Degradation of STK16 via KCTD17 with Ubiquitin–Proteasome System in Relation to Sleep–Wake Cycle
Abstract
:1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Animals
4.2. Quantitative PCR (qPCR)
4.3. Expression Vectors and Cell Culture
4.4. Immunoprecipitation
4.5. Immunoblotting Analysis
4.6. Statistical Analyses
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Modi, V.; Dunbrack, R.L., Jr. A Structurally-Validated Multiple Sequence Alignment of 497 Human Protein Kinase Domains. Sci. Rep. 2019, 9, 19790. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ligos, J.M.; Gerwin, N.; Fernandez, P.; Gutierrez-Ramos, J.C.; Bernad, A. Cloning, expression analysis, and functional characterization of PKL12, a member of a new subfamily of ser/thr kinases. Biochem. Biophys. Res. Commun. 1998, 249, 380–384. [Google Scholar] [CrossRef] [PubMed]
- Stairs, D.B.; Perry Gardner, H.; Ha, S.I.; Copeland, N.G.; Gilbert, D.J.; Jenkins, N.A.; Chodosh, L.A. Cloning and characterization of Krct, a member of a novel subfamily of serine/threonine kinases. Hum. Mol. Genet. 1998, 7, 2157–2166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kurioka, K.; Nakagawa, K.; Denda, K.; Miyazawa, K.; Kitamura, N. Molecular cloning and characterization of a novel protein serine/threonine kinase highly expressed in mouse embryo. Biochim. Biophys. Acta 1998, 1443, 275–284. [Google Scholar] [CrossRef] [PubMed]
- Berson, A.E.; Young, C.; Morrison, S.L.; Fujii, G.H.; Sheung, J.; Wu, B.; Bolen, J.B.; Burkhardt, A.L. Identification and characterization of a myristylated and palmitylated serine/threonine protein kinase. Biochem. Biophys. Res. Commun. 1999, 259, 533–538. [Google Scholar] [CrossRef]
- Ohta, S.; Takeuchi, M.; Deguchi, M.; Tsuji, T.; Gahara, Y.; Nagata, K. A novel transcriptional factor with Ser/Thr kinase activity involved in the transforming growth factor (TGF)-beta signalling pathway. Biochem. J. 2000, 350, 395–404. [Google Scholar] [CrossRef]
- Wang, J.; Ji, X.; Liu, J.; Zhang, X. Serine/Threonine Protein Kinase STK16. Int. J. Mol. Sci. 2019, 20, 1760. [Google Scholar] [CrossRef] [Green Version]
- Guinea, B.; Ligos, J.M.; Lain de Lera, T.; Martin-Caballero, J.; Flores, J.; Gonzalez de la Pena, M.; Garcia-Castro, J.; Bernad, A. Nucleocytoplasmic shuttling of STK16 (PKL12), a Golgi-resident serine/threonine kinase involved in VEGF expression regulation. Exp. Cell Res. 2006, 312, 135–144. [Google Scholar] [CrossRef]
- Ligos, J.M.; de Lera, T.L.; Hinderlich, S.; Guinea, B.; Sanchez, L.; Roca, R.; Valencia, A.; Bernad, A. Functional interaction between the Ser/Thr kinase PKL12 and N-acetylglucosamine kinase, a prominent enzyme implicated in the salvage pathway for GlcNAc recycling. J. Biol. Chem. 2002, 277, 6333–6343. [Google Scholar] [CrossRef] [Green Version]
- Liu, J.; Yang, X.; Li, B.; Wang, J.; Wang, W.; Liu, J.; Liu, Q.; Zhang, X. STK16 regulates actin dynamics to control Golgi organization and cell cycle. Sci. Rep. 2017, 7, 44607. [Google Scholar] [CrossRef]
- Sorrell, F.J.; Szklarz, M.; Abdul Azeez, K.R.; Elkins, J.M.; Knapp, S. Family-wide Structural Analysis of Human Numb-Associated Protein Kinases. Structure 2016, 24, 401–411. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eswaran, J.; Bernad, A.; Ligos, J.M.; Guinea, B.; Debreczeni, J.E.; Sobott, F.; Parker, S.A.; Najmanovich, R.; Turk, B.E.; Knapp, S. Structure of the human protein kinase MPSK1 reveals an atypical activation loop architecture. Structure 2008, 16, 115–124. [Google Scholar] [CrossRef] [PubMed]
