Genetic mechanisms of the influence of light and phototransduction on Drosophila melanogaster lifespan

The light of the visible spectrum (with wavelengths of 380-780 nm) is one of the fundamental abiotic factors to which organisms have been adapting since the start of biological evolution on the Earth. Numerous literature sources establish a connection between the duration of exposure to daylight, carcinogenesis and longevity, convincingly showing a significant reduction in the incidence of cancer in blind people, as well as in animal models. On the other hand, the stimulating nature of the effect of continuous illumination on reproductive function was noted, in particular, the effects of increasing the fecundity of females of various species are known. Increase in motor activity and, as a result, in metabolic rate and thermogenesis during permanent exposure to light also reduces the body's energy reserves and lifespan. In principle, in the context of aging, not only the exposure time, but also the age at the onset of exposure to constant illumination matter, the reverse effects are valid for the maintenance of experimental animals in the constant darkness. Over the long period of the evolution of light signal transduction systems, many mechanisms have emerged that allow to form an adequate response of the organism to illumination, modulating the highly conservative signaling cascades, including those associated with aging and lifespan (FOXO, SIRT1, NF-kB, mTOR/S6k, PPARa, etc). In this review, we consider the relationship between lifespan, photoregimens, and also the expression of the genes encoding the phototransduction cascade and the circadian oscillator elements of animal cells. In the present paper, basic transducers of light and other signals, such as the family of TRP receptors, G proteins, phospholipase C, and others, are considered in the context of aging and longevity. A relationship between the mechanisms of thermoreception, the temperature synchronization of the circadian oscillator and the life span is established in the review. Analysis of experimental data obtained from the Drosophila melano-gaster model allowed us to formulate the hypothesis of age-dependent photoresistance - a gradual decrease in the expression of genes associated with phototransduction and circadian oscillators, leading to deterioration in the ability to adapt to the photoregimen and to the increase in the rate of aging.

1. Anisimov VN. Pineal gland, biorhythms, and ageing. Uspehi Fiziologicheskih Nauk = Advances in Physiological Sciences. 2008;39(4):40-65. (in Russian)

2. Anisimov V.N., Vinogradova I.A., Borisenkov M.F., Bukalev A.V., Zabezhinsky M.A., Panchenko A.V., Popovich I.G., Semenchen-ko A.V., Tyndyk M.L. Light regimen, aging, and cancer. Vestnik Rossiyskogo Universiteta Druzhby Narodov. Seriya Meditsina = Bulletin of People’s Friendship University of Russia. Medical Series. 2012;7:29-30. (in Russian)

3. Anisimov V.N., Vinogradova I.A., Bukalev A.V., Borisenkov M.F., Popovich I.G., Zabezhinsky M.A., Panchenko A.V., Tyndyk M.L., Yurova M.N. Light-induced desynchronosis and risk of malignant tumors in laboratory animals: state of the problem. Voprosy Onkologii = Problems in Oncology. 2013;59(3):302-313. (in Russian)

4. inogradova I.A., Anisimov VN. Light Regime in the North and Age-Related Pathology. Petrozavodsk, 2012. (in Russian)

5. Dobrovol’skaya E.V., Solovyov I.A., Proshkina E.N., Moskalev A.A. Effects of circadian rhythm gene overactivation in different tissues on stress resistance and longevity in Drosophila melanogaster. Teoreticheskaya i Prikladnaya Eko-logiya = Theoretical and Applied Ecology. 2016;3:32-40. (in Russian)

6. Lotosh Т.А., Vinogradova I.A., Bukalev A.V., Anisimov V.N. Modifying influence of constant insolation on the rat body depending on the timing of the impact. Fundamentalnye Issledovaniya = Fundamental Research. 2013;5(2):308-313. (in Russian)

7. Москалев А.А., Малышева О.А. Роль светового режима в регуляции продолжительности жизни Drosophila melanogaster. Экология. 2009;40(3):221-226. [Moskalev A.A., Malysheva O.A. Effect of illumination regime on life span in Drosophila melanogaster. Russian Journal of Ecology. 2009;40(3):206-212.]

