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Protein & Peptide Letters

Editor-in-Chief

ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

Research Article

The Proteins Interacting with Prmt5 in Medaka (Oryzias latipes) Identified by Yeast Two-Hybridization

Author(s): Hao Shen, Xiaosha Zhang, Md. Abdullah Al Hafiz, Xiaoting Liang, Qiting Yao, Maomao Guo, Gongyu Xu, Xueping Zhong, Qingchun Zhou and Haobin Zhao*

Volume 27, Issue 10, 2020

Page: [971 - 978] Pages: 8

DOI: 10.2174/0929866527666200505213431

Price: $65

Abstract

Background: Prmt5 plays major role in regulation of gene expression, RNA processing, cell growth and differentiation, signal transduction, germ cell development, etc., in mammals. Prmt5 is also related to cancer. Knowing the proteins interacting with Prmt5 is important to understand Prmt5’s function in cells. Although there have been reports on proteins binding with Prmt5 in mammals, the partner proteins of Prmt5 in fish are still unclear.

Objectives: The objective was to obtain proteins that bind with Prmt5 in medaka, a model fish.

Methods: Yeast two hybridization was adopted to achieve the objective. Medaka Prmt5 was used as a bait to fish the prey, binding proteins in a cDNA library of medaka. Co-immunoprecipitation and in silicon analysis were performed to study the interaction of medaka Mep50 and Prmt5.

Results: Eight proteins were identified to bind with Prmt5 from 69 preliminary positive colonies. The binding proteins are methylosome protein 50 (Mep50), apolipoprotein A-I-like (Apo-AI), PR domain containing protein 1a with zinc fingers (Prdm1a), Prdm1b, T-cell immunoglobulin mucin family member 3 (Tim-3), phosphoribosylaminoimidazole carboxylase and phosphoribosylaminoimidazolesuccinocarboxamide synthase (Paics), NADH dehydrogenase subunit 4 (ND4) and sciellin (Scl). Co-immunoprecipitation confirmed the interaction of medaka Prmt5 and Mep50. Predicted structures of medaka Prtm5 and Mep50 are similar to that of human PRMT5 and MEP50.

Conclusion: Medaka Mep50, Prdm1a, Prdm1b, Apo-AI, Tim-3, Paics, ND4, and Scl bind with Prmt5.

Keywords: Prmt5, Mep50, Apo-AI, Prdm1a, Prdm1b, Tim-3, Paics, ND4, Scl, yeast two-hybridization, cDNA library, protein interaction, co-immunoprecipitation, modelling, medaka.

