Moa1与CENP-C和Rec8的相互作用及其在裂殖酵母减数分裂中的功能

doi:10.16288/j.yczz.24-035

[an error occurred while processing this directive]

Hereditas(Beijing) ›› 2024, Vol. 46 ›› Issue (8): 649-660.doi: 10.16288/j.yczz.24-035

• Research Article • Previous Articles Next Articles

Functional roles of the interaction of Moa1 with CENP-C and Rec8 in meiosis of Schizosaccharomyces pombe

Yu Min¹^,²(), Zihan Ni¹^,², Lingling Ma¹^,², Yoshinori Watanabe¹^,²()

1. Science Center for Future Foods, Jiangnan University, Wuxi 214122, China
2. School of Biotechnology, Jiangnan University, Wuxi 214122, China

Received:2024-03-08 Revised:2024-05-07 Online:2024-08-20 Published:2024-05-14
Contact: Yoshinori Watanabe E-mail:1401577396@qq.com;ywatanabe@jiangnan.edu.cn

Abstract

Abstract:

The localization of the meiotic specific regulatory molecule Moa1 to the centromere is regulated by the kinetochore protein CENP-C, and participates in the cohesion of sister chromatids in the centromere region mediated by the cohesin Rec8. To examine the interaction of these proteins, we analyzed the interactions between Moa1 and Rec8, CENP-C by yeast two-hybrid assays and identified several amino acid residues in Moa1 required for the interaction with CENP-C and Rec8. The results revealed that the interaction between Moa1 and CENP-C is crucial for the Moa1 to participate in the regulation of monopolar attachment of sister kinetochores. However, mutation at S143 and T150 of Moa1, which are required for interaction with Rec8 in the two-hybrid assay, did not show significant defects. Mutations in amino acid residues may not be sufficient to interfere with the interaction between Moa1 and Rec8 in vivo. Further research is needed to determine the interaction domain between Moa1 and Rec8. This study revealed specific amino acid sites at which Moa1 affects the meiotic homologous chromosome segregation, providing a deeper understanding of the mechanism of meiotic chromosome segregation.

Key words: meiosis, cohesin, kinetochore, mono-orientation

Yu Min, Zihan Ni, Lingling Ma, Yoshinori Watanabe. Functional roles of the interaction of Moa1 with CENP-C and Rec8 in meiosis of Schizosaccharomyces pombe[J]. Hereditas(Beijing), 2024, 46(8): 649-660.

