scholar 

  • Elmore, S., Apoptosis: A review of programmed cell death, Toxicol. Pathol., 2007, vol. 35, no. 4, pp. 495–516. doi 10.1080/01926230701320337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu-lan, W.E., Jie, G.E., Chun-ling, W.A., Hui, W.A., Benjun, Z.H., and Fan, Z.H., Expression of HIF-1a and VEGF in human dental pulp cells under mechanical stretch, Shanghai J. Stomatol., 2012, vol. 21, no. 5.

  • Gawri, R., Rosenzweig, D.H., Krock, E., Ouellet, J.A., Stone, L.S., Quinn, T.M., and Haglund, L., High mechanical strain of primary intervertebral disc cells promotes secretion of inflammatory factors associated with disc degeneration and pain, Arthritis Res. Ther., 2014, vol. 16, no. 1, p. 1. doi 10.1186/ar4449

    Article  Google Scholar 

  • Genander, M. and Frisén, J., Ephrins and Eph receptors in stem cells and cancer, Curr. Opin. Cell Biol., 2010, vol. 22, no. 5, pp. 611–616. doi 10.1016/j.ceb.2010.08.005

    Article  CAS  PubMed  Google Scholar 

  • Glossop, J.R. and Cartmell, S.H., Effect of fluid flowinduced shear stress on human mesenchymal stem cells: Differential gene expression of IL1B and MAP3K8 in MAPK signaling, Gene Expression Patterns, 2009, vol. 9, no. 5, pp. 381–388. doi 10.1016/j.gep.2009.01.001

    Article  CAS  PubMed  Google Scholar 

  • Itakura, T., Peters, D.M., and Fini, M.E., Glaucomatous MYOC mutations activate the IL-1/NF-kB inflammatory stress response and the glaucoma marker SELE in trabecular meshwork cells, Mol. Vision, 2015, vol. 21, p. 1071.

    CAS  Google Scholar 

  • Ivanisenko, V.A., Saik, O.V., Ivanisenko, N.V., Tiys, E.S., Ivanisenko, T.V., Demenkov, P.S., and Kolchanov, N.A., ANDSystem: An associative network discovery system for automated literature mining in the field of biology, BMC Syst. Biol., 2015, vol. 9, no. 2, p. 1. doi 10.1186/1752-0509-9-S2-S2

    Google Scholar 

  • Jindal, V., Glaucoma: An extension of various chronic neurodegenerative disorders, Mol. Neurobiol., 2013, vol. 48, no. 1, pp. 186–189. doi 10.1007/s12035-013-8416-8

    Article  CAS  PubMed  Google Scholar 

  • Jung, J.E., Kim, G.S., Chen, H., Maier, C.M., Narasimhan, P., Song, Y.S., Niizuma, K., Katsu, M., Okami, N., Yoshioka, H., and Sakata, H., Reperfusion and neurovascular dysfunction in stroke: From basic mechanisms to potential strategies for neuroprotection, Mol. Neurobiol., 2010, vol. 41, nos. 2–3, pp. 172–179. doi 10.1007/s12035-010-8102-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kerr, J.F.R., Wyllie, A.H., and Currie, A.R., Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics, Br. J. Cancer, 1972, vol. 26, no. 4, p. 239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klein, A., Maldonado, C., Vargas, L.M., Gonzalez, M., Robledo, F., de Arce, K.P., Muñoz, F.J., Hetz, C., Alvarez, A.R., and Zanlungo, S., Oxidative stress activates the c-Abl/p73 proapoptotic pathway in Niemann-Pick type C neurons, Neurobiol. Dis., 2011, vol. 41, no. 1, pp. 209–218. doi 10.1016/j.nbd.2010.09.008

    Article  CAS  PubMed  Google Scholar 

  • Kullander, K. and Klein, R., Mechanisms and functions of Eph and ephrin signalling, Nat. Rev. Mol. Cell Biol., 2002, vol. 3, no. 7, pp. 475–486. doi 10.1038/nrm856

    Article  CAS  PubMed  Google Scholar 

  • Lascaratos, G., Garway-Heath, D.F., Willoughby, C.E., Chau, K.Y., and Schapira, A.H., Mitochondrial dysfunction in glaucoma: Understanding genetic influences, Mitochondrion, 2012, vol. 12, no. 2, pp. 202–212. doi 10.1016/j.mito.2011.11.004

    Article  CAS  PubMed  Google Scholar 

  • Lu, S., Török, H.P., Gallmeier, E., Kolligs, F.T., Rizzani, A., Arena, S., Goke, B., Gerbes, A.L., and de Toni, E.N., Tivantinib (ARQ 197) affects the apoptotic and proliferative machinery downstream of c-MET: Role of Mcl-1, Bcl-xl and Cyclin B1, Oncotarget, 2015, vol. 6, no. 26, p. 22167. doi 10.18632/oncotarget.4240

