Nesfatin-1'in anoreksijenik fonksiyonunun gün içinde değişimi sirkadiyen ritimle ilişkili olabilir mi?

Abstract

Beslenme, organizmanın metabolik ihtiyaçlarını karşılamak için sergilenen bir vücut fonksiyonudur. Beslenme davranışının regülasyonu homeostatik mekanizmalar tarafından sağlanmaktadır. Bireylerin gıda tüketimi, yaklaşık 24 saatlik sirkadiyen döngü boyunca beyin tarafından zamana bağlı olarak koordine edilir. Vücuttaki biyolojik saatler gıda tüketiminin sirkadiyen ritimde meydana gelebileceği günlük aralıkları ayarlamaktadır. Bu zaman dilimleri genellikle aktif periyot evresinde yer almaktadır. Besin alımının sirkadiyen kontrolünü sağlayan biyolojik saatler, hipotalamusun suprakiazmatik nükleusunda ışıkla sürüklenen (entrain) bir ana saat ile beyinde ve vücudun diğer dokularında yer alan çok sayıdaki sekonder osilatörlerdir. Nesfatin-1, nükleobindin 2 öncü proteininden türetilen ve iştah üzerinde güçlü etkiler gösteren bir hormondur. Nesfatin-1’in anoreksijenik etkisi özellikle günün karanlık periyodunda daha belirgindir. Bu durum söz konusu hormonun sirkadiyen ritme sahip olup olmadığı sorusunu akıllara getirmektedir. Derlememizde konuyla ilgili çalışmalardan elde edilen bulgular kesitsel olarak ele alınarak, nesfatin-1’in beslenme davranışının regülasyonu ile etkilerinin sirkadiyen ritimle muhtemel ilişkisi değerlendirilmektedir.

Keywords

• nesfatin-1
• sirkadiyen ritim
• diürnal ritim
• beslenme
• anoreksijenik

Could the change of anorexigenic function of nesfatin-1 during the day be associated with circadian rhythm?

Abstract

Nutrition is a body function exhibited to provide the metabolic needs of the organism. The regulation of feeding behavior is provided by homeostatic mechanisms. Food consumption of individuals is time-dependently coordinated by the brain throughout the approximately 24-hour circadian cycle. The biological clocks in the body set the daily intervals in which food consumption can occur in the circadian rhythm. These time zones are usually in the active period phase. The biological clocks that provide circadian control of food intake are a light-entrained master clock in the suprachiasmatic nucleus of the hypothalamus and numerous secondary oscillators in the brain and other tissues of the body. Nesfatin-1 is a hormone derived from the precursor protein of nucleobindin 2 and has strong effects on appetite. The anorexigenic effect of Nesfatin-1 is more pronounced, especially in the dark period of the day. This raises the question of whether the hormone in question has a circadian rhythm. In our review, the findings obtained from the studies on the subject are discussed cross-sectionally, and the possible relationship between the regulation of feeding behavior and the effects of nesfatin-1 with the circadian rhythm is evaluated.

Keywords

• nesfatin-1
• circadian rhythm
• diurnal rhythm
• nutrition
• anorexigenic

References

1. 1. Gamble KL, Berry R, Frank SJ, Young ME. Circadian clock control of endocrine factors. Nat Rev Endocrinol 2014;10:466-75. DOI: 10.1038/nrendo.2014.78.
2. 2. Armstrong S. A chronometric approach to the study of feeding behavior. Neurosci Biobehav Rev 1980;4:27-53. DOI: 10.1016/0149-7634(80)90024-X.
3. 3. Oh-I S, Shimizu H, Satoh T, et al. Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 2006;443:709-12. DOI: 10.1038/nature05162.
4. 4 .Stengel A, Goebel M, Taché Y. Nesfatin-1: a novel inhibitory regulator of food intake and body weight. Obes Rev 2011;12:261-71. DOI: 10.1111/j.1467-789X.2010.00770.x.
5. 5. Challet E. The circadian regulation of food intake. Nat Rev Endocrinol 2019;15:393-405. DOI: 10.1038/s41574-019-0210-x.
6. 6. Kraly FS, Cushin BJ, Smith GP. Nocturnal hyperphagia in the rat is characterized by decreased postprandial satiety. J Comp Physiol Psychol 1980;94:375-87. DOI: 10.1037/ h0077663.
7. 7. Strubbe JH, van Dijk G. The temporal organization of ingestive behaviour and its interaction with regulation of energy balance. Neurosci Biobehav Rev 2002;26:485-98. DOI: 10.1016/S0149-7634(02)00016-7.
8. 8. Scheer FAJL, Morris CJ, Shea SA. The internal circadian clock increases hunger and appetite in the evening independent of food intake and other behaviors. Obesity 2013;21:421-3. DOI: 10.1002/oby.20351.

