MicroRNA in the pathogenesis of glaucoma Review article
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Published:
Dec 9, 2020
Keywords:
microRNA, glaucoma, trabecular meshwork, oxidative stress
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Abstract
MicroRNAs are short ribonucleic acid molecules that regulate gene expression. The involvement of various types of microRNAs in the pathogenesis of glaucoma has been proved. Most of them affect trabecular meshwork in the anterior chamber angle, causing excessive deposition of extracellular matrix and blockage of the aqueous humor outflow. MicroRNAs affect the contractility of the trabecular meshwork cells, decreasing its permeability and increasing intraocular pressure. They participate in the regulation of apoptosis of trabecular meshwork cells and retinal ganglion cells. MicroRNAs may be potential biomarkers for glaucoma and, in the future, a target for gene therapy.
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1.
Gasińska K, Kosior-Jarecka E, Żarnowski T. MicroRNA in the pathogenesis of glaucoma. Ophthatherapy [Internet]. 2020Dec.9 [cited 2024Nov.22];7(4):277-86. Available from: https://journalsmededu.pl/index.php/ophthatherapy/article/view/1108
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Diagnostics
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Address reprint requests to: Medical Education, Marcin Kuźma (marcin.kuzma@mededu.pl)
References
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6. Dellago H, Bobbili MR, Grillari J. MicroRNA-17-5p: At the Crossroads of Cancer and Aging – A Mini-Review. Gerontology. 2017; 63: 20-8.
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8. Juźwik CA, S. Drake S, Zhang Y et al. microRNA dysregulation in neurodegenerative diseases: A systematic review. Prog Neurobiol. 2019; 182: 101664. https://doi.org/10.1016/j.pneurobio.2019.101664.
9. Lagos-Quintana M, Rauhut R, Meyer J et al. New microRNAs from mouse and human. RNA. 2003; 9: 175-9.
10. Raghunath A, Perumal E. Micro-RNAs and Their Roles in Eye Disorders. Ophthalmic Res. 2015; 53: 169-86.
11. Woeller CF, Roztocil E, Hammond C et al. TSHR Signaling Stimulates Proliferation Through PI3K/Akt and Induction of miR-146a and miR-155 in Thyroid Eye Disease Orbital Fibroblasts. Invest Ophthalmol Vis Sci. 2019; 60: 4336-45.
12. Puccetti A, Pelosi A, Fiore PF et al. MicroRNA Expression Profiling in Behçet’s Disease. J Immunol Res. 2018; 2018: 2405150.
13. Chang R, Yi S, Tan X et al. MicroRNA-20a-5p suppresses IL-17 production by targeting OSM and CCL1 in patients with Vogt-Koyanagi-Harada disease. Br J Ophthalmol. 2018; 102: 282-90.
14. Pilson Q, Smith S, Jefferies CA et al. miR-744-5p contributes to ocular inflammation in patients with primary Sjogrens Syndrome. Sci Rep. 2020; 10: 7484.
15. Poczęta M, Nowak E, Bieg D et al. Epigenetic modifications and gene expression in cancerogenesis. Ann Acad Med Siles. 2018; 72: 80-9.
16. Quigley HA. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006; 90: 262-7.
17. Wróbel-Dudzińska D, Kosior-Jarecka E, Łukasik U et al. Risk Factors in Normal-Tension Glaucoma and High-Tension Glaucoma in relation to Polymorphisms of Endothelin-1 Gene and Endothelin-1 Receptor Type A Gene. J Ophthalmol. 2015; 2015: 1-12.
18. Weinreb RN, Aung T, Medeiros FA. The Pathophysiology and Treatment of Glaucoma: A Review. JAMA. 2014; 311: 1901-11.
19. Jayaram H, Phillips JI, Lozano DC et al. Comparison of MicroRNA Expression in Aqueous Humor of Normal and Primary Open-Angle Glaucoma Patients Using PCR Arrays: A Pilot Study. Invest Ophthalmol Vis Sci. 2017; 58: 2884-90.
20. Drewry MD, Challa P, Kuchtey JG et al. Differentially expressed microRNAs in the aqueous humor of patients with exfoliation glaucoma or primary open-angle glaucoma. Hum Mol Genet. 2018; 27: 1263-75.