Graphical Abstract

[1]
Boisvert, F.M.; Côté, J.; Boulanger, M.C.; Richard, S. A proteomic analysis of arginine-methylated protein complexes. Mol. Cell. Proteomics, 2003, 2(12), 1319-1330.
[http://dx.doi.org/10.1074/mcp.M300088-MCP200] [PMID: 14534352]
[2]
Bedford, M.T.; Clarke, S.G. Protein arginine methylation in mammals: Who, what, and why. Mol. Cell, 2009, 33(1), 1-13.
[http://dx.doi.org/10.1016/j.molcel.2008.12.013] [PMID: 19150423]
[3]
Minarovits, J.; Banati, F.; Szenthe, K.; Niller, H.H. Epigenetic regulation. Patho-Epigenetics of Infectious Disease. In: Advances in Experimental Medicine and Biology; Minarovits, J.; Niller, H., Eds.; Springer: Cham, 2016; Vol. 879, pp. 1-25.
[http://dx.doi.org/10.1007/978-3-319-24738-0_1]
[4]
Krause, C.D.; Yang, Z.H.; Kim, Y.S.; Lee, J.H.; Cook, J.R.; Pestka, S. Protein arginine methyltransferases: Evolution and assessment of their pharmacological and therapeutic potential. Pharmacol. Ther., 2007, 113(1), 50-87.
[http://dx.doi.org/10.1016/j.pharmthera.2006.06.007] [PMID: 17005254]
[5]
Stopa, N.; Krebs, J.E.; Shechter, D. The PRMT5 arginine methyltransferase: Many roles in development, cancer and beyond. Cell. Mol. Life Sci., 2015, 72(11), 2041-2059.
[http://dx.doi.org/10.1007/s00018-015-1847-9] [PMID: 25662273]
[6]
Yang, M.; Sun, J.; Sun, X.; Shen, Q.; Gao, Z.; Yang, C. Caenorhabditis elegans protein arginine methyltransferase PRMT-5 negatively regulates DNA damage-induced apoptosis. PLoS Genet., 2009, 5(6), e1000514.
[http://dx.doi.org/10.1371/journal.pgen.1000514] [PMID: 19521535]
[7]
Boulanger, M.C.; Miranda, T.B.; Clarke, S.; Di Fruscio, M.; Suter, B.; Lasko, P.; Richard, S. Characterization of the Drosophila protein arginine methyltransferases DART1 and DART4. Biochem. J., 2004, 379(Pt 2), 283-289.
[http://dx.doi.org/10.1042/bj20031176] [PMID: 14705965]
[8]
Chen, W.; Cao, M.; Yang, Y.; Nagahama, Y.; Zhao, H. Expression pattern of prmt5 in adult fish and embryos of medaka, Oryzias latipes. Fish Physiol. Biochem., 2009, 35(3), 325-332.
[http://dx.doi.org/10.1007/s10695-008-9233-2] [PMID: 19578939]
[9]
Hung, C.M.; Li, C. Identification and phylogenetic analyses of the protein arginine methyltransferase gene family in fish and ascidians. Gene, 2004, 340(2), 179-187.
[http://dx.doi.org/10.1016/j.gene.2004.07.039] [PMID: 15475159]
[10]
Pal, S.; Baiocchi, R.A.; Byrd, J.C.; Grever, M.R.; Jacob, S.T.; Sif, S. Low levels of miR-92b/96 induce PRMT5 translation and H3R8/H4R3 methylation in mantle cell lymphoma. EMBO J., 2007, 26(15), 3558-3569.
[http://dx.doi.org/10.1038/sj.emboj.7601794] [PMID: 17627275]
[11]
Zhao, Q.; Rank, G.; Tan, Y.T.; Li, H.; Moritz, R.L.; Simpson, R.J.; Cerruti, L.; Curtis, D.J.; Patel, D.J.; Allis, C.D.; Cunningham, J.M.; Jane, S.M. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat. Struct. Mol. Biol., 2009, 16(3), 304-311.
[http://dx.doi.org/10.1038/nsmb.1568] [PMID: 19234465]
[12]
Boisvert, F.M.; Cote, J.; Boulanger, M.C.; Cleroux, P.; Bachand, F.; Autexier, C.; Richard, S. Symmetrical dimethylarginine methylation is required for the localization of SMN in Cajal bodies and pre-mRNA splicing. J. Cell Biol., 2002, 159(6), 957-969.
[http://dx.doi.org/10.1083/jcb.200207028] [PMID: 12486110]
[13]
