The role of circadian rhythm in the regulation of cellular protein profiles in the brain

Background/aim: Circadian rhythm plays a significant role in the regulation of almost all kinds of physiological processes. In addition, it may also have a direct or indirect effect on the neurodegenerative processes, including Alzheimer’s disease, Parkinson’s disease, and ischemic stroke. Therefore, the identification of circadian rhythm-related proteins is crucial to be able to understand the molecular mechanism of the circadian rhythm and to define new therapeutic target for the treatment of degenerative disorders. Materials and methods: To identify the light and dark regulated proteins, 8–12 weeks, male Balb/C mice were used at two different time points (morning (Zeitgeber time-0 (ZT0)) and midnight (ZT18)) under physiological conditions. Therefore, brain tissues were analyzed via liquid chromatography tandem mass spectrometry. Results: A total of 1621 different proteins were identified between ZT0 and ZT18 mice. Among these proteins, 23 proteins were differentially expressed (p < 0.05 and fold change 1.4) in ZT18 mice, 11 upregulated (AKAP10, ALDOC, BLK, NCALD, NFL, PDE10A, PICAL, PSMB6, RL10, SH3L3, and SYNJ1), and 12 downregulated (AT2A2, AT2B1, CPNE5, KAP3, MAON, NPM, PI51C, PPR1B, SAM50, TOM70, TY3H, and VAPA) as compared with ZT0 mice. Conclusion: Taken together, here we identified circadian rhythm-related proteins, and our further analysis revealed that these proteins play significant roles in molecular function, membrane trafficking, biogenesis, cellular process, metabolic process, and neurodegenerative disorders such as Parkinson’s disease.Key words: Circadian rhythm, lc-ms/ms, PDE10A, proteomics, zeitgeber time

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1. Xie Y, Tang Q, Chen G, Xie M, Yu S et al. New insights into the circadian rhythm and its related diseases. Frontiers in Physiology 2019; 10: 682. doi: 10.3389/fphys.2019.00682
2. Panda S, Hogenesch JB, Kay SA. Circadian rhythms from flies to human. Nature 2002; 417 (6886): 329-335. doi: 10.1038/417329a
3. Reppert SM, Weaver DR. Coordination of circadian timing in mammals. Nature 2002; 418 (6901): 935-941. doi: 10.1038/nature00965
4. Hastings MH, Maywood ES, Brancaccio M. Generation of circadian rhythms in the suprachiasmatic nucleus. Nature Reviews Neuroscience 2018; 19 (8): 453-469. doi: 10.1038/s41583-018-0026-z
5. Patke A, Young MW, Axelrod S. Molecular mechanisms and physiological importance of circadian rhythms. Nature Reviews Molecular Cell Biology 2020; 21 (2): 67-84. doi: 10.1038/s41580-019-0179-2
6. Ripamonti L, Riva R, Maioli F, Zenesini C, Procaccianti G. Daily variation in the occurrence of different subtypes of stroke. Stroke Research and Treatment 2017; 2017: 9091250. doi: 10.1155/2017/9091250
7. Beker MC, Caglayan B, Yalcin E, Caglayan AB, Turkseven S et al. Time-of-day dependent neuronal injury after ischemic stroke: implication of circadian clock transcriptional factor Bmal1 and survival kinase AKT. Molecular Neurobiology 2018; 55 (3): 2565-2576. doi: 10.1007/s12035-017-0524-4
8. Hood S, Amir S. Neurodegeneration and the circadian clock. Frontiers in Aging Neuroscience 2017; 9: 170. doi: 10.3389/fnagi.2017.00170
9. Wisniewski JR, Zougman A, Nagaraj N, Mann M. Universal sample preparation method for proteome analysis. Nature Methods 2009; 6 (5): 359-362. doi: 10.1038/nmeth.1322
10. Yalcin E, Beker MC, Turkseven S, Caglayan B, Gurel B et al. Evidence that melatonin downregulates Nedd4-1 E3 ligase and its role in cellular survival. Toxicology and Applied Pharmacology 2019; 379: 114686. doi: 10.1016/j.taap.2019.114686
11. Acioglu C, Mirabelli E, Baykal AT, Ni L, Ratnayake A et al. Toll like receptor 9 antagonism modulates spinal cord neuronal function and survival: direct versus astrocyte-mediated mechanisms. Brain, Behavior, and Immunity 2016; 56: 310- 324. doi: 10.1016/j.bbi.2016.03.027
12. Beker M, Caglayan AB, Beker MC, Altunay S, Karacay R et al. Lentivirally administered glial cell line-derived neurotrophic factor promotes post-ischemic neurological recovery, brain remodeling and contralesional pyramidal tract plasticity by regulating axonal growth inhibitors and guidance proteins. Experimental Neurology 2020; 331: 113364. doi: 10.1016/j.expneurol.2020.113364
