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Chronobiological approaches to studying the progression of primary open-angle glaucoma

https://doi.org/10.53432/2078-4104-2025-24-3-52-64

Abstract

Recent advances in chronobiology have provided new insights into the nature of complex changes in the temporal reorganization of biological processes in the body that occur with aging. The risk of developing and progressing primary open-angle glaucoma (POAG) increases dramatically with age. In recent years, glaucoma has been regarded to as a dysregulatory condition characterized by impaired integrity and hierarchy in the self-regulation and homeostatic systems of the body. The review article presents data from Russian and foreign researchers on the study of chronobiological aspects in the pathogenesis of glaucoma.

About the Authors

T. N. Malishevskaya
Helmholtz National Medical Research Center of Eye Diseases
Russian Federation

Dr. Sci. (Med.), Head of the Department of Analytical Work, Associate Professor at the Department of Continuing Medical Education

14/19 Sadovaya-Chernogryazskaya St., Moscow, 105064 



E. V. Renziak
West Siberian Institute of Postgraduate Medical Education ; District Clinical Hospital of the Khanty-Mansi Autonomous Okrug – Yugra
Russian Federation

Assistant Professor at the Academic Department of Ophthalmology, Head of the Inpatient Department of the Ophthalmological Center

5/11 Prokopy Artamonov St., Tyumen, 625051

40 Kalinina St., Khanty-Mansiysk, 628012



D. G. Gubin
Tyumen State Medical University ; Tyumen Cardiology Research Center — branch of the Tomsk Scientific Research Center of the Russian Academy of Sciences
Russian Federation

Dr. Sci. (Med.), Professor, Head of the Laboratory of Chronobiology and Chronomedicine at the University Research Institute of Biotechnology and Biomedicine, Professor at the Academic Department of Biology, Leading Researcher at the Department of Arterial Hypertension and Coronary Insufficiency of the Scientific Department of Clinical Cardiology

54 Odesskaya St., Tyumen, 625150

111 Melnikaite St., Tyumen, 625026



S. N. Kolomeychuk
Tyumen State Medical University ; Karelian Scientific Center of the Russian Academy of Sciences ; Almazov National Medical Research Center
Russian Federation

Cand. Sci. (Biol.), Head of the Laboratory of Genomics, Proteomics and Metabolomics at the University Research Institute of Biotechnology and Biomedicine, Senior Researcher at the Laboratory of Genetics at the Institute of Biology, Researcher of the Somnology Working Group at the Research Department for Arterial Hypertension

54 Odesskaya St., Tyumen, 625150

11 Pushkinskaya St., Petrozavodsk, 185910

2 Akkuratova St., Saint Petersburg, 197341



N. G. Zumbulidze
North-Western State Medical University named after I.I. Mechnikov
Russian Federation

Cand. Sci. (Med.), Associate Professor at the Academic Department of Ophthalmology 

41 Kirochnaya St., Saint Petersburg, 191015 



E. K. Zakharova
Yakutsk Republican Ophthalmological Hospital
Russian Federation

Cand. Sci. (Med.), Head of Ophthalmology Department 

15 Sverdlova St., Yakutsk, 677005 



References

1. Gubin D., Nelaeva A., Uzhakova A. et al. Disrupted circadian rhythms of body temperature, heart rate and fasting blood glucose in prediabetes and type 2 diabetes mellitus. Chronobiology Int 2017; 34(8):1136- 1148. https://doi.org/10.1080/07420528.2017.1347670

2. Gubin D., Weinert D. Temporal order deterioration and circadian disruption with age 1. Central and peripheral mechanisms. Advances in Gerontology 2015; 5:209-218.

3. Gubin D., Weinert D. Deterioration of temporal order and circadian disruption with age 2: Systemic mechanisms of aging-related circadian disruption and approaches to its correction. Advances in Gerontology 2016; 6:10-20.