8. Moskalev A.A., Malysheva O.A. The role of genes for transcription factors dFOXO, dSIR2, and HSP70 in lifespan alteration of Drosophila melanogaster under various light conditions. Ekologicheskaya Genetika = Ecological Genetics. 2010;8(3):67-80. (in Russian)

9. Moskalev A.A., Shostal’ O.A., Zainullin V.G. Genetics aspects of the influence of different light regimes on Drosophila life span. Us-pekhi Gerontologii = Advances in Gerontology. 2006;18:55-58. (in Russian)

10. Solovyov I.A., Dobrovol’skaya E.V., Moskalev A.A. Genetic control of circadian rhythms and aging. Russian Journal of Genetics. 2016;52(4):343-361.

11. Anisimov V.N., Vinogradova I.A., Panchenko A.V., Popovich I.G., Za-bezhinski M.A. Light-at-night-induced circadian disruption, cancer and aging. Curr. Aging Sci. 2012;5(3):170-177.

12. Bee L., Marini S., Pontarin G., Ferraro P., Costa R., Albrecht U., Ce-lotti L. Nucleotide excision repair efficiency in quiescent human fibroblasts is modulated by circadian clock. Nucleic Acids Res. 2015; 43(4):2126-2137. DOI 10.1093/nar/gkv081.

13. Biello S., Bonsall R., Atkinson D., Molyneux L., Harrington P.E., Lall G.M. Alterations in glutamatergic signaling contribute to the decline of circadian photoentrainment in aged mice. Neurobiol. Aging. 2018;66:75-84. DOI 10.1016/j.neurobiolaging.2018.02.013.

14. Bjorn L.O. Photobiology: the Science of Light and Life. New York, 2015.

15. Chang J.S., Noh D.Y., Park I.A., Kim M.J., Song H., Ryu S.H., Suh P.G. Overexpression of phospholipase C-y1 in rat 3Y1 fibroblast cells leads to malignant transformation. Cancer Res. 1997;57(24):5465-5468.

16. Chaudhari A., Gupta R., Makwana K., Kondratov R. Circadian clocks, diets and aging. Nutr. Healthy Aging. 2017;4(2):101-112. DOI 10.3233/NHA-160006.

17. Daneault V., Hebert M., Albouy G., Doyon J., Dumont M., Carrier J., Vandewalle G. Aging reduces the stimulating effect of blue light on cognitive brain functions. Sleep. 2014;37(1):85-96. DOI 10.5665/sleep.3314.

18. Dibner C., Schibler U. Circadian timing of metabolism in animal models and humans. J. Intern. Med. 2015;277(5):513-527. DOI 10.1111/joim.12347.

19. Feillet C., van der Horst G.T., Levi F., Rand D.A., Delaunay F. Coupling between the circadian clock and cell cycle oscillators: implication for healthy cells and malignant growth. Front. Neurol. 2015;6:96. DOI 10.3389/fneur.2015.00096.

20. Fogle K.J., Baik L.S., Houl J.H., Tran T.T., Roberts L., Dahm N.A., Cao Y., Zhou M., Holmes T.C. CRYPTOCHROME-mediated phototransduction by modulation of the potassium ion channel P-subunit redox sensor. Proc. Natl. Acad. Sci. USA. 2015;112(7):2245-2250. DOI 10.1073/pnas.1416586112.

21. Fortini M.E., Bonini N.M. Modeling human neurodegenerative diseases in Drosophila: on a wing and a prayer. Trends Genet. 2000; 16(4):161-167. DOI 10.1016/S0168-9525(99)01939-3.

22. Fuhr L., Abreu M., Pett P., Relogio A. Circadian systems biology: when time matters. Comput. Struct. Biotechnol. J. 2015;13:417-426. DOI 10.1016/j.csbj.2015.07.001.

23. Giebultowicz J.M. The circadian system and aging of Drosophila. Circadian Rhythms and Their Impact on Aging. Cham, Switzerland. 2017;129-145. DOI 10.1007/978-3-319-64543-8_6.

24. Hall H., Medina P., Cooper D.A., Escobedo S.E., Rounds J., Brennan K.J., Vincent C., Miura P., Doerge R., Weake V.M. Transcrip-tome profiling of aging Drosophila photoreceptors reveals gene expression trends that correlate with visual senescence. BMC Genomics. 2017;18(1):894. DOI 10.1186/s12864-017-4304-3.

25. Hardeland R. Melatonin as a geroprotector: healthy aging vs. extension of lifespan. Ed. A.M. Vaiserman. Anti-aging Drugs: From Basic Research to Clinical Practice. Cambridge: Royal Society of Chemistry. UK, 2017;474-495. DOI 10.1039/9781782626602-00474.