- Zhou, J.; Ma, S.; Wang, D.; Zeng, J.; Jiang, T. FreePSI: An alignment-free approach to estimating exon-inclusion ratios without a reference transcriptome. Nucleic Acids Res. 2018, 46, e11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, J.; Wang, Y.; Meng, X.; Liang, H. Modulation of transcriptional activity in brain lower grade glioma by alternative splicing. PeerJ 2018, 6, e4686. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, H.; Cho, S.J.; Moon, I.S. The non-canonical effect of N-acetyl-D-glucosamine kinase on the formation of neuronal dendrites. Mol. Cells 2014, 37, 248–256. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Islam, M.A.; Sharif, S.R.; Lee, H.; Moon, I.S. N-Acetyl-D-Glucosamine Kinase Promotes the Axonal Growth of Developing Neurons. Mol. Cells 2015, 38, 876–885. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Islam, M.A.; Sharif, S.R.; Lee, H.; Seog, D.H.; Moon, I.S. N-acetyl-D-glucosamine kinase interacts with dynein light-chain roadblock type 1 at Golgi outposts in neuronal dendritic branch points. Exp. Mol. Med. 2015, 47, e177. [Google Scholar] [CrossRef] [Green Version]
- Butkinaree, C.; Park, K.; Hart, G.W. O-linked beta-N-acetylglucosamine (O-GlcNAc): Extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 2010, 1800, 96–106. [Google Scholar] [CrossRef] [Green Version]
- Love, D.C.; Hanover, J.A. The hexosamine signaling pathway: Deciphering the “O-GlcNAc code”. Sci. STKE Signal Transduct. Knowl. Environ. 2005, 2005, re13. [Google Scholar] [CrossRef]
- Hayakawa, K.; Sakamoto, Y.; Kanie, O.; Ohtake, A.; Daikoku, S.; Ito, Y.; Shiota, K. Reactivation of hyperglycemia-induced hypocretin (HCRT) gene silencing by N-acetyl-d-mannosamine in the orexin neurons derived from human iPS cells. Epigenetics 2017, 12, 764–778. [Google Scholar] [CrossRef]
- Hayakawa, K.; Hirosawa, M.; Tabei, Y.; Arai, D.; Tanaka, S.; Murakami, N.; Yagi, S.; Shiota, K. Epigenetic switching by the metabolism-sensing factors in the generation of orexin neurons from mouse embryonic stem cells. J. Biol. Chem. 2013, 288, 17099–17110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hayakawa, K.; Ohgane, J.; Tanaka, S.; Yagi, S.; Shiota, K. Oocyte-specific linker histone H1foo is an epigenomic modulator that decondenses chromatin and impairs pluripotency. Epigenetics 2012, 7, 1029–1036. [Google Scholar] [CrossRef] [Green Version]
- de Lecea, L.; Sutcliffe, J.G. The hypocretins and sleep. FEBS J. 2005, 272, 5675–5688. [Google Scholar] [CrossRef] [PubMed]
- Sakurai, T. The neural circuit of orexin (hypocretin): Maintaining sleep and wakefulness. Nat. Rev. Neurosci. 2007, 8, 171–181. [Google Scholar] [CrossRef] [PubMed]
- Saper, C.B.; Fuller, P.M.; Pedersen, N.P.; Lu, J.; Scammell, T.E. Sleep state switching. Neuron 2010, 68, 1023–1042. [Google Scholar] [CrossRef] [Green Version]
- Oughtred, R.; Rust, J.; Chang, C.; Breitkreutz, B.J.; Stark, C.; Willems, A.; Boucher, L.; Leung, G.; Kolas, N.; Zhang, F.; et al. The BioGRID database: A comprehensive biomedical resource of curated protein, genetic, and chemical interactions. Protein Sci. A Publ. Protein Soc. 2021, 30, 187–200. [Google Scholar] [CrossRef] [PubMed]