4. Gubin D.G., Weinert D., Bolotnova T.V. Age-Dependent Changes of the Temporal Order – Causes and Treatment. Curr Aging Sci 2016; 9:14-25. https://doi.org/10.2174/1874609809666151130215824

5. Gubin D.G., Weinert D., Rybina S.V. et al. Activity, Sleep and Ambient Light Have a Different Impact on Circadian Blood Pressure, Heart Rate and Body Temperature Rhythms. Chronobiology Int 2017; 34(5):632- 649. https://doi.org/10.1080/07420528.2017.1288632

6. La Morgia C., Ross-Cisneros F.N., Sadun A.A., Carelli V. Retinal Ganglion Cells and Circadian Rhythms in Alzheimer’s Disease, Parkinson’s Disease, and Beyond. Frontiers in Neurology 2017; 8:162. https://doi.org/10.3389/fneur.2017.00162

7. Gibson E.M., Williams W.P., Kriegsfeld L.J. Aging in the circadian system: considerations for health, disease prevention and-longevity. Experimental Gerontology 2009; 44(1–2):51-56. https://doi.org/10.1016/j.exger.2008.05.007

8. Baranova N.A., Kuroedov A.V., Ovchinnikov Yu.V. New factors determining the variability of circadian rhythms of ophthalmotonus and perfusion pressure in patients with glaucoma. Ophthalmology 2016; 13(1):20-24. https://doi.org/10.18008/1816-5095-2016-1-20-24

9. Girardin J-L., Zizi F., Lazzaro D.R., Wolintz A.H. Circadian rhythm dysfunction in glaucoma: A hypothesis. Journal of Circadian Rhythms 2008; 6:1. https://doi.org/10.1186/17403391-6-1

10. Jean-Louis G., Zizi F., Lazzaro D.R., Wolintz A.H. Circadian rhythm dysfunction in glaucoma: A hypothesis. J Circadian Rhythms 2008; 6:1. https://doi.org/10.1186/1740-3391-6-1

11. Gubin D., Weinert D. Melatonin, circadian rhythms and glaucoma: Current perspective. Neural Regen Res 2022; 17:1759-1760. https://doi.org/10.4103/1673-5374.332149

12. Gubin D., Malishevskaya T., Weinert D., Zakharova E., Astakhov S., Cornelissen G. Circadian Disruption in Glaucoma: Causes, Consequences, and Countermeasures. Front Biosci 2024; 29(12):410. https://doi.org/10.31083/j.fbl2912410

13. Drouyer E., Dkhissi-Benyahya O., Chiquet C. et al. Glaucoma alters the circadian timing system. PLoS ONE 2008; 3(12):e3931. https://doi.org/10.1371/journal.pone.0003931

14. Liu J.H.; Kripke D.F.; Hoffman R.E.; Twa M.D. et al. Nocturnal elevation of intraocular pressure in young adults. Investig Ophthalmol Vis Sci 1998; 39:2707-2712.

15. Gracitelli C.P., Duque-Chica G.L., Roizenblatt M., Moura A.L. et al. Intrinsically photosensitive retinal ganglion cell activity is associated with decreased sleep quality in patients with glaucoma. Ophthalmology 2015; 122(6):1139-1148. https://doi.org/10.1016/j.ophtha.2015.02.030

16. Lax P., Ortuño-Lizarán I., Maneu V., Vidal-Sanz M. et al. Photosensitive Melanopsin-Containing Retinal Ganglion Cells in Health and Disease: Implications for Circadian Rhythms. Int J Mol Sci 2019; 20(13):3164. https://doi.org/10.3390/ijms20133164

17. Kripke D.F., Elliott J.A., Youngstedt S.D., Rex K.M. Circadian phase response curves to light in older and young women and men. Journal of Circadian Rhythms 2007; 5:4. https://doi.org/10.1186/1740-3391-5-4

18. Guido M.E. et al. Inner retinal circadian clocks and non-visual photoreceptors: Novel players in the circadian system. Progress in Neurobiology 2010; 92(4):484-504. https://doi.org/10.1016/j.pneurobio.2010.08.005