21. Stamer WD, Clark AF. The many faces of the trabecular meshwork cell. Exp Eye Res. 2017; 158: 112-23.
22. Vranka JA, Kelley MJ, Acott TS et al. Extracellular matrix in the trabecular meshwork: Intraocular pressure regulation and dysregulation in glaucoma. Exp Eye Res. 2015; 133: 112-25.
23. Kasetti RB, Maddineni P, Millar JC et al. Increased synthesis and deposition of extracellular matrix proteins leads to endoplasmic reticulum stress in the trabecular meshwork. Sci Rep. 2017; 7: 14951.
24. Nita M, Grzybowski A. The Role of the Reactive Oxygen Species and Oxidative Stress in the Pathomechanism of the Age-Related Ocular Diseases and Other Pathologies of the Anterior and Posterior Eye Segments in Adults. Oxid Med Cell Longev. 2016; 2016: 1-23.
25. Sarniak A, Lipińska J, Tytman K et al. Endogenne mechanizmy powstawania reaktywnych form tlenu (ROS). Postepy Hig Med Dosw. 2016; 70: 1150-64.
26. Izzotti A, Saccà SC, Longobardi M et al. Sensitivity of ocular anterior chamber tissues to oxidative damage and its relevance to the pathogenesis of glaucoma. Invest Ophthalmol Vis Sci. 2009; 50: 5251-8.
27. Ferreira SM, Lerner SF, Brunzini R et al. Oxidative stress markers in aqueous humor of glaucoma patients. Am J Ophthalmol. 2004; 137: 62-9.
28. Mozaffarieh M, Grieshaber MC, Flammer J. Oxygen and blood flow: players in the pathogenesis of glaucoma. Mol Vis. 2008; 14: 224-33.
29. Braunger BM, Fuchshofer R, Tamm ER. The aqueous humor outflow pathways in glaucoma: A unifying concept of disease mechanisms and causative treatment. Eur J Pharm Biopharm. 2015; 95: 173-81.
30. Li G, Luna C, Qiu J et al. Targeting of Integrin β1 and Kinesin 2α by MicroRNA 183. J Biol Chem. 2010; 285: 5461-71.
31. Luna C, Li G, Qiu J et al. Role of miR-29b on the regulation of the extracellular matrix in human trabecular meshwork cells under chronic oxidative stress. Mol Vis. 2009; 15: 2488-97.
32. Villarreal G, Oh D-J, Kang MH et al. Coordinated Regulation of Extracellular Matrix Synthesis by the MicroRNA-29 Family in the Trabecular Meshwork. Invest Ophthalmol Vis Sci. 2011; 52: 3391-7.
33. Fuchshofer R, Stephan DA, Russell P et al. Gene expression profiling of TGFβ2- and/or BMP7-treated trabecular meshwork cells: Identification of Smad7 as a critical inhibitor of TGF-β2 signaling. Exp Eye Res. 2009; 88: 1020-32.
34. Yin R, Chen X. Regulatory effect of miR‑144‑3p on the function of human trabecular meshwork cells and fibronectin‑1. Exp Ther Med. 2019; 18: 647-53.
35. Luna C, Li G, Qiu J et al. MicroRNA-24 regulates the processing of latent TGFβ1 during cyclic mechanical stress in human trabecular meshwork cells through direct targeting of FURIN. J Cell Physiol. 2011; 226: 1407-14.
36. Luna C, Li G, Huang J et al. Regulation of Trabecular Meshwork Cell Contraction and Intraocular Pressure by miR-200c. PLoS One. 2012; 7: e51688.
37. Li X, Zhao F, Xin M et al. Regulation of intraocular pressure by microRNA cluster miR-143/145. Sci Rep. 2017; 7: 915.
38. Klein BEK. Intraocular pressure and systemic blood pressure: longitudinal perspective: the Beaver Dam Eye Study. Brit J Ophthalmol. 2005; 89: 284-7.
39. Skrzypecki J, Grabska-Liberek I, Przybek J et al. A common humoral background of intraocular and arterial blood pressure dysregulation. Curr Med Res Opin. 2018; 34: 521-9.