13. Leng Y, Musiek ES, Hu K, Cappuccio FP, Yaffe K. Association between circadian rhythms and neurodegenerative diseases. The Lancet Neurology 2019; 18 (3): 307-318. doi: 10.1016/S1474-4422(18)30461-7
14. He S, Zhang X, Qu S. Glutamate, glutamate transporters, and circadian rhythm sleep disorders in neurodegenerative diseases. ACS Chemical Neuroscience 2019; 10 (1): 175-181. doi: 10.1021/acschemneuro.8b00419
15. Fifel K, Videnovic A. Circadian alterations in patients with neurodegenerative diseases: Neuropathological basis of underlying network mechanisms. Neurobiology of Disease 2020; 144: 105029. doi: 10.1016/j.nbd.2020.105029
16. Wang L, Sunahara RK, Krumins A, Perkins G, Crochiere ML et al. Cloning and mitochondrial localization of full-length DAKAP2, a protein kinase A anchoring protein. Proceedings of the National Academy of Sciences of the United States of America 2001; 98 (6): 3220-3225. doi: 10.1073/pnas.051633398
17. Xie Z, Adamowicz WO, Eldred WD, Jakowski AB, Kleiman RJ et al. Cellular and subcellular localization of PDE10A, a striatumenriched phosphodiesterase. Neuroscience 2006; 139 (2): 597-607. doi: 10.1016/j.neuroscience.2005.12.042
18. Seeger TF, Bartlett B, Coskran TM, Culp JS, James LC et al. Immunohistochemical localization of PDE10A in the rat brain. Brain Research 2003; 985 (2): 113-126. doi: 10.1016/s0006- 8993(03)02754-9
19. Cardinale A, Fusco FR. Inhibition of phosphodiesterases as a strategy to achieve neuroprotection in Huntington's disease. CNS Neuroscience & Therapeutics 2018; 24 (4): 319-328. doi: 10.1111/cns.12834
20. Birjandi SZ, Abduljawad N, Nair S, Dehghani M, Suzuki K et al. Phosphodiesterase 10A inhibition leads to brain regionspecific recovery based on stroke type. Translational Stroke Research 2020. doi: 10.1007/s12975-020-00819-8
21. Hemmings HC, Jr., Greengard P, Tung HY, Cohen P. DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature 1984; 310 (5977): 503-505. doi: 10.1038/310503a0
22. Yger M, Girault JA. DARPP-32, Jack of all trades... Master of which? Frontiers in Behavioral Neuroscience 2011; 5: 56. doi: 10.3389/fnbeh.2011.00056
23. Upadhyay A, Hosseinibarkooie S, Schneider S, Kaczmarek A, Torres-Benito L et al. Neurocalcin delta knockout impairs adult neurogenesis whereas half reduction is not pathological. Frontiers in Molecular Neuroscience 2019; 12: 19. doi: 10.3389/fnmol.2019.00019
24. Kho C, Lee A, Hajjar RJ. Altered sarcoplasmic reticulum calcium cycling--targets for heart failure therapy. Nature Reviews Cardiology 2012; 9 (12): 717-733. doi: 10.1038/nrcardio.2012.145
25. Satoh K, Matsu-Ura T, Enomoto M, Nakamura H, Michikawa T et al. Highly cooperative dependence of sarco/endoplasmic reticulum calcium ATPase SERCA2a pump activity on cytosolic calcium in living cells. The Journal of Biological Chemistry 2011; 286 (23): 20591-20599. doi: 10.1074/jbc.M110.204685
26. Chang YC, Tsai HF, Huang SP, Chen CL, Hsiao M et al. Enrichment of aldolase C correlates with low non-mutated IDH1 expression and predicts a favorable prognosis in glioblastomas. Cancers 2019; 11 (9). doi: 10.3390/cancers11091238
27. Petersen DL, Berthelsen J, Willerslev-Olsen A, Fredholm S, Dabelsteen S et al. A novel BLK-induced tumor model. Tumor Biology 2017; 39 (7): 1010428317714196. doi: 10.1177/1010428317714196
28. Bernal-Quiros M, Wu YY, Alarcon-Riquelme ME, CastillejoLopez C. BANK1 and BLK act through phospholipase C gamma 2 in B-cell signaling. PloS One 2013; 8 (3): e59842. doi: 10.1371/journal.pone.0059842
29. Yang H, Wang L, Zang C, Wang Y, Shang J et al. Src inhibition attenuates neuroinflammation and protects dopaminergic neurons in parkinson's disease models. Frontiers in Neuroscience 2020; 14: 45. doi: 10.3389/fnins.2020.00045
30. Vriend J, Marzban H. The ubiquitin-proteasome system and chromosome 17 in cerebellar granule cells and medulloblastoma subgroups. Cellular and Molecular Life Sciences 2017; 74 (3): 449-467. doi: 10.1007/s00018-016- 2354-3