- Kasahara, K.; Kawakami, Y.; Kiyono, T.; Yonemura, S.; Kawamura, Y.; Era, S.; Matsuzaki, F.; Goshima, N.; Inagaki, M. Ubiquitin-proteasome system controls ciliogenesis at the initial step of axoneme extension. Nat. Commun. 2014, 5, 5081. [Google Scholar] [CrossRef] [Green Version]
- Lecker, S.H.; Goldberg, A.L.; Mitch, W.E. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J. Am. Soc. Nephrol. JASN 2006, 17, 1807–1819. [Google Scholar] [CrossRef]
- Fan, W.H.; Hou, Y.; Meng, F.K.; Wang, X.F.; Luo, Y.N.; Ge, P.F. Proteasome inhibitor MG-132 induces C6 glioma cell apoptosis via oxidative stress. Acta Pharmacol. Sin. 2011, 32, 619–625. [Google Scholar] [CrossRef]
- Li, W.; Ye, Y. Polyubiquitin chains: Functions, structures, and mechanisms. Cell. Mol. Life Sci. CMLS 2008, 65, 2397–2406. [Google Scholar] [CrossRef]
- Pickart, C.M. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 2001, 70, 503–533. [Google Scholar] [CrossRef] [PubMed]
- Weissman, A.M. Themes and variations on ubiquitylation. Nat. Reviews. Mol. Cell Biol. 2001, 2, 169–178. [Google Scholar] [CrossRef] [PubMed]
- Huttlin, E.L.; Bruckner, R.J.; Navarrete-Perea, J.; Cannon, J.R.; Baltier, K.; Gebreab, F.; Gygi, M.P.; Thornock, A.; Zarraga, G.; Tam, S.; et al. Dual proteome-scale networks reveal cell-specific remodeling of the human interactome. Cell 2021, 184, 3022–3040+e28. [Google Scholar] [CrossRef]
- Young, B.D.; Sha, J.; Vashisht, A.A.; Wohlschlegel, J.A. Human Multisubunit E3 Ubiquitin Ligase Required for Heterotrimeric G-Protein beta-Subunit Ubiquitination and Downstream Signaling. J. Proteome Res. 2021, 20, 4318–4330. [Google Scholar] [CrossRef]
- Prakash, S.; Tian, L.; Ratliff, K.S.; Lehotzky, R.E.; Matouschek, A. An unstructured initiation site is required for efficient proteasome-mediated degradation. Nat. Struct. Mol. Biol. 2004, 11, 830–837. [Google Scholar] [CrossRef] [PubMed]
- Beekman, J.M.; Vervoort, S.J.; Dekkers, F.; van Vessem, M.E.; Vendelbosch, S.; Brugulat-Panes, A.; van Loosdregt, J.; Braat, A.K.; Coffer, P.J. Syntenin-mediated regulation of Sox4 proteasomal degradation modulates transcriptional output. Oncogene 2012, 31, 2668–2679. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kikuma, K.; Li, X.; Perry, S.; Li, Q.; Goel, P.; Chen, C.; Kim, D.; Stavropoulos, N.; Dickman, D. Cul3 and insomniac are required for rapid ubiquitination of postsynaptic targets and retrograde homeostatic signaling. Nat. Commun. 2019, 10, 2998. [Google Scholar] [CrossRef] [Green Version]
- Pfeiffenberger, C.; Allada, R. Cul3 and the BTB adaptor insomniac are key regulators of sleep homeostasis and a dopamine arousal pathway in Drosophila. PLoS Genet. 2012, 8, e1003003. [Google Scholar] [CrossRef] [Green Version]
- Stavropoulos, N.; Young, M.W. insomniac and Cullin-3 regulate sleep and wakefulness in Drosophila. Neuron 2011, 72, 964–976. [Google Scholar] [CrossRef] [Green Version]
- Ryu, K.Y.; Fujiki, N.; Kazantzis, M.; Garza, J.C.; Bouley, D.M.; Stahl, A.; Lu, X.Y.; Nishino, S.; Kopito, R.R. Loss of polyubiquitin gene Ubb leads to metabolic and sleep abnormalities in mice. Neuropathol. Appl. Neurobiol. 2010, 36, 285–299. [Google Scholar] [CrossRef]
- Peng, W.; Wu, Z.; Song, K.; Zhang, S.; Li, Y.; Xu, M. Regulation of sleep homeostasis mediator adenosine by basal forebrain glutamatergic neurons. Science 2020, 369, eabb0556. [Google Scholar] [CrossRef]
- Szymusiak, R.; McGinty, D. Hypothalamic regulation of sleep and arousal. Ann. N.Y. Acad. Sci. 2008, 1129, 275–286. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, M.; Tahara, Y. Timing of Food/Nutrient Intake and Its Health Benefits. J. Nutr. Sci. Vitam. 2022, 68, S2–S4. [Google Scholar] [CrossRef] [PubMed]