    Article  PubMed  Google Scholar 

  • Maity-Kumar, G., Thal, D.R., Baumann, B., Scharffetter-Kochanek, K., and Wirth, T., Neuronal redox imbalance results in altered energy homeostasis and early postnatal lethality, FASEB J., 2015, vol. 29, no. 7, pp. 2843–2858. doi 10.1096/fj.14-265157

    Article  CAS  PubMed  Google Scholar 

  • Matsopoulos, G.K., Asvestas, P.A., Delibasis, K.K., Mouravliansky, N.A., and Zeyen, T.G., Detection of glaucomatous change based on vessel shape analysis, Comput. Med. Imaging Graphics, 2008, vol. 32, no. 3, pp. 183–192. doi 10.1016/j.compmedimag.2007.11.003

    Article  Google Scholar 

  • McCubrey, J.A., Steelman, L.S., Bertrand, F.E., Davis, N.M., Sokolosky, M., Abrams, S.L., Montalto, G., D’Assoro, A.B., Libra, M., Nicoletti, F., and Maestro, R., GSK-3 as potential target for therapeutic intervention in cancer, Oncotarget, 2014, vol. 5, no. 10, pp. 2881–2911. doi 10.18632/oncotarget. 2037

    Article  PubMed  PubMed Central  Google Scholar 

  • Nakagami, H., Morishita, R., Yamamoto, K., Taniyama, Y., Aoki, M., Yamasaki, K., Matsumoto, K., Nakamura, T., Kaneda, Y., and Ogihara, T., Hepatocyte growth factor prevents endothelial cell death through inhibition of bax translocation from cytosol to mitochondrial membrane, Diabetes, 2002, vol. 51, no. 8, pp. 2604–2611.

    Article  CAS  PubMed  Google Scholar 

  • Ozaki, T., Kubo, N., and Nakagawara, A., p73-binding partners and their functional significance, Int. J. Proteomics, 2010. doi 10.1155/2010/283863

    Google Scholar 

  • Paduch, R., Gil, J.J., and Niedziela, P., Hepatocyte growth factor (HGF), heat shock proteins (HSPs) and multidrug resistance protein (MRP) expreßsion in co-culture of colon tumor spheroids with normal cells after incubation with interleukin-1ß (IL-1ß) and/or camptothecin (CPT-11), Indian J. Exp. Biol., 2010, vol. 48, no. 4, pp. 354–364.

    CAS  PubMed  Google Scholar 

  • Park, J., Park, S.Y., Shin, E., Lee, S.H., Kim, Y.S., Lee, D.H., Roh, G.S., Kim, H.J., Kang, S.S., Cho, G.J., and Jeong, B.Y., Hypoxia inducible factor-1a directly regulates nuclear clusterin transcription by interacting with hypoxia response elements in the clusterin promoter, Mol. Cells, 2014, vol. 37, no. 2, pp. 178–186. doi 10.14348/molcells.2014.2349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quigley, H.A., Neuronal death in glaucoma, Prog. Retinal Eye Res., 1999, vol. 18, no. 1, pp. 39–57.

    Article  CAS  Google Scholar 

  • Quigley, H.A., Glaucoma, Lancet, 2011, vol. 377, no. 9774, pp. 1367–1377. doi 10.1016/S0140-6736(10)61423-7

    Article  PubMed  Google Scholar 

  • Rong, S.S., Chen, L.J., Leung, C.K., Matsushita, K., Jia, L., Miki, A., Chiang, S.W., Tam, P.O., Hashida, N., Young, A.L., and Tsujikawa, M., Ethnic specific association of the CAV1/CAV2 locus with primary open-angle glaucoma, Sci. Rep., 2016, vol. 6, p. 27837. 27837 doi 10.1038/srep

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao, Q., Arakaki, N., Ohnishi, T., Nakamura, O., and Daikuhara, Y., Effect of hepatocyte growth factor/scatter factor on lipogenesis in adult rat hepatocytes in primary culture, J. Biochem., 1996, vol. 119, no. 5, pp. 940–946.

    Article  CAS  PubMed  Google Scholar 

  • Slemmer, J.E., Zhu, C., Landshamer, S., Trabold, R., Grohm, J., Ardeshiri, A., Wagner, E., Sweeney, M.I., Blomgren, K., Culmsee, C., and Weber, J.T., Causal role of apoptosis-inducing factor for neuronal cell death following traumatic brain injury, Am. J. Pathol., 2008, vol. 173, no. 6, pp. 1795–1805. doi 10.2353/ajpath.2008.080168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun, R.J., Muller, S., Zhuang, F.Y., Stoltz, J.F., and Wang, X., Caveolin-1 redistribution in human endothelial cells induced by laminar flow and cytokine, Biorheology, 2003, vol. 40, nos. 1,2, 3, pp. 31–39.