40. Wang X, Li Z, Bai J et al. MiR‑17‑5p regulates the proliferation and apoptosis of human trabecular meshwork cells by targeting phosphatase and tensin homolog. Mol Med Report. 2019; 19: 3132-8.
41. Tezel G. Oxidative stress in glaucomatous neurodegeneration: Mechanisms and consequences. Prog Retin Eye Res. 2006; 25: 490-513.
42. Izzotti A, Ceccaroli C, Longobardi M et al. Molecular Damage in Glaucoma: from Anterior to Posterior Eye Segment. The MicroRNA Role. MiRNA. 2015; 4: 3-17.
43. Pałasz E, Bąk A, Gąsiorowska A et al. The role of trophic factors and inflammatory processes in physical activity-induced neuroprotection in Parkinson’s disease. Postepy Hig Med Dosw. 2017; 71: 713-26.
44. Czajkowski J, Depczyńska M, Hein K et al. Rola naczyniowych czynników ryzyka i ich występowanie w polskiej populacji chorych na jaskrę. Wyniki 14 208 badań ankietowych. Okulistyka – wyd. spec 2003; 1-8.
45. Parisi V, Oddone F, Ziccardi L et al. Citicoline and Retinal Ganglion Cells: Effects on Morphology and Function. Curr Neuropharmacol. 2018; 16: 919-32.
46. Kong N, Lu X, Li B. Downregulation of microRNA-100 protects apoptosis and promotes neuronal growth in retinal ganglion cells. BMC Mol Biol. 2014; 15: 25.
47. Machaliński B, Łażewski-Banaszak P, Dąbkowska E et al. Rola czynników neurotroficznych w procesach regeneracji układu nerwowego. Neurol Neurochir Pol. 2012; 46: 579-90.
48. Chitranshi N, Dheer Y, Abbasi M et al. Glaucoma Pathogenesis and Neurotrophins: Focus on the Molecular and Genetic Basis for Therapeutic Prospects. Curr Neuropharmacol. 2018; 16: 1018-35.
49. Saccà SC, Pulliero A, Izzotti A. The Dysfunction of the Trabecular Meshwork During Glaucoma Course. J Cell Physiol. 2015; 230: 510-25.
50. Van den Pol AN. Neuropeptide transmission in brain circuits. Neuron. 2012; 76: 98-115.
51. Duan X, Lu Q, Xue P et al. Proteomic analysis of aqueous humor from patients with myopia. Mol Vis. 2008; 14: 370-7.
52. Wang LM, Dong LJ, Liu X et al. Proteomic analysis of aqueous humor in acute primary angle-closure glaucoma. Zhonghua Yan Ke Za Zhi. 2019; 55: 687-94.
53. Johnson M, McLaren JW, Overby DR. Unconventional aqueous humor outflow: A review. Exp Eye Res. 2017; 158: 94-111.
54. Bosco A, Crish SD, Steele MR et al. Early reduction of microglia activation by irradiation in a model of chronić glaucoma. PLoS One. 2012; 7: e43602.
55. Tezel G, Wax MB. Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000; 20: 8693-700.
56. Nakazawa T, Nakazawa C, Matsubara A et al. Tumor Necrosis Factor- Mediates Oligodendrocyte Death and Delayed Retinal Ganglion Cell Loss in a Mouse Model of Glaucoma. J Neurosci. 2006; 26: 12633-41.
57. Echevarria F, Walker C, Abella S et al. Stressor-dependent Alterations in Glycoprotein 130: Implications for Glial Cell Reactivity, Cytokine Signaling and Ganglion Cell Health in Glaucoma. J Clin Exp Ophthalmol. 2013; 4: 1000286.
58. Mossböck G, Weger M, Faschinger C et al. Role of functional single nucleotide polymorphisms of MMP1, MMP2, and MMP9 in open angle glaucomas. Mol Vis. 2010; 16: 1764-70.
59. Toda N, Nakanishitoda M. Nitric oxide: Ocular blood flow, glaucoma, and diabetic retinopathy. Prog Retin Eye Res. 2007; 26: 205-38.