Scoumanne, A.; Zhang, J.; Chen, X. PRMT5 is required for cell-cycle progression and p53 tumor suppressor function. Nucleic Acids Res., 2009, 37(15), 4965-4976.
[http://dx.doi.org/10.1093/nar/gkp516] [PMID: 19528079]
[14]
Tee, W.W.; Pardo, M.; Theunissen, T.W.; Yu, L.; Choudhary, J.S.; Hajkova, P.; Surani, M.A. Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev., 2010, 24(24), 2772-2777.
[http://dx.doi.org/10.1101/gad.606110] [PMID: 21159818]
[15]
Ancelin, K.; Lange, U.C.; Hajkova, P.; Schneider, R.; Bannister, A.J.; Kouzarides, T.; Surani, M.A. Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells. Nat. Cell Biol., 2006, 8(6), 623-630.
[http://dx.doi.org/10.1038/ncb1413] [PMID: 16699504]
[16]
Zhu, J.; Zhang, D.; Liu, X.; Yu, G.; Cai, X.; Xu, C.; Rong, F.; Ouyang, G.; Wang, J.; Xiao, W. Zebrafish prmt5 arginine methyltransferase is essential for germ cell development. Development, 2019, 146(20), dev179572.
[http://dx.doi.org/10.1242/dev.179572] [PMID: 31533925]
[17]
Dacwag, C.S.; Ohkawa, Y.; Pal, S.; Sif, S.; Imbalzano, A.N. The protein arginine methyltransferase Prmt5 is required for myogenesis because it facilitates ATP-dependent chromatin remodeling. Mol. Cell. Biol., 2007, 27(1), 384-394.
[http://dx.doi.org/10.1128/MCB.01528-06] [PMID: 17043109]
[18]
Richard, S.; Morel, M.; Cléroux, P. Arginine methylation regulates IL-2 gene expression: A role for protein arginine methyltransferase 5 (PRMT5). Biochem. J., 2005, 388(Pt 1), 379-386.
[http://dx.doi.org/10.1042/BJ20040373] [PMID: 15654770]
[19]
Wei, H.; Wang, B.; Miyagi, M.; She, Y.; Gopalan, B.; Huang, D.B.; Ghosh, G.; Stark, G.R.; Lu, T. PRMT5 dimethylates R30 of the p65 subunit to activate NF-κB. Proc. Natl. Acad. Sci. USA, 2013, 110(33), 13516-13521.
[http://dx.doi.org/10.1073/pnas.1311784110] [PMID: 23904475]
[20]
Nicholas, C.; Yang, J.; Peters, S.B.; Bill, M.A.; Baiocchi, R.A.; Yan, F.; Sïf, S.; Tae, S.; Gaudio, E.; Wu, X.; Grever, M.R.; Young, G.S.; Lesinski, G.B. PRMT5 is upregulated in malignant and metastatic melanoma and regulates expression of MITF and p27(Kip1.). PLoS One, 2013, 8(9), e74710.
[http://dx.doi.org/10.1371/journal.pone.0074710] [PMID: 24098663]
[21]
Antonysamy, S.; Bonday, Z.; Campbell, R.M.; Doyle, B.; Druzina, Z.; Gheyi, T.; Han, B.; Jungheim, L.N.; Qian, Y.; Rauch, C.; Russell, M.; Sauder, J.M.; Wasserman, S.R.; Weichert, K.; Willard, F.S.; Zhang, A.; Emtage, S. Crystal structure of the human PRMT5:MEP50 complex. Proc. Natl. Acad. Sci. USA, 2012, 109(44), 17960-17965.
[http://dx.doi.org/10.1073/pnas.1209814109] [PMID: 23071334]
[22]
Ho, M.C.; Wilczek, C.; Bonanno, J.B.; Xing, L.; Seznec, J.; Matsui, T.; Carter, L.G.; Onikubo, T.; Kumar, P.R.; Chan, M.K.; Brenowitz, M.; Cheng, R.H.; Reimer, U.; Almo, S.C.; Shechter, D. Structure of the arginine methyltransferase PRMT5-MEP50 reveals a mechanism for substrate specificity. PLoS One, 2013, 8(2), e57008.
[http://dx.doi.org/10.1371/journal.pone.0057008] [PMID: 23451136]
[23]
Cheng, N.; Guo, M.; Chang, P.; Zhang, X.; Zhang, R.; Qi, C.; Zhong, X.; Zhou, Q.; Zhao, H. Expression of mep50 in adult and embryos of medaka fish (Oryzias latipes). Fish Physiol. Biochem., 2016, 42(3), 1053-1061.
[http://dx.doi.org/10.1007/s10695-016-0196-4] [PMID: 26749004]
[24]