19. Ikegami K., Shigeyoshi Y., Masubuchi S. Circadian Regulation of IOP Rhythm by Dual Pathways of Glucocorticoids and the Sympathetic Nervous System. Invest Ophthalmol Vis Sci 2020; 61(3):26. https://doi.org/10.1167/iovs.61.3.26

20. Ikegami K. Circadian rhythm of intraocular pressure. J Physiol Sci 2024; 74(1):14. https://doi.org/10.1186/s12576-024-00905-8

21. Dekking H.M., Coster H.D. Dynamic tonometry. Ophthalmologica 1967; 154(1):59-74. https://doi.org/10.1159/000305149

22. Iliev M.E., Goldblum D., Katsoulis K., Amstutz C. et al. Comparison of rebound tonometry with Goldmannapplanation tonometry and correlation with central corneal thickness. Br J Ophthalmol 2006; 90(7):833-835. https://doi.org/10.1136/bjo.2005.089870

23. Greene M., Gilman B. Intraocular pressure measurement with instrumented contact lenses. Invest Ophthalmol Vis Sci 1974; 13:299-302.

24. Bhartiya S., Gangwani M., Kalra R.B., Aggarwal A. et al. 24-hour Intraocular pressure monitoring: the way ahead. Rom J Ophthalmol 2019; 63(4):315-320.

25. Todani A., Behlau I., Fava M.A. et al. Intraocular pressure measurement by radio wave telemetry. Invest Ophthalmol Vis Sci 2011; 52:9573-9580. https://doi.org/10.1167/iovs.11-7878

26. Tan S., Baig N., Hansapinyo L. et al. Comparison of selfmeasured diurnal intraocular pressure profiles using rebound tonometry between primary angle closure glaucoma and primary open angle glaucoma patients. PLOS ONE 2017; 12(3):e0173905. https://doi.org/10.1371/journal.pone.0173905

27. Fogagnolo P., Orzalesi N., Ferreras A., Rossetti L. The circadian curve of intraocular pressure: can we estimate its characteristics during office hours? Invest Ophthalmol Vis Sci 2009; 50(5):2209-2215. https://doi.org/10.1167/iovs.08-2889

28. Song Y.K., Lee C-K., Kim J. et al. Instability of 24-hour intraocular pressure fluctuation in healthy young subjects: a prospective, crosssectional study. BMC Ophthalmology 2014; 14:127. https://doi.org/10.1186/1471-2415-14-127

29. Malishevskaya T.N., Gubin D.G., Nemcova I.V., Vlasova A.S. et al. Analysis of the circadian rhythm of intraocular pressure in stable and progressive forms of primary open-angle glaucoma. Russian Ophthalmological Journal 2019; 12(4):35-42. https://doi.org/10.21516/2072-0076-2019-12-4-35-42

30. Gubin D.G., Malishevskaya T.N., Weinert D., Astakhov S.Yu. et al. Features of the circadian rhythm of intraocular pressure in stable and progressive primary open-angle glaucoma. Tyumenskii meditsinskii zhurnal 2018; 20(3):3-9.

31. Agnifili L., Mastropasqua R., Frezzotti P., Fasanella V. et al. Circadian intraocular pressure patterns in healthy subjects, primary open angle and normal tension glaucoma patients with a contact lens sensor. Acta Ophthalmol 2015; 93(1):e14-21. https://doi.org/10.1111/aos.12408

32. Mallick J., Devi L., Malik P.K., Mallick J. Update on Normal Tension Glaucoma. Journal of Ophthalmic & Vision Research 2016; 11(2):204- 208. https://doi.org/10.4103/2008-322X.183914

33. Van Eijgen J., Melgarejo J.D., Van Laeken J., Van der Pluijm C. et al. The Relevance of Arterial Blood Pressure in the Management of Glaucoma Progression: A Systematic Review. Am J Hypertens 2024; 37(3):179-198. https://doi.org/10.1093/ajh/hpad111