26. Hardie R.C., Juusola M. Phototransduction in Drosophila. Curr. Opin. Neurobiol. 2015;34:37-45. DOI 10.1016/j.conb.2015.01.008.

27. Hendricks J.C., Lu S., Kume K., Yin J.C., Yang Z., Sehgal A. Gender dimorphism in the role of cycle (BMAL1) in rest, rest regulation, and longevity in Drosophila melanogaster. J. Biol. Rhythms. 2003; 18(1):12-25. DOI 10.1177/0748730402239673.

28. Hori M., Shibuya K., Sato M., Saito Y. Lethal effects of short-wavelength visible light on insects. Sci. Rep. 2014;4:7383. DOI 10.1038/srep07383.

29. Ito C., Tomioka K. Heterogeneity of the peripheral circadian systems in Drosophila melanogaster: a review. Front. Physiol. 2016;7:8. DOI 10.3389/fphys.2016.00008.

30. Kamdar B.B., Tergas A.I., Mateen F.J., Bhayani N.H., Oh J. Night-shift work and risk of breast cancer: a systematic review and meta-analysis. Breast Cancer Res. Treat. 2013;138(1):291-301. DOI 10.1007/s10549-013-2433-1.

31. Katewa S.D., Akagi K., Bose N., Rakshit K., Camarella T., Zheng X., Hall D., Davis S., Nelson C.S., Brem R.B., Ramanathan A., Sehgal A., Giebultowicz J.M., Kapahi P. Peripheral circadian clocks mediate dietary restriction-dependent changes in lifespan and fat metabolism in Drosophila. Cell Metab. 2016;23(1):143-154. DOI 10.1016/j.cmet.2015.10.014.

32. Kim M., Subramanian M., Cho Y.H., Kim G.H., Lee E., Park J.J. Shortterm exposure to dim light at night disrupts rhythmic behaviors and causes neurodegeneration in fly models of tauopathy and Alzheimer’s disease. Biochem. Biophys. Res. Commun. 2018;495(2):1722-1729. DOI 10.1016/j.bbrc.2017.12.021.

33. Kirkwood T.B. Evolution of ageing. Nature. 1977;270(5635):301-304. DOI 10.1038/270301a0.

34. Klarsfeld A., Rouyer F. Effects of circadian mutations and LD periodicity on the life span of Drosophila melanogaster. J. Biol. Rhythms. 1998;13(6):471-478. DOI 10.1177/074873098129000309.

35. Kloog I., Haim A., Portnov B.A. Using kernel density function as an urban analysis tool: Investigating the association between nightlight exposure and the incidence of breast cancer in Haifa, Israel. Com-put. Environ. Urban Syst. 2009;33(1):55-63. DOI 10.1016/j.com-penvurbsys.2008.09.006.

36. Kloog I., Haim A., Stevens R.G., Barchana M., Portnov B.A. Light at night co-distributes with incident breast but not lung cancer in the female population of Israel. Chronobiol. Int. 2008;25(1):65-81. DOI 10.1080/07420520801921572.

37. Kloog I., Stevens R.G., Haim A., Portnov B.A. Nighttime light level codistributes with breast cancer incidence worldwide. Cancer Causes Control. 2010;21(12):2059-2068. DOI 10.1007/s10552-010-9624-4.

38. Krishnan N., Kretzschmar D., Rakshit K., Chow E., Giebultowicz J.M. The circadian clock gene period extends health span in aging Drosophila melanogaster. Aging (Albany N.Y.). 2009;1(11):937-948. DOI 10.18632/aging.100103.

39. Lans H., Jansen G. Multiple sensory G proteins in the olfactory, gustatory and nociceptive neurons modulate longevity in Caenorhabdi-tis elegans. Dev. Biol. 2007;303(2):474-482. DOI 10.1016/j.ydbio.2006.11.028.

40. Lehrer S. Blindness increases life span of male rats: pineal effect on longevity. J. Chronic. Dis. 1981;34(8):427-429. DOI 10.1016/0021-9681(81)90041-2.

41. McLay L.K., Green M.P., Jones T.M. Chronic exposure to dim artificial light at night decreases fecundity and adult survival in Drosophila melanogaster. J. Insect Physiol. 2017;100:15-20. DOI 10.1016/j.jinsphys.2017.04.009.