    CAS  PubMed  Google Scholar 

  • Takano, Y., Shi, D., Shimizu, A., Funayama, T., Mashima, Y., Yasuda, N., Fukuchi, T., Abe, H., Ideta, H., Zheng, X., and Shiraishi, A., Association of Toll-like receptor 4 gene polymorphisms in Japanese subjects with primary openangle, normal-tension, and exfoliation glaucoma, Am. J. Ophthalmol., 2012, vol. 154, no. 5, pp. 825–832. doi 10.1016/j.ajo.2012.03.050

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi, F., Harada, T., Deura, I., Iwabe, T., Tsukihara, S., and Terakawa, N., Hepatocyte growth factor promotes cell proliferation and inhibits progesterone secretion via PKA and MAPK pathways in a human granulosa cell line, Mol. Reprod. Dev., 2004, vol. 68, no. 3, pp. 335–344. doi 10.1002/mrd.20076

    Article  CAS  PubMed  Google Scholar 

  • Uchida, K., Nakajima, H., Takamura, T., Furukawa, S., Kobayashi, S., Yayama, T., and Baba, H., Gene expression profiles of neurotrophic factors in rat cultured spinal cord cells under cyclic tensile stress, Spine, 2008, vol. 33, no. 24, pp. 2596–2604. doi 10.1097/BRS.0b013e31818917af

    Article  PubMed  Google Scholar 

  • Wang, F., Xiong, L., Huang, X., Zhao, T., Wu, L.Y., Liu, Z.H., Ding, X., Liu, S., Wu, Y., Zhao, Y., and Wu, K., miR-210 suppresses BNIP3 to protect against the apoptosis of neural progenitor cells, Stem Cell Res., 2013, vol. 11, no. 1, pp. 657–667. doi 10.1016/j.scr.2013.04.005

    Article  CAS  PubMed  Google Scholar 

  • Zhao, Y., Zhu, L., Yu, S., Zhu, J., and Wang, C., CaMKII inhibition promotes neuronal apoptosis by transcriptionally upregulating Bim expression, NeuroReport, 2016, vol. 27, no. 14, pp. 1018–1023. doi 10.1097/WNR.0000000000000648

    Article  CAS  PubMed  Google Scholar 

  • Zhou, Y., Millward-Sadler, S.J., Lin, H., Robinson, H., Goldring, M., Salter, D.M., and Nuki, G., Evidence for JNK-dependent up-regulation of proteoglycan synthesis and for activation of JNK1 following cyclical mechanical stimulation in a human chondrocyte culture model, Osteo- Arthritis Cartilage, 2007, vol. 15, no. 8, pp. 884–893. doi 10.1016/j.joca.2007.02.001

    Article  CAS  Google Scholar 

  • Zhou, Y., Shuai, P., Li, X., Liu, X., Wang, J., Yang, Y., Hao, F., Lin, H., Zhang, D., and Gong, B., Association of SOD2 polymorphisms with primary open angle glaucoma in a Chinese population, Ophthalmic Genet., 2015, vol. 36, no. 1, pp. 43–49. doi 10.3109/13816810.2014.985844

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cytology and Genetics, Siberian Branch, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    O. V. Saik, P. S. Demenkov, N. V. Ivanisenko, T. V. Ivanisenko, D. E. Ivanoshchuk, O. A. Podkolodnaya, I. N. Lavrik, N. A. Kolchanov & V. A. Ivanisenko

  2. Tyumen State Medical University, Tyumen, 625023, Russia

    N. A. Konovalova & O. S. Konovalova

  3. Novosibirsk State University, Novosibirsk, 630090, Russia

    N. V. Ivanisenko

  4. Institute of Experimental Internal Medicine, Otto von Guericke University, Magdeburg, 39120, Germany

    I. N. Lavrik

Authors
  1. O. V. Saik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. A. Konovalova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. S. Demenkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. V. Ivanisenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. V. Ivanisenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. D. E. Ivanoshchuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. O. S. Konovalova
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. O. A. Podkolodnaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. I. N. Lavrik
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. N. A. Kolchanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. V. A. Ivanisenko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to O. V. Saik.

Additional information

Original Russian Text © O.V. Saik, N.A. Konovalova, P.S. Demenkov, N.V. Ivanisenko, T.V. Ivanisenko, D.E. Ivanoshchuk, O.S. Konovalova, O.A. Podkolodnaya, I.N. Lavrik, N.A. Kolchanov, V.A. Ivanisenko, 2016, published in Vavilovskii Zhurnal Genetiki i Selektsii, 2016, Vol. 20, No. 6, pp. 840–847.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Saik, O.V., Konovalova, N.A., Demenkov, P.S. et al. Molecular mechanisms of the interaction between the processes of the cell response to mechanical stress and neuronal apoptosis in primary open-angle glaucoma. Russ J Genet Appl Res 7, 558–564 (2017). https://doi.org/10.1134/S2079059717050173

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079059717050173

Keywords

Search

Navigation