34. Kim K.E., Oh S., Baek S.U., Ahn S.J. et al. Ocular Perfusion Pressure and the Risk of Open-Angle Glaucoma: Systematic Review and Metaanalysis. Sci Rep 2020; 10(1):10056. https://doi.org/10.1038/s41598-020-66914-w

35. Fuchsjäger-Mayrl G., Wally B., Georgopoulos M., Rainer G. et al. Ocular blood flow and systemic blood pressure in patients with primary open-angle glaucoma and ocular hypertension. Invest Ophthalmol Vis Sci 2004; 45(3):834-839. https://doi.org/10.1167/iovs.03-0461)

36. Samsudin A., Isaacs N., Tai M.L., Ramli N. et al. Ocular perfusion pressure and ophthalmic artery flow in patients with normal tension glaucoma. BMC Ophthalmol 2016; 14(16):39. https://doi.org/10.1186/s12886-016-0215-3

37. Sung K.R., Lee S., Park S.B., Choi J. et al. Twenty-four hour ocular perfusion pressure fluctuation and risk of normal-tension glaucoma progression. Invest Ophthalmol Vis Sci 2009; 50(11):5266-5274. https://doi.org/10.1167/iovs.09-3716

38. Flammer J., Mozaffarieh M. What is the present pathogenetic concept of glaucomatous optic neuropathy? Surv Ophthalmol 2007; 52(2):162-173. https://doi.org/10.1016/j.survophthal.2007.08.012

39. Gubin D.G., Weinert D. Biorhythms and age. Uspekhi fiziologicheskikh nauk 1991; 1(22):77-96.

40. Gubin G.D., Gubin D.G., Kulikova S.V. Spectral structure of body temperature biorhythms in human ontogenesis. Uspekhi sovremennogo estestvoznaniya 2006; 12:48-51.

41. Ogren J.M. The inaccuracy of axillary temperatures measured with an electronic thermometer. Am J Dis Child 1990; 144(1):109-111. https://doi.org/10.1001/archpedi.1990.02150250121048

42. Monnard C.R., Fares E.J., Calonne J., Miles-Chan J.L. et al. Issues in Continuous 24-h Core Body Temperature Monitoring in Humans Using an Ingestible Capsule Telemetric Sensor. Front Endocrinol (Lausanne) 2017; 8:130. https://doi.org/10.3389/fendo.2017.00130

43. Ortiz-Tudela E., Martinez-Nicolas A., Compos M. et al. A new integrated variable based on thermometry,actimetry and body position (TAP) to evaluate circadian system status in humans. PLoS Comput Biol 2010; 11(6):10-15. https://doi.org/10.1371/journal.pcbi.1000996

44. Vlasova A.S., Petrov S.A., Malishevskaya T.N., Gubin D.G. et al. The connection of polymorphism and diurnal changes of the biological clock gene expression with the risk of progression of primary openangle glaucoma. Russian Ophthalmological Journal 2021; 14(4):38- 45. https://doi.org/10.21516/2072-0076-2021-14-4-38-45

45. Bonmati-Carrion M.A., Arguelles-Prieto R., Martinez-Madrid M.J. et al. Protecting the Melatonin Rhythm through Circadian Healthy Light Exposure. Int J Mol Sci 2014; 15(12):23448-23500. https://doi.org/10.3390/ijms151223448

46. Ciulla L., Moortthy M. et al. Circadian Rhythm and Glaucoma: What do We Know? J Glaucoma 2020; 29(2):127-132. https://doi.org/10.1097/IJG.0000000000001402

47. Gubin D.G. The variety of physiological effects of melatonin. Mezhdunarodnyi zhurnal prikladnykh i fundamental'nykh issledovanii 2016; 11(6):1048-1053.