9. 9. Sargent C, Zhou X, Matthews R, Darwent D, Roach G. Daily rhythms of hunger and satiety in healthy men during one week of sleep restriction and circadian misalignment. Int J Environ Res Public Health 2016;13:170. DOI: 10.3390/ ijerph13020170.
10. 10. Yang S, Liu A, Weidenhammer A, et al. The role of mPer2 clock gene in glucocorticoid and feeding rhythms. Endocrinology 2009;150:2153-60. DOI: 10.1210/en.2008-0705.
11. 11. Adamovich Y, Rousso-Noori L, Zwighaft Z, et al. Circadian clocks and feeding time regulate the oscillations and levels of hepatic triglycerides. Cell Metab 2014;19:319-30. DOI: 10.1016/j.cmet.2013.12.016.
12. 12. Kettner NM, Mayo SA, Hua J, Lee C, Moore DD, Fu L. Circadian dysfunction induces leptin resistance in mice. Cell Metab 2015;22:448-59. DOI: 10.1016/j.cmet.2015.06.005.
13. 13. Sen S, Dumont S, Sage-Ciocca D, et al. Expression of the clock gene Rev-erbα in the brain controls the circadian organisation of food intake and locomotor activity, but not daily variations of energy metabolism. J Neuroendocrinol 2018;30:e12557. DOI: 10.1111/jne.12557.
14. 14. Nagai K, Nishio T, Nakagawa H, Nakamura S, Fukuda Y. Effect of bilateral lesions of the suprachiasmatic nuclei on the circadian rhythm of food-intake. Brain Res 1978;142:384-9. DOI: 10.1016/0006-8993(78)90648-0.
15. 15. Stoynev A, Ikonpmov O, Usunoff K. Feeding pattern and light-dark variations in water intake and renal excretion after suprachiasmatic nuclei lesions in rats. Physiol Behav 1982;29:35-40. DOI: 10.1016/0031-9384(82)90362-6.
16. 16. Jaeger C, Sandu C, Malan A, Mellac K, Hicks D, Felder‐Schmittbuhl M. Circadian organization of the rodent retina involves strongly coupled, layer‐specific oscillators. FASEB J 2015;29:1493-504. DOI: 10.1096/fj.14-261214.
17. 17. Lucas RJ, Lall GS, Allen AE, Brown TM. How rod, cone, and melanopsin photoreceptors come together to enlighten the mammalian circadian clock, 2012, p. 1-18. DOI: 10.1016/B978-0-444-59427-3.00001-0.
18. 18. Holmes M., Mistlberger R. Food anticipatory activity and photic entrainment in food-restricted BALB/c mice. Physiol Behav 2000;68:655-66. DOI: 10.1016/S0031-9384(99)00231 -0.
19. 19. Castillo MR, Hochstetler KJ, Tavernier RJ, Greene DM, Bult-Ito A. Entrainment of the master circadian clock by scheduled feeding. Am J Physiol Integr Comp Physiol 2004;287:R551-5. DOI: 10.1152/ajpregu.00247.2004.
20. 20. Bechtold DA, Loudon ASI. Hypothalamic clocks and rhythms in feeding behaviour. Trends Neurosci 2013;36:74-82. DOI: 10.1016/j.tins.2012.12.007.
21. 21. Guzmán-Ruiz M, Saderi N, Cazarez-Márquez F, et al. The suprachiasmatic nucleus changes the daily activity of the arcuate nucleus α-MSH neurons in male rats. Endocrinology 2014;155:525-35. DOI: 10.1210/en.2013-1604.
22. 22. Mistlberger RE. Neurobiology of food anticipatory circadian rhythms. Physiol Behav 2011;104:535-45. DOI: 10.1016/j.physbeh.2011.04.015.
23. 23. Feillet CA, Albrecht U, Challet E. “Feeding time” for the brain: A matter of clocks. J Physiol 2006;100:252-60. DOI: 10.1016/j.jphysparis.2007.05.002.
24. 24. Guilding C, Piggins HD. Challenging the omnipotence of the suprachiasmatic timekeeper: are circadian oscillators present throughout the mammalian brain? Eur J Neurosci 2007;25:3195-216. DOI: 10.1111/j.1460-9568.2007.05581. x.
25. 25. Albrecht U. Timing to perfection: The biology of central and peripheral circadian clocks. Neuron 2012;74:246-60. DOI: 10.1016/j.neuron.2012.04.006.
26. 26. Damiola F, Le Minh N, Preitner N, Kornmann B, Fleury-Olela F, Schibler U. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev 2000;14:2950-61. DOI: 10.1101/gad.183500.