31. Shi J, Zhang L, Zhou D, Zhang J, Lin Q et al. Biological function of ribosomal protein L10 on cell behavior in human epithelial ovarian cancer. Journal of Cancer 2018; 9 (4): 745-756. doi: 10.7150/jca.21614
32. Khalil AA. Biomarker discovery: a proteomic approach for brain cancer profiling. Cancer Science 2007; 98 (2): 201-213. doi: 10.1111/j.1349-7006.2007.00374.x
33. Ashton NJ, Leuzy A, Lim YM, Troakes C, Hortobagyi T et al. Increased plasma neurofilament light chain concentration correlates with severity of post-mortem neurofibrillary tangle pathology and neurodegeneration. Acta Neuropathologica Communications 2019; 7 (1): 5. doi: 10.1186/s40478-018- 0649-3
34. Xu W, Tan L, Yu JT. The role of PICALM in Alzheimer's disease. Molecular Neurobiology 2015; 52 (1): 399-413. doi: 10.1007/s12035-014-8878-3
35. Cremona O, Di Paolo G, Wenk MR, Luthi A, Kim WT et al. Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 1999; 99 (2): 179-188. doi: 10.1016/s0092-8674(00)81649-9
36. Drouet V, Lesage S. Synaptojanin 1 mutation in Parkinson's disease brings further insight into the neuropathological mechanisms. BioMed Research International 2014; 2014: 289728. doi: 10.1155/2014/289728
37. Ding X, Jin Y, Wu Y, Wu Y, Wu H et al. Localization and cellular distribution of CPNE5 in embryonic mouse brain. Brain Research 2008; 1224: 20-28. doi: 10.1016/j.brainres.2008.05.051
38. Ding XF, Wang HJ, Qian L, Hu ZY, Feng SF et al. Cpne5 is Involved in Regulating Rodent Anxiety Level. CNS Neuroscience & Therapeutics 2017; 23 (3): 266-268. doi: 10.1111/cns.12674
39. Zhang Q, Li J, Tan XP, Zhao Q. Effects of ME3 on the proliferation, invasion and metastasis of pancreatic cancer cells through epithelial-mesenchymal transition. Neoplasma 2019; 66 (6): 896-907. doi: 10.4149/neo_2019_190119N59
40. Hasan NM, Longacre MJ, Stoker SW, Kendrick MA, MacDonald MJ. Mitochondrial malic enzyme 3 is important for insulin secretion in pancreatic beta-cells. Molecular Endocrinology 2015; 29 (3): 396-410. doi: 10.1210/me.2014-1249
41. Ahn JY, Liu X, Cheng D, Peng J, Chan PK et al. Nucleophosmin/B23, a nuclear PI(3,4,5)P(3) receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD. Molecular Cell 2005; 18 (4): 435-445. doi: 10.1016/j.molcel.2005.04.010
42. Di Paolo G, Pellegrini L, Letinic K, Cestra G, Zoncu R et al. Recruitment and regulation of phosphatidylinositol phosphate kinase type 1 gamma by the FERM domain of talin. Nature 2002; 420 (6911): 85-89. doi: 10.1038/nature01147
43. Zhu T, Chappel JC, Hsu FF, Turk J, Aurora R et al. Type I phosphotidylinosotol 4-phosphate 5-kinase gamma regulates osteoclasts in a bifunctional manner. The Journal of Biological Chemistry 2013; 288 (8): 5268-5277. doi: 10.1074/jbc.M112.446054
44. Jian F, Chen D, Chen L, Yan C, Lu B et al. Sam50 regulates PINK1- Parkin-mediated mitophagy by controlling PINK1 stability and mitochondrial morphology. Cell Reports 2018; 23 (10): 2989- 3005. doi: 10.1016/j.celrep.2018.05.015
45. Chai YL, Xing H, Chong JR, Francis PT, Ballard CG et al. Mitochondrial translocase of the outer membrane alterations may underlie dysfunctional oxidative phosphorylation in Alzheimer's disease. Journal of Alzheimer's Disease 2018; 61 (2): 793-801. doi: 10.3233/JAD-170613
46. Kobayashi K, Nagatsu T. Molecular genetics of tyrosine 3- monooxygenase and inherited diseases. Biochemical and Biophysical Research Communications 2005; 338 (1): 267- 270. doi: 10.1016/j.bbrc.2005.07.186
47. Nagatsu T, Levitt M, Udenfriend S. Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. The Journal of Biological Chemistry 1964; 239: 2910-2917. doi: 10.1016/S0021-9258(18)93832-9
48. Nagatsu T, Nakashima A, Ichinose H, Kobayashi K. Human tyrosine hydroxylase in Parkinson's disease and in related disorders. Journal of Neural Transmission 2019; 126 (4): 397- 409. doi: 10.1007/s00702-018-1903-3
49. Wyles JP, McMaster CR, Ridgway ND. Vesicle-associated membrane protein-associated protein-A (VAP-A) interacts with the oxysterol-binding protein to modify export from the endoplasmic reticulum. The Journal of Biological Chemistry 2002; 277 (33): 29908-29918. doi: 10.1074/jbc.M201191200