NEUROPEPTIDES AS REGULATORS OF THE INTERACTION BETWEEN CELLULAR OSCILLATORS OF RHYTHMS

DOI: https://doi.org/10.29296/24999490-2019-01-02

M.P. Chernysheva, A.D. Nozdrachev St-Petersburg State University, Universitetskaya embankment., 7/9, St-Petersburg, 199034, Russian Federation E-mail: mp_chern@mail.ru

Peptidergic structures of the hypothalamus arrange a basis of its unique ability to regulate the organism's functions in time, adjusting metabolism, energy exchange and motor activity as sources of its own energy- to the dynamics of energy intake from external sources, primarily light. Axons of the retinohypothalamic tract create synapses on the peptidergic neurons of suprachiasmatic nuclei (SCN). For such function of SCN as a «master clock» of circadian rhythms, it is necessary to regulate both intracellular oscillators and the network structure of the nucleus. The review focuses on the analysis of the role of neuropeptides in regulating the activity and interaction of oscillators of the cell membrane, mitochondria, cytosol and nucleus in SCN neurons. There is discussed the possibility of the participation of neuropeptides in the implementation of other functions as the regulation of local circulation and metabolism in the SCN.
Keywords: 
suprachiasmatic nucleus, cellular oscillators, neuropeptides, glutamate, GABA

Список литературы: 
  1. Chernysheva M.P., Nozdrachev A.D. Gipotalamus kak gomeostat e`ndogennogo vremeni. Zhurn. e`vol. biohim. fiziol. im I.M. Sechenova. 2017; 53 (1): 3–16. [Chernysheva M. P., Nozdrachev A. D. Hypothalamus as a homeostat of endogenous time. J. Evol. Biochem Physiol. I.M. Sechenov. 2017; 53 (1): 3–16 (in Russian)]
  2. Edgar R., Green E., Zhao Y., van Ooijen G., Olmedo M., Qin X., Xu Y., Pan M., Valekunja U., Feeney K.A., Maywood E., Hastings M.H., Baliga N., Merrow M., Millar A., Johnson C.H., Kyriacou C., O’Neill J.S., Reddy A.B. Peroxiredoxins are conserved markers of circadian rhythms. Nature. 2012; 485 (7399): 459–64.
  3. Feliciano A., Vaz F., Torres V.M., Valentim-Coelho C., Silva R., Prosinecki V., Alexandre B.M., Carvalho A.S., Matthiesen R., Malhotra A., Pinto P., Bárbara C., Penque D. Evening and morning peroxiredoxin-2 redox/oligomeric state changes in obstructive sleep apnea red blood cells: Correlation with polysomnographic and metabolic parameters. Biochim. Biophys. Acta. 2017; 1863: 621–9.
  4. Hoyle N.P., O’Neill J.S. Oxidation-reduction cycles of peroxiredoxin proteins and nontranscriptional aspects of timekeeping. Biochemistry. 2015; 54: 184–93.
  5. Southey B.R., Eun L.J., Zamdborg L., Atkins N.Jr., Mitchell J.W., Li M., Gillette M.U., Kelleher N.L., Sweedler J.V. Comparing label-free quantitative peptidomics approaches to characterize diurnal variation of peptides in the rat suprachiasmatic nucleus. Anal Chem. 2014; 86: 443–52.
  6. Yoshikawa T., Inagaki N.F., Takagi S., Kuroda S., Yamasaki M., Watanabe M., Honma S., Honma K.I. Localization of photoperiod responsive circadian oscillators in the mouse suprachiasmatic nucleus. Sci Rep. 2017; 7: 8210.
  7. Morin L.P. Neuroanatomy of the extended circadian rhythm system. Exp Neurol. 2013; 243: 4–20.
  8. Takahashi J.S. Molecular architecture of the circadian clock in mammals. In: Time for metabolism and hormones. Eds Sassone-Corsi P., Christen Y. Heidelberg:Springer. 2016; 13–24.
  9. Golombek D.A., Bussi I.L., Agostino P.V. Minutes, days and years: molecular interactions among different scales of biological timing. Philos Trans R Soc Lond B Biol Sci. 2014; 369: 20120465.
  10. Enoki R., OdaY., Mieda M., Ono D., Honma S., Honma K.I. Synchronous circadian voltage rhythms with asynchronous calcium rhythms in the suprachiasmatic nucleus. Proc Natl Acad Sci USA. 2017; 114: 2476–85.
  11. Farajnia S., Meijer J.H., Michel St. Photoperiod modulates fast delayed rectifier potassium currents in the mammalian circadian clock. ASN Neuro. 2016; 8: 1759091416670778.
  12. Chernysheva M.P. Vremennaya struktura biosistem i biologicheskoe vremya. SPb.: Super, 2016; 213.
  13. [Chernysheva M.P. Temporal structure of a biosystem and biological time. SPb.: Super, 2016; 213 (in Russian)]
  14. Adelman J.P., Maylie J., Sah P. Small-conductance Ca2+-activated K+ channels: form and function. Annu Rev Physiol. 2012; 74: 245–69.