27. 27. Stokkan K-A, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science 2001;291:490-3. DOI: 10.1126/science. 291.5503. 490.
28. 28. Kräuchi K, Cajochen C, Werth E, Wirz-Justice A. Alteration of internal circadian phase relationships after morning versus evening carbohydrate-rich meals in humans. J Biol Rhythms 2002;17:364-76. DOI: 10.1177/074873040201700 409.
29. 29. Wehrens SMT, Christou S, Isherwood C, et al. Meal timing regulates the human circadian system. Curr Biol 2017;27:1768-1775.e3. DOI: 10.1016/j.cub.2017.04.059.
30. 30. Gonzalez R, Mohan H, Unniappan S. Nucleobindins: Bioactive precursor proteins encoding putative endocrine factors? Gen Comp Endocrinol 2012;176:341-6. DOI: 10.1016/ j.ygcen.2011.11.021.
31. 31. Moncrief ND, Kretsinger RH, Goodman M. Evolution of EF-hand calcium-modulated proteins. I. Relationships based on amino acid sequences. J Mol Evol 1990;30:522-62. DOI: 10.1007/BF02101108.
32. 32. Mohan H, Unniappan S. Phylogenetic aspects of nucleobindin-2/nesfatin-1. Curr Pharm Des 2013;19:6929-34. DOI: 10.2174/138161281939131127124149.
33. 33. Shimizu H, Oh-I S, Hashimoto K, et al. Peripheral administration of nesfatin-1 reduces food intake in mice: The leptin-independent mechanism. Endocrinology 2009;150: 662-71. DOI: 10.1210/en.2008-0598.
34. 34. Mortazavi S, Gonzalez R, Ceddia R, Unniappan S. Long-term infusion of nesfatin-1 causes a sustained regulation of whole-body energy homeostasis of male Fischer 344 rats. Front Cell Dev Biol 2015;3. DOI: 10.3389/fcell. 2015.00022.
35. 35. Mohan H, Ramesh N, Mortazavi S, Le A, Iwakura H, Unniappan S. Nutrients differentially regulate nucleobindin-2/Nesfatin-1 in vitro in cultured stomach ghrelinoma (MGN3-1) cells and in vivo in male mice. PLoS One 2014;9:e115102. DOI: 10.1371/journal.pone.0115102.
36. 36. Wernecke K, Lamprecht I, Jöhren O, Lehnert H, Schulz C. Nesfatin-1 increases energy expenditure and reduces food intake in rats. Obesity 2014;22:1662-8. DOI: 10.1002/ oby.20736.
37. 37. Kelestimur H, Sahin Z, Bulmus O, Ozcan M, Canpolat S. Kisspeptin antagonist, peptide 234, blocks both kisspeptin-10 and nesfatin-1-induced luteinizing hormone release in the female rats. J Sex Med 2015;12:287.
38. 38. Sahin Z, Cuce G, Ozcan M, et al. Nesfatin-1 may interfere with kisspeptin/kiss1 system in gonadal activity of female rats. Acta Physiol 2016;218 (S709):25.
39. 39. Swanson LW, Sawchenko PE. Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 1983;6:269-324. DOI: 10.1146/annurev.ne.06.030183.001413.
40. 40. Buijs RM, Hermes MHLJ, Kalsbeek A. The suprachiasmatic nucleus-paraventricular nucleus interactions: a bridge to the neuroendocrine and autonomic nervous system. Prog Brain Res 1998;119:365-82. DOI: 10.1016/s0079-6123(08) 61581-2.
41. 41. Kalsbeek A. Suprachiasmatic GABAergic inputs to the paraventricular nucleus control plasma glucose concentrations in the rat via sympathetic innervation of the liver. J Neurosci 2004;24:7604-13. DOI: 10.1523/JNEUROSCI. 5328-03.2004.
42. 42. Kim ER, Xu Y, Cassidy RM, et al. Paraventricular hypothalamus mediates diurnal rhythm of metabolism. Nat Commun 2020;11:3794. DOI: 10.1038/s41467-020-17578-7.
43. 43. Vrang N, Larsen PJ, Mikkelsen JD. Direct projection from the suprachiasmatic nucleus to hypophysiotrophic corticotropin-releasing factor immunoreactive cells in the paraventricular nucleus of the hypothalamus demonstrated by means of Phaseolus vulgaris-leucoagglutinin tract tracing. Brain Res 1995;684:61-9. DOI: 10.1016/0006-8993 (95)00425-P.