60. Goswami R, Subramanian G, Silayeva L et al. Gene Therapy Leaves a Vicious Cycle. Front Oncol. 2019; 9: 297.
2. Świstek J, Kwiecień J, Starska K. Rola wybranych microRNA w procesie neoplazmatycznym. Otorynolaryngologia. 2017; 16: 81-7.
3. Kopczyński P, Krawczyński MR. Rola onkogenów i genów supresji nowotworów w onkogenezie. Now Lek. 2012; 81: 679-81.
4. Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993; 75: 843-54.
5. Sosińska P, Mikuła-Pietrasik J, Książek K. Molekularne podstawy komórkowego starzenia: fenomen Hayflicka 50 lat później. Postepy Hig Med Dosw. 2016; 70: 231-42.
6. Dellago H, Bobbili MR, Grillari J. MicroRNA-17-5p: At the Crossroads of Cancer and Aging – A Mini-Review. Gerontology. 2017; 63: 20-8.
7. Kumar S, Vijayan M, Bhatti JS et al. MicroRNAs as Peripheral Biomarkers in Aging and Age-Related Diseases. Prog Mol Biol Transl. 2017; 146: 47-94.
8. Juźwik CA, S. Drake S, Zhang Y et al. microRNA dysregulation in neurodegenerative diseases: A systematic review. Prog Neurobiol. 2019; 182: 101664. https://doi.org/10.1016/j.pneurobio.2019.101664.
9. Lagos-Quintana M, Rauhut R, Meyer J et al. New microRNAs from mouse and human. RNA. 2003; 9: 175-9.
10. Raghunath A, Perumal E. Micro-RNAs and Their Roles in Eye Disorders. Ophthalmic Res. 2015; 53: 169-86.
11. Woeller CF, Roztocil E, Hammond C et al. TSHR Signaling Stimulates Proliferation Through PI3K/Akt and Induction of miR-146a and miR-155 in Thyroid Eye Disease Orbital Fibroblasts. Invest Ophthalmol Vis Sci. 2019; 60: 4336-45.
12. Puccetti A, Pelosi A, Fiore PF et al. MicroRNA Expression Profiling in Behçet’s Disease. J Immunol Res. 2018; 2018: 2405150.
13. Chang R, Yi S, Tan X et al. MicroRNA-20a-5p suppresses IL-17 production by targeting OSM and CCL1 in patients with Vogt-Koyanagi-Harada disease. Br J Ophthalmol. 2018; 102: 282-90.
14. Pilson Q, Smith S, Jefferies CA et al. miR-744-5p contributes to ocular inflammation in patients with primary Sjogrens Syndrome. Sci Rep. 2020; 10: 7484.
15. Poczęta M, Nowak E, Bieg D et al. Epigenetic modifications and gene expression in cancerogenesis. Ann Acad Med Siles. 2018; 72: 80-9.
16. Quigley HA. The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol. 2006; 90: 262-7.
17. Wróbel-Dudzińska D, Kosior-Jarecka E, Łukasik U et al. Risk Factors in Normal-Tension Glaucoma and High-Tension Glaucoma in relation to Polymorphisms of Endothelin-1 Gene and Endothelin-1 Receptor Type A Gene. J Ophthalmol. 2015; 2015: 1-12.
18. Weinreb RN, Aung T, Medeiros FA. The Pathophysiology and Treatment of Glaucoma: A Review. JAMA. 2014; 311: 1901-11.
19. Jayaram H, Phillips JI, Lozano DC et al. Comparison of MicroRNA Expression in Aqueous Humor of Normal and Primary Open-Angle Glaucoma Patients Using PCR Arrays: A Pilot Study. Invest Ophthalmol Vis Sci. 2017; 58: 2884-90.
20. Drewry MD, Challa P, Kuchtey JG et al. Differentially expressed microRNAs in the aqueous humor of patients with exfoliation glaucoma or primary open-angle glaucoma. Hum Mol Genet. 2018; 27: 1263-75.
21. Stamer WD, Clark AF. The many faces of the trabecular meshwork cell. Exp Eye Res. 2017; 158: 112-23.
22. Vranka JA, Kelley MJ, Acott TS et al. Extracellular matrix in the trabecular meshwork: Intraocular pressure regulation and dysregulation in glaucoma. Exp Eye Res. 2015; 133: 112-25.