  15. Guarina L., Vandael D.H., Carabelli V., Carbone E. Low pH boosts burst firing and catecholamine release by blocking TASK-1 and BK channels while preserving Cav1 channels in mouse chromaffin cells. J. Physiol. 2017; 595: 2587–609.
  16. O’Neill J.S., Reddy A.B. The essential role of cAMP/Ca2+ signalling in mammalian circadian timekeeping. Biochem Soc Trans. 2012; 40: 44–50.
  17. Noguchi T., Leise T.L., Kingsbury N.J., Diemer T., Wang L.L., Henson M.A., Welsh D.K. Calcium circadian rhythmicity in the suprachiasmatic nucleus: cell autonomy and network modulation. eNeuro. 2017; 4: ENEURO.0160-17.2017.
  18. Sassone-Corsi P. The epigenetic and metabolic language of the circadian clock. In: Time for metabolism and hormones. Eds. Sassone- Corsi P., Christen Y. Heidelberg :Springer. 2016; 1–20.
  19. Dokudovskaya S., Rout M.P. SEA you later alli-GATOR – a dynamic regulator of the TORC1 stress response pathway. J. Cell. Sci. 2015; 128: 2219–28.
  20. Gau D., Lemberger T., von Gall C., Kretz O., Le Minh N., Gass P., Schmid W., Schibler U., Korf H. W., Schütz G. Phosphorylation of CREB Ser142 regulates light-induced phase shifts of the circadian clock. PloSOne. 2012; 7: e45130.
  21. Sharapov M.G., Ravin V.K., Novoselov V.I. Peroksiredoksiny kak mul`tifunkcional`nye e`nzimy. Mol. Biol. (Moskva). 2014; 48: 600–28.
  22. [Sharapov M.G., Ravin V.K., and Novoselov V.I. Peroxiredoxins as multifunctional enzymes. Mol. biol. (Moscow). 2014; 48: 600–28 (in Russian)]
  23. de Keizer P.L., Burgering B.M., Dansen T.B. Forkhead box O as a sensor, mediator, and regulator of redox signaling. Antioxid Redox Signal. 2011; 14: 1093–106.
  24. Putker M., O’Neill J.S. Reciprocal control of the circadian clock and cellular redox state – a critical appraisal. Mol Cell. 2016; 39: 6–9.
  25. Reddy A.B. Redox and metabolic oscillation in the clockwork. In: Time for metabolism and hormones. Eds Sassone-Corsi P., Christen Y. Heidelberg: Springer. 2016; 51–62.
  26. McIntosh B.E., Hogenesch J.B., Bradfield C.A. Mammalian Per-Arnt-Sim proteins in environmental adaptation. Physiol. Rev. 2010; 72: 625–45.
  27. Chi-Castañeda D., Ortega A. Clock genes in glia cells. A rhythmic history. ASN Neuro. 2016; 8: 1759091416670766.
  28. Chernysheva M.P., Nozdrachev A.D. Gormonal`nyy faktor prostranstva i vremeni vnutrenney sredy organizma. SPb.: Nauka, 2006; 248.
  29. [Chernysheva M.P., Nozdrachev A.D. Hormonal factor of space and time of organism’s internal environment. SPb.: Nauka, 2006; 248 (in Russian)]
  30. Vaudry D., Falluel-Morel A., Bourgault S., Basille M., Burel D., Wurtz O., Fournier A., Chow B.K.C., Hashimoto H., Galas L., Vaudry H. Pituitary adenylate cyclase-activating polypeptide and its receptors: 20 years after the discovery. Pharm. Rev. 2009; 61: 283–357.
  31. Loh D.H., Dragich J.M., Kudo T., Schroeder A.M., Nakamura T.J., Waschek J.A., Block G.D., Colwell C.S. Effects of vasoactive intestinal peptide genotype on circadian gene expression in the SCN and peripheral organs. J. Biol. Rhythms. 2011; 26: 200–9.
  32. Tsuji T., Allchorne A.J., Zhang M., Tsuji C., Tobin V.A., Pineda R., Raftogianni A., Stern J.E., Grinevich V., Leng G., Ludwig M. Vasopressin casts light on the suprachiasmatic nucleus. J. Physiol. 2017; 595: 3497–514.
  33. Subhedar N.K., Nakhate K.T., .Upadhya M.A., Kokare D.M. CART in the brain of vertebrates: Circuits, functions and evolution. Peptides. 2014; 54: 108–30.
  34. Lee J.E., Zamdborg L., Southey B.R., Atkins N., Mitchel J.W., Lee M.X, Gillette M.U., Kelleher N.L., Sweedler J.V. Quantitative peptidomics for discovery of circadian-related peptides from the rat suprachiasmatic nucleus. J. Proteome Res. 2013; 12: 585–93.
  35. Fahrenkrug J., Georg B., Hannibal J., Jørgensen H.L. Altered rhythm of adrenal clock genes, StAR and serum corticosterone in VIP receptor 2-deficient mice. J. Mol. Neurosci. 2012; 48: 584–96.