44. 44. Nakata M, Kumari P, Kita R, et al. Circadian clock component BMAL1 in the paraventricular nucleus regulates glucose metabolism. Nutrients 2021;13:4487. DOI: 10.3390/ nu13124487.
45. 45. Goebel M, Stengel A, Wang L, Taché Y. Central nesfatin-1 reduces the nocturnal food intake in mice by reducing meal size and increasing inter-meal intervals. Peptides 2011;32:36-43. DOI: 10.1016/j.peptides.2010.09.027.
46. 46. Stengel A, Taché Y. Minireview: Nesfatin-1-an emerging new player in the brain-gut, endocrine, and metabolic axis. Endocrinology 2011;152:4033-8. DOI: 10.1210/en. 2011-1500.
47. 47. Goebel-Stengel M, Wang L. Central and peripheral expression and distribution of NUCB2/nesfatin-1. Curr Pharm Des 2013;19:6935-40. DOI: 10.2174/138161281939 131127124814.
48. 48. Stengel A, Goebel M, Wang L, et al. Central nesfatin-1 reduces dark-phase food intake and gastric emptying in rats: Differential role of corticotropin-releasing factor2 receptor. Endocrinology 2009;150:4911-9. DOI: 10.1210/en.2009-0578.
49. 49. Nonogaki K, Ohba Y, Sumii M, Oka Y. Serotonin systems upregulate the expression of hypothalamic NUCB2 via 5-HT2C receptors and induce anorexia via a leptin-independent pathway in mice. Biochem Biophys Res Commun 2008;372:186-90. DOI: 10.1016/j.bbrc.2008.05.010.
50. 50. Maejima Y, Sedbazar U, Suyama S, et al. Nesfatin-1-regulated oxytocinergic signaling in the paraventricular nucleus causes anorexia through a leptin-independent melanocortin pathway. Cell Metab 2009;10:355-65. DOI: 10.1016/j.cmet. 2009.09.002.
51. 51. Darambazar G, Nakata M, Okada T, et al. Paraventricular NUCB2/nesfatin-1 is directly targeted by leptin and mediates its anorexigenic effect. Biochem Biophys Res Commun 2015;456:913-8. DOI: 10.1016/j.bbrc.2014.12. 065.
52. 52. Tabarin A, Diz-Chaves Y, Consoli D, et al. Role of the corticotropin-releasing factor receptor type 2 in the control of food intake in mice: a meal pattern analysis. Eur J Neurosci 2007;26:2303-14. DOI: 10.1111/j.1460-9568.2007. 05856.x.
53. 53. Yosten GLC, Samson WK. Nesfatin-1 exerts cardiovascular actions in brain: possible interaction with the central melanocortin system. Am J Physiol Integr Comp Physiol 2009;297:R330-6. DOI: 10.1152/ajpregu.90867.2008.
54. 54. Yosten GLC, Samson WK. The anorexigenic and hypertensive effects of nesfatin-1 are reversed by pretreatment with an oxytocin receptor antagonist. Am J Physiol Integr Comp Physiol 2010;298:R1642-7. DOI: 10.1152/ajpregu. 00804. 2009.
55. 55. Sedbazar U, Maejima Y, Nakata M, Mori M, Yada T. Paraventricular NUCB2/nesfatin-1 rises in synchrony with feeding suppression during early light phase in rats. Biochem Biophys Res Commun 2013;434:434-8. DOI: 10.1016/j.bbrc. 2013.03.090.
56. 56. Nakata M, Gantulga D, Santoso P, et al. Paraventricular NUCB2/Nesfatin-1 supports oxytocin and vasopressin neurons to control feeding behavior and fluid balance in male mice. Endocrinology 2016;157:2322-32. DOI: 10.1210/en. 2015-2082.
57. 57. Ongür D, An X, Price JL. Prefrontal cortical projections to the hypothalamus in macaque monkeys. J Comp Neurol 1998;401:480-505.
58. 58. Stengel A, Goebel M, Yakubov I, et al. Identification and characterization of nesfatin-1 immunoreactivity in endocrine cell types of the rat gastric oxyntic mucosa. Endocrinology 2009;150:232-8. DOI: 10.1210/en.2008-0747.
59. 59. Garcia-Galiano D, Navarro VM, Roa J, et al. The anorexigenic neuropeptide, nesfatin-1, is indispensable for normal puberty onset in the female rat. J Neurosci 2010;30:7783-92. DOI: 10.1523/JNEUROSCI.5828-09. 2010.