Pal, S.; Yun, R.; Datta, A.; Lacomis, L.; Erdjument-Bromage, H.; Kumar, J.; Tempst, P.; Sif, S. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell. Biol., 2003, 23(21), 7475-7487.
[http://dx.doi.org/10.1128/MCB.23.21.7475-7487.2003] [PMID: 14559996]
[25]
Brahms, H.; Meheus, L.; de Brabandere, V.; Fischer, U.; Lührmann, R. Symmetrical dimethylation of arginine residues in spliceosomal Sm protein B/B′ and the Sm-like protein LSm4, and their interaction with the SMN protein. RNA, 2001, 7(11), 1531-1542.
[http://dx.doi.org/10.1017/S135583820101442X] [PMID: 11720283]
[26]
Lacroix, M.; El Messaoudi, S.; Rodier, G.; Le Cam, A.; Sardet, C.; Fabbrizio, E. The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep., 2008, 9(5), 452-458.
[http://dx.doi.org/10.1038/embor.2008.45] [PMID: 18404153]
[27]
Guderian, G.; Peter, C.; Wiesner, J.; Sickmann, A.; Schulze-Osthoff, K.; Fischer, U.; Grimmler, M. RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J. Biol. Chem., 2011, 286(3), 1976-1986.
[http://dx.doi.org/10.1074/jbc.M110.148486] [PMID: 21081503]
[28]
Gurung, B.; Feng, Z.; Iwamoto, D.V.; Thiel, A.; Jin, G.; Fan, C.M.; Ng, J.M.; Curran, T.; Hua, X. Menin epigenetically represses Hedgehog signaling in MEN1 tumor syndrome. Cancer Res., 2013, 73(8), 2650-2658.
[http://dx.doi.org/10.1158/0008-5472.CAN-12-3158] [PMID: 23580576]
[29]
Nibona, E.; Xu, G.; Wu, K.; Shen, H.; Zhang, R.; Ke, X.; Al Hafiz, A.; Wang, Z.; Qi, C.; Zhao, H. Identification, characterization, expression profiles of OlHavcr2 in medaka (Oryzias latipes). Gen. Comp. Endocrinol., 2019, 277, 30-37.
[http://dx.doi.org/10.1016/j.ygcen.2018.10.023] [PMID: 30395804]
[30]
Furuno, K.; Masatsugu, T.; Sonoda, M.; Sasazuki, T.; Yamamoto, K. Association of Polycomb group SUZ12 with WD-repeat protein MEP50 that binds to histone H2A selectively in vitro. Biochem. Biophys. Res. Commun., 2006, 345(3), 1051-1058.
[http://dx.doi.org/10.1016/j.bbrc.2006.05.014] [PMID: 16712789]
[31]
Sun, L.; Wang, M.; Lv, Z.; Yang, N.; Liu, Y.; Bao, S.; Gong, W.; Xu, R.M. Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc. Natl. Acad. Sci. USA, 2011, 108(51), 20538-20543.
[http://dx.doi.org/10.1073/pnas.1106946108] [PMID: 22143770]
[32]
Zhao, H.; Zhang, X.; Cheng, N.; Duan, J.; Wang, J.; Nagahama, Y.; Zhong, X.; Zhou, Q.; Wang, Y. Identification and expression profiles of prdm1 in medaka Oryzias latipes. Mol. Biol. Rep., 2014, 41(2), 617-626.
[http://dx.doi.org/10.1007/s11033-013-2899-2] [PMID: 24343424]
[33]
John, S.A.; Garrett-Sinha, L.A. Blimp1: A conserved transcriptional repressor critical for differentiation of many tissues. Exp. Cell Res., 2009, 315(7), 1077-1084.
[http://dx.doi.org/10.1016/j.yexcr.2008.11.015] [PMID: 19073176]
[34]
Gyory, I.; Wu, J.; Fejér, G.; Seto, E.; Wright, K.L. PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat. Immunol., 2004, 5(3), 299-308.
[http://dx.doi.org/10.1038/ni1046] [PMID: 14985713]
[35]
Eckert, D.; Biermann, K.; Nettersheim, D.; Gillis, A.J.; Steger, K.; Jäck, H.M.; Müller, A.M.; Looijenga, L.H.; Schorle, H. Expression of BLIMP1/PRMT5 and concurrent histone H2A/H4 arginine 3 dimethylation in fetal germ cells, CIS/IGCNU and germ cell tumors. BMC Dev. Biol., 2008, 8, 106.
[http://dx.doi.org/10.1186/1471-213X-8-106] [PMID: 18992153]
[36]