  36. Evans J.A. Collective timekeeping among cells of the master circadian clock. J. Endocrinol. 2016; 230: 27–49.
  37. Butcher G.Q., Lee B., Cheng H.Y.M., Obrietan K. Light stimulates MSK1 activation in the suprachiasmatic nucleus via a PACAP-ERK/MAPkinase-dependent mechanism. J. Neurosci. 2005; 25: 5305–13.
  38. Gamble K.L., Kudo T., Colwell C.S., McMahon D.G. Gastrin-releasing peptide modulates fast delayed rectifier potassium current in Per1-expressing SCN neurons. J. Biol. Rhythms. 2011; 26: 99–106.
  39. Hablitz L.M., Molzof H.E., Abrahamsson K.E., Cooper J.M., Prosser R.A., Gamble K.L. GIRK Channels Mediate the Nonphotic Effects of Exogenous Melatonin. J. Neurosci. 2015; 35: 14957–65.
  40. Maywood E.S., Chesham J.E., O’Brien J.A., Hastings M.H. A diversity of paracrine signals sustains molecular circadian cycling in suprachiasmatic nucleus circuits. Proc Natl Acad Sci USA. 2011; 108: 14306–11.
  41. Ukena K., Osugi T., Leprince J., Vaudry H., Tsutsui K. Molecular evolution of GPCRs: 26Rfa/GPR103. J. Mol. Endocrinol. 2014; 52: 119–31.
  42. Vu J.P., Goyal D., Luong L., Oh S., Sandhu R., Norris J., Parsons W., Pisegna J.R., Germano P.M. PACAP intraperitoneal treatment suppresses appetite and food intake via PAC1 receptor in mice by inhibiting ghrelin and increasing GLP-1 and leptin. Am J Physiol Gastrointest Liver Physiol. 2015; 309: 816–25.
  43. Fukuhara C., Brewer J.M., Dirden J.C., Bittman E.L., Tosini G., Harrington M. E. Neuropeptide Y rapidly reduces Period 1 and Period 2 mRNA levels in the hamster suprachiasmatic nucleus. Neurosci Lett. 2001; 314: 119–22.
  44. Neitz A., Mergia E., Imbrosci B., Petrasch-Parwez E., Eysel U.T., Koesling D., Mittmann T. Postsynaptic NO/cGMP increases NMDA receptor currents via hyperpolarization-activated cyclic nucleotide-gated channels in the hippocampus. Cereb Cortex. 2014; 24: 1923–36.
  45. Hummer D.L., Ehlen J.C., Larkin T.E., McNeill J.K., Pamplin J.R., Walker C. A., Walker P.V., Dhanraj D.R., Albers H.E. Sustained activation of GABAA receptors in the suprachiasmatic nucleus mediates light-induced phase delays of the circadian clock: a novel function of ionotropic receptors. Eur. J. Neurosci. 2015; 42: 1830–8.
  46. Sumova A., Bendova Z., Sladek M., El-Hennamy R., Laurinova K., Jindrakova Z., Illnerova H. Setting the biological time in central and peripheral clocks during ontogenesis. The FEBS letters, 2006; 580: 2836–42.
  47. Burton K.J., Li X., Li B., Cheng M.Y., Urbanski H.F., Zhou Q.Y. Expression of prokineticin 2 and its receptor in the macaque monkey brain. Chronobiol Int. 2016; 33: 191–9.
  48. Li J.D., Burton K.J., Zhang C., Hu S.B., Zhou Q.Y. Vasopressin receptor V1a regulates circadian rhythms of locomotor activity and expression of clock-controlled genes in the suprachiasmatic nuclei. Am. J. Physiol. Regul. Integr omp. Physiol. 2009; 296: 824–30.
  49. Mieda M., Ono D., Hasegawa E., Okamoto H., Honma K., Honma S., Sakurai T. Cellular clocks in AVP neurons of the SCN are critical for interneuronal coupling regulating circadian behavior rhythm. Neuron. 2015; 85: 1103–16.
  50. Vida B., Hrabovszky E., Kalamatianos T., Coen C.W., Liposits Z., Kalló I. Oestrogen receptor α and β immunoreactive cells in the SCN of mice: distribution, sex differences and regulation by gonadal hormones. J. Neuroendocrinol. 2008; 20: 1270–6.
  51. Van der Zee E.A, Roman V., Ten Brinke O., Meerlo P. TGF alfa and AVP in the mouse SCN anatomical relationship and daily profiles. Brain Res. 2005; 1054: 159–66.
  52. Ikegami K., Yoshimura N. Molecular mechanism regulating seasonality. In: Biological timekeeping: clocks, rhythms and behavior. Ed. Kumar V., Springer (India). 2017; 589–606.
  53. Kalsbeek A., van der Spek R., Lei J., Endert E., Buijs R.M., Fliers E. Circadian rhythms in the hypothalamo–pituitary–adrenal (HPA) axis. Mol Cell Endocrinol. 2012; 349: 20–9.