48. Ma X-P., Shen M-Y., Shen G-L., Qi Q-R. et al. Melatonin concentrations in serum of primary glaucoma patients. International Journal of Ophthalmology 2018; 11(8):1337-1341. https://doi.org/10.18240/ijo.2018.08.14

49. Uz, Т. The regional and cellular expression profile of the melatonin receptor MT1 in the central dopaminergic system. Brain Res Mol Brain Res 2005; 136:45-53. https://doi.org/10.1016/j.molbrainres.2005.01.002

50. Wiechmann A.F., Summers J.A. Circadian rhythms in the eye: the physiological significance of melatonin receptors in ocular tissues. Prog Retin Eye Res 2008; 27(2):137-160. https://doi.org/10.1016/j.preteyeres.2007.10.001

51. Carracedo G. Carpen C., Concepción P., Díaz V. et al. Presence of melatonin in human tears. Journal of Optometry 2017; 10(1):3-4. https://doi.org/10.1016/j.optom.2016.03.002

52. Alkozi H.A., Navarro G., Aguinaga D., Reyes-Resin I. et al. Adrenomelatonin receptor complexes control ion homeostasis and intraocular pressure - their disruption contributes to hypertensive glaucoma. Br J Pharmacol 2020; 177(9):2090-2105. https://doi.org/10.1111/bph.14971

53. Dal Monte M. Cammalleri M., Amato R., Pezzino S. et al. A Topical Formulation of Melatoninergic Compounds Exerts Strong Hypotensive and Neuroprotective Effects in a Rat Model of Hypertensive Glaucoma. Int J Mol Sci 2020; 21(23):9267. https://doi.org/10.3390/ijms21239267

54. Martínez-Águila A., Fonseca B., M.J.Pérez de Lara, Pintor J. Effect of Melatonin and 5-Methoxycarbonylamino-N-Acetyltryptamine on the Intraocular Pressure of Normal and Glaucomatous Mice. J Pharmacol Exp Ther 2016; 357:293-299. https://doi.org/10.1124/jpet.115.231456

55. Pintor J., Martin L., Pelaez T. et al. Involvement of melatonin MT3 receptors in the regulation of intraocular pressure in rabbits. Eur J Pharmacol 2001; 416(3):251-254. https://doi.org/10.1016/s0014-2999(01)00864-0

56. Viggano S.R., Koskela T.K., Klee G.G. et al. The effect of melatonin on the aqueous humor flow in humans during the day. Ophthalmology 1994; 101(2):326–331. https://doi.org/10.1016/s0161-6420(94)31332-7

57. Skene D., Arendt J. Circadian rhythm sleep disorders in the blind and their treatment with melatonin. Sleep Med 2007; 8(6):651-655. https://doi.org/10.1016/j.sleep.2006.11.013

58. Hofman M.A., Swaab D.F. Living by the clock: the circadian pacemaker in older people. Ageing Res Rev 2006; 5(1):33-51. https://doi.org/10.1016/j.arr.2005.07.001

59. Kunieda T., Minamino T., Katsuno T. et al. Cellular senescence impairs circadianexpression of clock genes in vitro and in vivo. Circ Res 2006; 98(4):532-539. https://doi.org/10.1161/01.RES.0000204504.25798.a8

60. Lo M.T., Bardin C., Yang Y-W. et al. CLOCK 3111T/C genetic variant influences the daily rhythm of autonomic nervous function: relevance to body weight control. International Journal of Obesity 2018; 42(2):190-197. https://doi.org/10.1038/ijo.2017.168

61. Cox K., Takahashi J. Circadian clock genes and the transcriptional architecture of the clock mechanism. Journal of Molecular Endocrinology 2019; 63(4):93-102. https://doi.org/10.1530/JME-19-0153

62. Walker W.H., Walton J.C., Devries A.C., Nelson R.J. Circadian rhythm disruption and mental health. Transl Psychiatry 2020; 10(1):28. https://doi.org/10.1038/s41398-020-0694-0

63. Dalvin L.A., Fautsch M.P. Analysis of Circadian Rhythm Gene Expression With Reference to Diurnal Pattern of Intraocular Pressure in Mice. Invest Ophthalmol Vis Sci 2015; 56(4):2657-2663. https://doi.org/10.1167/iovs.15-16449

64. Wenzel R. Enhanced vasoconstriction to endothelin-1, angiotensin II and noradrenaline in carriers of the GNB3 825T allele in the skin microcirculation. Pharmacogenetics 2002; 12(6):489-495. https://doi.org/10.1097/00008571-200208000-00010

65. Sener A., Ozsavci D., Bingol-Ozakpinar O. Oxidized-LDL and Fe3+/ ascorbic acid-induced oxidative modifications and phosphatidylserine exposure in human platelets are reduced by melatonin. Folia biologica 2009; 55(2):45-52.