23. Kasetti RB, Maddineni P, Millar JC et al. Increased synthesis and deposition of extracellular matrix proteins leads to endoplasmic reticulum stress in the trabecular meshwork. Sci Rep. 2017; 7: 14951.
24. Nita M, Grzybowski A. The Role of the Reactive Oxygen Species and Oxidative Stress in the Pathomechanism of the Age-Related Ocular Diseases and Other Pathologies of the Anterior and Posterior Eye Segments in Adults. Oxid Med Cell Longev. 2016; 2016: 1-23.
25. Sarniak A, Lipińska J, Tytman K et al. Endogenne mechanizmy powstawania reaktywnych form tlenu (ROS). Postepy Hig Med Dosw. 2016; 70: 1150-64.
26. Izzotti A, Saccà SC, Longobardi M et al. Sensitivity of ocular anterior chamber tissues to oxidative damage and its relevance to the pathogenesis of glaucoma. Invest Ophthalmol Vis Sci. 2009; 50: 5251-8.
27. Ferreira SM, Lerner SF, Brunzini R et al. Oxidative stress markers in aqueous humor of glaucoma patients. Am J Ophthalmol. 2004; 137: 62-9.
28. Mozaffarieh M, Grieshaber MC, Flammer J. Oxygen and blood flow: players in the pathogenesis of glaucoma. Mol Vis. 2008; 14: 224-33.
29. Braunger BM, Fuchshofer R, Tamm ER. The aqueous humor outflow pathways in glaucoma: A unifying concept of disease mechanisms and causative treatment. Eur J Pharm Biopharm. 2015; 95: 173-81.
30. Li G, Luna C, Qiu J et al. Targeting of Integrin β1 and Kinesin 2α by MicroRNA 183. J Biol Chem. 2010; 285: 5461-71.
31. Luna C, Li G, Qiu J et al. Role of miR-29b on the regulation of the extracellular matrix in human trabecular meshwork cells under chronic oxidative stress. Mol Vis. 2009; 15: 2488-97.
32. Villarreal G, Oh D-J, Kang MH et al. Coordinated Regulation of Extracellular Matrix Synthesis by the MicroRNA-29 Family in the Trabecular Meshwork. Invest Ophthalmol Vis Sci. 2011; 52: 3391-7.
33. Fuchshofer R, Stephan DA, Russell P et al. Gene expression profiling of TGFβ2- and/or BMP7-treated trabecular meshwork cells: Identification of Smad7 as a critical inhibitor of TGF-β2 signaling. Exp Eye Res. 2009; 88: 1020-32.
34. Yin R, Chen X. Regulatory effect of miR‑144‑3p on the function of human trabecular meshwork cells and fibronectin‑1. Exp Ther Med. 2019; 18: 647-53.
35. Luna C, Li G, Qiu J et al. MicroRNA-24 regulates the processing of latent TGFβ1 during cyclic mechanical stress in human trabecular meshwork cells through direct targeting of FURIN. J Cell Physiol. 2011; 226: 1407-14.
36. Luna C, Li G, Huang J et al. Regulation of Trabecular Meshwork Cell Contraction and Intraocular Pressure by miR-200c. PLoS One. 2012; 7: e51688.
37. Li X, Zhao F, Xin M et al. Regulation of intraocular pressure by microRNA cluster miR-143/145. Sci Rep. 2017; 7: 915.
38. Klein BEK. Intraocular pressure and systemic blood pressure: longitudinal perspective: the Beaver Dam Eye Study. Brit J Ophthalmol. 2005; 89: 284-7.
39. Skrzypecki J, Grabska-Liberek I, Przybek J et al. A common humoral background of intraocular and arterial blood pressure dysregulation. Curr Med Res Opin. 2018; 34: 521-9.
40. Wang X, Li Z, Bai J et al. MiR‑17‑5p regulates the proliferation and apoptosis of human trabecular meshwork cells by targeting phosphatase and tensin homolog. Mol Med Report. 2019; 19: 3132-8.