42. Moskalev A.A., Proshkina E.N., Belyi A.A., Solovyev I.A. Genetics of aging and longevity. Russian Journal of Genetics: Applied Research. 2017;7(4):369-384. DOI 10.1134/s2079059717040074.

43. Ostrovsky M.A. Rhodopsin: Evolution and comparative physiology. Pa-leontol. J. 2017;51(5):562-572. DOI 10.1134/s0031030117050069.

44. Papp S.J., Huber A.L., Jordan S.D., Kriebs A., Nguyen M., Mores-co J.J., Yates J.R., Lamia K.A. DNA damage shifts circadian clock time via Hausp-dependent Cry1 stabilization. Elife. 2015;4. DOI 10.7554/eLife.04883.

45. Patel S.A., Chaudhari A., Gupta R., Velingkaar N., Kondratov R.V. Circadian clocks govern calorie restriction-mediated life span extension through BMAL1- and IGF-1-dependent mechanisms. FASEB J. 2016;30(4):1634-1642. DOI 10.1096/fj.15-282475.

46. Plachetzki D.C., Fong C.R., Oakley T.H. The evolution of phototransduction from an ancestral cyclic nucleotide gated pathway. Proc. Biol. Sci. 2010;277(1690):1963-1969. DOI 10.1098/rspb.2009.1797.

47. Poletini M.O., Moraes M.N., Ramos B.C., Jeronimo R., Castrucci A.M. TRP channels: a missing bond in the entrainment mechanism of peripheral clocks throughout evolution. Temperature (Austin). 2015; 2(4):522-534. DOI 10.1080/23328940.2015.1115803.

48. Randall A.S., Liu C.H., Chu B., Zhang Q., Dongre S.A., Juusola M., Franze K., Wakelam M.J., Hardie R.C. Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids. J. Neurosci. 2015;35(6):2731-2746. DOI 10.1523/JNEUROSCI.1150-14.2015.

49. Riera C.E., Huising M.O., Follett P., Leblanc M., Halloran J., Van An-del R., de Magalhaes Filho C.D., Merkwirth C., Dillin A. TRPV1 pain receptors regulate longevity and metabolism by neuropeptide signaling. Cell. 2014;157(5):1023-1036. DOI 10.1016/j.cell.2014.03.051.

50. Shen J., Zhu X., Gu Y., Zhang C., Huang J., Xiao Q. Toxic effect of visible light on Drosophila life span depending on diet protein content. J. Gerontol. Ser. A. 2018. DOI 10.1093/gerona/gly042.

51. Sheng Y., Tang L., Kang L., Xiao R. Membrane ion channels and receptors in animal lifespan modulation. J. Cell. Physiol. 2017;232(11): 2946-2956. DOI 10.1002/jcp.25824.

52. Shostal O.A., Moskalev A.A. The genetic mechanisms of the influence of the light regime on the lifespan of Drosophila melanogaster. Front. Genet. 2012;3:325. DOI 10.3389/fgene.2012.00325.

53. Solovev I., Shaposhnikov M., Kudryavtseva A., Moskalev A. Drosophila melanogaster as a model for studying the epigenetic basis of aging. Epigenetics of Aging and Longevity. Elsevier: Academic Press, 2018; 293-307. DOI 10.1016/B978-0-12-811060-7.00014-0.

54. Song B.M., Lee C.H. Toward a mechanistic understanding of color vision in insects. Front. Neural Circuits. 2018;12(16). DOI 10.3389/fncir.2018.00016.

55. Szklarczyk D., Morris J.H., Cook H., Kuhn M., Wyder S., Simo-novic M., Santos A., Doncheva N.T., Roth A., Bork P., Jensen L.J., von Mering C. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45(D1):D362-D368. DOI 10.1093/nar/gkw937.

56. Wolff T., Ready D.F. Pattern formation in the Drosophila retina. The Development of Drosophila melanogaster. N.Y. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. 1993;2:1277-1325.

57. Xiao R., Liu J., Xu X.Z. Thermosensation and longevity. J. Comp. Physiol. A-Neuroethol. Sens. Neural. Behav. Physiol. 2015;201(9):857-867. DOI 10.1007/s00359-015-1021-8.

58. Zou S., Meadows S., Sharp L., Jan L.Y., Jan Y.N. Genome-wide study of aging and oxidative stress response in Drosophila melanogas-ter. Proc. Natl. Acad. Sci. USA. 2000;97(25):13726-13731. DOI 10.1073/pnas.260496697.