66. Ghosh P., Dey T., Majumder R., Datta M., Chattopadhyay A. et al. Insights into the antioxidative mechanisms of melatonin in ameliorating chromium-induced oxidative stress-mediated hepatic and renal tissue injuries in male Wistar rats. Food Chem Toxicol 2023; 173:113630. https://doi.org/10.1016/j.fct.2023.113630

67. Hussain S.A., Ismail S.H., Hussein K.I. Improvement of the hypolipidemic effect of lovastatin with melatonin. Iraqi Postgrad Med J 2004; 3:343-346.

68. Chen D., Zhang T., Lee T.H. Cellular Mechanisms of Melatonin: Insight from Neurodegenerative Diseases. Biomolecules 2020; 10(8):1158. https://doi.org/10.3390/biom10081158

69. Filippova Yu.E., Malishevskaya T.N., Kolomeichuk S.N., Gubin D.G., Vlasova A.S. The severity of endothelial dysfunction, oxidative stress, lipid metabolism disorders, decreased elastic properties and tone of peripheral vessels in patients with different POAG course variants, depending on the polymorphism of the genes of the biological clock. Russian Ophthalmological Journal 2022; 15(1):78-88. https://doi.org/10.21516/2072-0076-2022-15-1-78-88

70. Gubin D., Neroev V., Malishevskaya T., Kolomeichuk S. et al. Daytime Lipid Metabolism Modulated by CLOCK Gene Is Linked to Retinal Ganglion Cells Damage in Glaucoma. Applied Sciences 2022; 12(13):6374. https://doi.org/10.3390/app12136374

71. Neroev V., Malishevskaya T., Weinert D., Astakhov S. et al. Disruption of 24-Hour Rhythm in Intraocular Pressure Correlates with Retinal Ganglion Cell Loss in Glaucoma. Int J Mol Sci 2020; 22(1):359. https://doi.org/10.3390/ijms22010359

72. Gubin D.G., Malishevskaya Т.N., Astakhov Y.S., Astakhov S.Y. et al. Progressive retinal ganglion cell loss in primary open-angle glaucoma is associated with temperature circadian rhythm phase delay and compromised sleep. Chronobiol Int 2019; 36(4):564-577. https://doi.org/10.1080/07420528.2019.1566741

73. Gracitelli C.P.B., Duque-Chica G.L., Moura A.L. de A. et al. Relationship between Daytime Sleepiness and Intrinsically Photosensitive Retinal Ganglion Cells in Glaucomatous Disease. Journal of Ophthalmology 2016; 2016:5317371. https://doi.org/10.1155/2016/5317371

74. Boland M., Qiu M., Ramulu P. Association between sleep parameters and glaucoma in the United States population: National Health and Nutrition Examination Survey. Journal of Glaucoma 2019; 28(2):97- 104. https://doi.org/10.1097/IJG.0000000000001169

75. Gubin D., Neroev V., Malishevskaya T., Kolomeichuk S. et al. Depression scores are associated with retinal ganglion cells loss. J Affect Disord 2023; 333:290-296. https://doi.org/10.1016/j.jad.2023.04.039


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Malishevskaya T.N., Renziak E.V., Gubin D.G., Kolomeychuk S.N., Zumbulidze N.G., Zakharova E.K. Chronobiological approaches to studying the progression of primary open-angle glaucoma. National Journal glaucoma. 2025;24(3):52-64. (In Russ.) https://doi.org/10.53432/2078-4104-2025-24-3-52-64

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