- Lee, Y.; Field, J.M.; Sehgal, A. Circadian Rhythms, Disease and Chronotherapy. J. Biol. Rhythm. 2021, 36, 503–531. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Ma, J.; Miyoshi, C.; Li, Y.; Sato, M.; Ogawa, Y.; Lou, T.; Ma, C.; Gao, X.; Lee, C.; et al. Quantitative phosphoproteomic analysis of the molecular substrates of sleep need. Nature 2018, 558, 435–439. [Google Scholar] [CrossRef] [PubMed]
- Fink, C.C.; Meyer, T. Molecular mechanisms of CaMKII activation in neuronal plasticity. Curr. Opin. Neurobiol. 2002, 12, 293–299. [Google Scholar] [CrossRef]
- Tone, D.; Ode, K.L.; Zhang, Q.; Fujishima, H.; Yamada, R.G.; Nagashima, Y.; Matsumoto, K.; Wen, Z.; Yoshida, S.Y.; Mitani, T.T.; et al. Distinct phosphorylation states of mammalian CaMKIIbeta control the induction and maintenance of sleep. PLoS Biol. 2022, 20, e3001813. [Google Scholar] [CrossRef]
- Belfort, G.M.; Kandror, K.V. Cellugyrin and synaptogyrin facilitate targeting of synaptophysin to a ubiquitous synaptic vesicle-sized compartment in PC12 cells. J. Biol. Chem. 2003, 278, 47971–47978. [Google Scholar] [CrossRef] [Green Version]
- Tanaka, S.; Honda, Y.; Honda, M.; Yamada, H.; Honda, K.; Kodama, T. Anti-Tribbles Pseudokinase 2 (TRIB2)-Immunization Modulates Hypocretin/Orexin Neuronal Functions. Sleep 2017, 40, zsw036. [Google Scholar] [CrossRef]
- Tanaka, S.; Honda, Y.; Takaku, S.; Koike, T.; Oe, S.; Hirahara, Y.; Yoshida, T.; Takizawa, N.; Takamori, Y.; Kurokawa, K.; et al. Involvement of PLAGL1/ZAC1 in hypocretin/orexin transcription. Int. J. Mol. Med. 2019, 43, 2164–2176. [Google Scholar] [CrossRef]
- Tanaka, S.; Kodama, T.; Nonaka, T.; Toyoda, H.; Arai, M.; Fukazawa, M.; Honda, Y.; Honda, M.; Mignot, E. Transcriptional regulation of the hypocretin/orexin gene by NR6A1. Biochem. Biophys. Res. Commun. 2010, 403, 178–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Terao, A.; Wisor, J.P.; Peyron, C.; Apte-Deshpande, A.; Wurts, S.W.; Edgar, D.M.; Kilduff, T.S. Gene expression in the rat brain during sleep deprivation and recovery sleep: An Affymetrix GeneChip study. Neuroscience 2006, 137, 593–605. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takizawa, N.; Tanaka, S.; Oe, S.; Koike, T.; Matsuda, T.; Yamada, H. Hypothalamohypophysial system in rats with autotransplantation of the adrenal cortex. Mol. Med. Rep. 2017, 15, 3215–3221. [Google Scholar] [CrossRef] [PubMed]
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Tanaka, S.; Honda, Y.; Sawachika, M.; Futani, K.; Yoshida, N.; Kodama, T. Degradation of STK16 via KCTD17 with Ubiquitin–Proteasome System in Relation to Sleep–Wake Cycle. Kinases Phosphatases 2023, 1, 14-22. https://doi.org/10.3390/kinasesphosphatases1010003
Tanaka S, Honda Y, Sawachika M, Futani K, Yoshida N, Kodama T. Degradation of STK16 via KCTD17 with Ubiquitin–Proteasome System in Relation to Sleep–Wake Cycle. Kinases and Phosphatases. 2023; 1(1):14-22. https://doi.org/10.3390/kinasesphosphatases1010003
Chicago/Turabian StyleTanaka, Susumu, Yoshiko Honda, Misa Sawachika, Kensuke Futani, Namika Yoshida, and Tohru Kodama. 2023. "Degradation of STK16 via KCTD17 with Ubiquitin–Proteasome System in Relation to Sleep–Wake Cycle" Kinases and Phosphatases 1, no. 1: 14-22. https://doi.org/10.3390/kinasesphosphatases1010003