Arciello, A.; Piccoli, R.; Monti, D.M. Apolipoprotein A-I: The dual face of a protein. FEBS Lett., 2016, 590(23), 4171-4179.
[http://dx.doi.org/10.1002/1873-3468.12468] [PMID: 27790714]
[37]
Llewellyn, L.; Ramsurn, V.P.; Wigham, T.; Sweeney, G.E.; Power, D.M. Cloning, characterisation and expression of the apolipoprotein A-I gene in the sea bream (Sparus aurata). Biochim. Biophys. Acta, 1998, 1442(2-3), 399-404.
[http://dx.doi.org/10.1016/S0167-4781(98)00171-7] [PMID: 9804999]
[38]
Villarroel, F.; Bastías, A.; Casado, A.; Amthauer, R.; Concha, M.I. Apolipoprotein A-I, an antimicrobial protein in Oncorhynchus mykiss: Evaluation of its expression in primary defence barriers and plasma levels in sick and healthy fish. Fish Shellfish Immunol., 2007, 23(1), 197-209.
[http://dx.doi.org/10.1016/j.fsi.2006.10.008] [PMID: 17391986]
[39]
Harel, A.; Fainaru, M.; Shafer, Z.; Hernandez, M.; Cohen, A.; Schwartz, M. Optic nerve regeneration in adult fish and apolipoprotein A-I. J. Neurochem., 1989, 52(4), 1218-1228.
[http://dx.doi.org/10.1111/j.1471-4159.1989.tb01869.x] [PMID: 2494299]
[40]
Henikoff, S.; Nash, D.; Hards, R.; Bleskan, J.; Woolford, J.F.; Naguib, F.; Patterson, D. Two Drosophila melanogaster mutations block successive steps of de novo purine synthesis. Proc. Natl. Acad. Sci. USA, 1986, 83(11), 3919-3923.
[http://dx.doi.org/10.1073/pnas.83.11.3919] [PMID: 3086869]
[41]
Holland, C.; Lipsett, D.B.; Clark, D.V. A link between impaired purine nucleotide synthesis and apoptosis in Drosophila melanogaster. Genetics, 2011, 188(2), 359-367.
[http://dx.doi.org/10.1534/genetics.110.124222] [PMID: 21441212]
[42]
Wallace, D.C.; Singh, G.; Lott, M.T.; Hodge, J.A.; Schurr, T.G.; Lezza, A.M.; Elsas, L.J., II; Nikoskelainen, E.K. Mitochondrial DNA mutation associated with Leber’s hereditary optic neuropathy. Science, 1988, 242(4884), 1427-1430.
[http://dx.doi.org/10.1126/science.3201231] [PMID: 3201231]
[43]
Champliaud, M.F.; Burgeson, R.E.; Jin, W.; Baden, H.P.; Olson, P.F. cDNA cloning and characterization of sciellin, a LIM domain protein of the keratinocyte cornified envelope. J. Biol. Chem., 1998, 273(47), 31547-31554.
[http://dx.doi.org/10.1074/jbc.273.47.31547] [PMID: 9813070]
[44]
Corona, W.; Karkera, D.J.; Patterson, R.H.; Saini, N.; Trachiotis, G.D.; Korman, L.Y.; Liu, B.; Alexander, E.P.; De la Pena, A.S.; Marcelo, A.B.; Wadleigh, R. Analysis of Sciellin (SCEL) as a candidate gene in esophageal squamous cell carcinoma. Anticancer Res., 2004, 24(3a), 1417-1419.
[PMID: 15274303]
[45]
Chou, C.K.; Fan, C.C.; Lin, P.S.; Liao, P.Y.; Tung, J.C.; Hsieh, C.H.; Hung, M.C.; Chen, C.H.; Chang, W.C. Sciellin mediates mesenchymal-to-epithelial transition in colorectal cancer hepatic metastasis. Oncotarget, 2016, 7(18), 25742-25754.
[http://dx.doi.org/10.18632/oncotarget.8264] [PMID: 27013588]
[46]
Lee, J.; Phong, B.; Egloff, A.M.; Kane, L.P. TIM polymorphisms-genetics and function. Genes Immun., 2011, 12(8), 595-604.
[http://dx.doi.org/10.1038/gene.2011.75] [PMID: 22048452]
[47]
Cheng, L.; Ruan, Z. Tim-3 and Tim-4 as the potential targets for antitumor therapy. Hum. Vaccin. Immunother., 2015, 11(10), 2458-2462.
[http://dx.doi.org/10.1080/21645515.2015.1056953] [PMID: 26211834]

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