41. Tezel G. Oxidative stress in glaucomatous neurodegeneration: Mechanisms and consequences. Prog Retin Eye Res. 2006; 25: 490-513.
42. Izzotti A, Ceccaroli C, Longobardi M et al. Molecular Damage in Glaucoma: from Anterior to Posterior Eye Segment. The MicroRNA Role. MiRNA. 2015; 4: 3-17.
43. Pałasz E, Bąk A, Gąsiorowska A et al. The role of trophic factors and inflammatory processes in physical activity-induced neuroprotection in Parkinson’s disease. Postepy Hig Med Dosw. 2017; 71: 713-26.
44. Czajkowski J, Depczyńska M, Hein K et al. Rola naczyniowych czynników ryzyka i ich występowanie w polskiej populacji chorych na jaskrę. Wyniki 14 208 badań ankietowych. Okulistyka – wyd. spec 2003; 1-8.
45. Parisi V, Oddone F, Ziccardi L et al. Citicoline and Retinal Ganglion Cells: Effects on Morphology and Function. Curr Neuropharmacol. 2018; 16: 919-32.
46. Kong N, Lu X, Li B. Downregulation of microRNA-100 protects apoptosis and promotes neuronal growth in retinal ganglion cells. BMC Mol Biol. 2014; 15: 25.
47. Machaliński B, Łażewski-Banaszak P, Dąbkowska E et al. Rola czynników neurotroficznych w procesach regeneracji układu nerwowego. Neurol Neurochir Pol. 2012; 46: 579-90.
48. Chitranshi N, Dheer Y, Abbasi M et al. Glaucoma Pathogenesis and Neurotrophins: Focus on the Molecular and Genetic Basis for Therapeutic Prospects. Curr Neuropharmacol. 2018; 16: 1018-35.
49. Saccà SC, Pulliero A, Izzotti A. The Dysfunction of the Trabecular Meshwork During Glaucoma Course. J Cell Physiol. 2015; 230: 510-25.
50. Van den Pol AN. Neuropeptide transmission in brain circuits. Neuron. 2012; 76: 98-115.
51. Duan X, Lu Q, Xue P et al. Proteomic analysis of aqueous humor from patients with myopia. Mol Vis. 2008; 14: 370-7.
52. Wang LM, Dong LJ, Liu X et al. Proteomic analysis of aqueous humor in acute primary angle-closure glaucoma. Zhonghua Yan Ke Za Zhi. 2019; 55: 687-94.
53. Johnson M, McLaren JW, Overby DR. Unconventional aqueous humor outflow: A review. Exp Eye Res. 2017; 158: 94-111.
54. Bosco A, Crish SD, Steele MR et al. Early reduction of microglia activation by irradiation in a model of chronić glaucoma. PLoS One. 2012; 7: e43602.
55. Tezel G, Wax MB. Increased production of tumor necrosis factor-alpha by glial cells exposed to simulated ischemia or elevated hydrostatic pressure induces apoptosis in cocultured retinal ganglion cells. J Neurosci. 2000; 20: 8693-700.
56. Nakazawa T, Nakazawa C, Matsubara A et al. Tumor Necrosis Factor- Mediates Oligodendrocyte Death and Delayed Retinal Ganglion Cell Loss in a Mouse Model of Glaucoma. J Neurosci. 2006; 26: 12633-41.
57. Echevarria F, Walker C, Abella S et al. Stressor-dependent Alterations in Glycoprotein 130: Implications for Glial Cell Reactivity, Cytokine Signaling and Ganglion Cell Health in Glaucoma. J Clin Exp Ophthalmol. 2013; 4: 1000286.
58. Mossböck G, Weger M, Faschinger C et al. Role of functional single nucleotide polymorphisms of MMP1, MMP2, and MMP9 in open angle glaucomas. Mol Vis. 2010; 16: 1764-70.
59. Toda N, Nakanishitoda M. Nitric oxide: Ocular blood flow, glaucoma, and diabetic retinopathy. Prog Retin Eye Res. 2007; 26: 205-38.
60. Goswami R, Subramanian G, Silayeva L et al. Gene Therapy Leaves a Vicious Cycle. Front Oncol. 2019; 9: 297.