Figures/Tables 6

Table 1

Fig. 1

Fig. 2

Fig. 3

Fig. 4

Fig. 5

References 49

[1]	Börner GV, Hochwagen A, Macqueen AJ. Meiosis in budding yeast. Genetics, 2023, 225(2): 1-33.
[2]	Hochwagen A. Meiosis. Curr Biol, 2008, 18(15): R641-R645.
[3]	Sakuno T, Watanabe Y. Studies of meiosis disclose distinct roles of cohesion in the core centromere and pericentromeric regions. Chromosome Res, 2009, 17(2): 239-249. doi: 10.1007/s10577-008-9013-y pmid: 19308704
[4]	Kagami A, Sakuno T, Yamagishi Y, Ishiguro T, Tsukahara T, Shirahige K, Tanaka K, Watanabe Y. Acetylation regulates monopolar attachment at multiple levels during meiosis I in fission yeast. EMBO Rep, 2011, 12(11): 1189-1195. doi: 10.1038/embor.2011.188 pmid: 21979813
[5]	Yokobayashi S, Watanabe Y. The kinetochore protein Moal enables cohesion-mediated monopolar attachment at meiosis I. Cell, 2005, 123(5): 803-817. pmid: 16325576
[6]	Lee BH, Kiburz BM, Amon A. Spo13 maintains centromeric cohesion and kinetochore coorientation during meiosis I. Curr Biol, 2004, 14(24): 2168-2182. pmid: 15620644
[7]	Kim J, Ishiguro K-I, Nambu A, Akiyoshi B, Yokobayashi S, Kagami A, Ishiguro T, Pendas AM, Takeda N, Sakakibara Y, Kitajima TS, Tanno Y, Sakuno T, Watanabe Y. Meikin is a conserved regulator of meiosis-I-specific kinetochore function. Nature, 2014, 517(7535): 466-471.
[8]	Hayashi T, Ebe M, Nagao K, Kokubu A, Sajiki K, Yanagida M. Schizosaccharomyces pombe centromere protein Mis19 links Mis16 and Mis18 to recruit CENP-A through interacting with NMD factors and the SWI/SNF complex. Genes Cells, 2014, 19(7): 541-554.
[9]	Earnshaw WC, Rothfield N. Identification of a family of human centromere proteins using autoimmune sera from patients with scleroderma. Chromosoma, 1985, 91(3-4): 313-321. doi: 10.1007/BF00328227 pmid: 2579778
[10]	She CW, Song YC. Advances in research of the structure and function of plant centromeres. Hereditas(Beijing), 2006, 28(12): 1597-1606.
	佘朝文, 宋运淳. 植物着丝粒结构和功能的研究进展. 遗传, 2006, 28(12): 1597-1606.
[11]	Przewloka MR, Venkei Z, Bolanos-Garcia VM, Debski J, Dadlez M, Glover DM. CENP-C is a structural platform for kinetochore assembly. Curr Biol, 2011, 21(5): 399-405. doi: 10.1016/j.cub.2011.02.005 pmid: 21353555
[12]	Hara M, Ariyoshi M, Sano T, Nozawa RS, Shinkai S, Onami S, Jansen I, Hirota T, Fukagawa T. Centromere/ kinetochore is assembled through CENP-C oligomerization. Mol Cell, 2023, 83(13): 2188-2205.e13.
[13]	Chik JK, Moiseeva V, Goel PK, Meinen BA, Koldewey P, An SJ, Mellone BG, Subramanian L, Cho US. Structures of CENP-C cupin domains at regional centromeres reveal unique patterns of dimerization and recruitment functions for the inner pocket. J Biol Chem, 2019, 294(38): 14119-14134.
[14]	Musacchio A, Desai A. A molecular view of kinetochore assembly and function. Biology (Basel), 2017, 6(1): 5.
[15]	Kwon M-S, Hori T, Okada M, Fukagawa T. CENP-C is involved in chromosome segregation, mitotic checkpoint function, and kinetochore assembly. Mol Biol Cell, 2007, 18(6): 2155-2168.
[16]	Fellmeth JE, Jang JK, Persaud M, Sturm H, Changela N, Parikh A, Mckim KS. A dynamic population of prophase CENP-C is required for meiotic chromosome segregation. PLoS Genet, 2023, 19(11): e1011066.
[17]	Heeger S, Leismann O, Schittenhelm R, Schraidt O, Heidmann S, Lehner CF. Genetic interactions of separase regulatory subunits reveal the diverged Drosophila Cenp-C homolog. Genes Dev, 2005, 19(17): 2041-2053.
[18]	Moore LL, Roth MB. Hcp-4, a Cenp-C-like protein in Caenorhabditis elegans, is required for resolution of sister centromeres. J Cell Biol, 2001, 153(6): 1199-1208. doi: 10.1083/jcb.153.6.1199 pmid: 11402064
[19]	Fellmeth JE, Mckim KS. Meiotic CENP-C is a shepherd: bridging the space between the centromere and the kinetochore in time and space. Essays Biochem, 2020, 64(2): 251-261. doi: 10.1042/EBC20190080 pmid: 32794572
[20]	Hillers KJ, Jantsch V, Martinez-Perez E, Yanowitz JL. Meiosis. WormBook, 2017, 2017: 1-43. doi: 10.1895/wormbook.1.178.1 pmid: 26694509
[21]	XU XY, Yanagida M. Cohesin organization, dynamics, and subdomain functions revealed by genetic suppressor screening. Proc Jpn Acad Ser B Phys Biol Sci, 2023, 99(3): 61-74.
[22]	Zhang N, Zhang J, Lin G. Advances in the study of DNA damage and repair in mammalian oocytes. Hereditas (Beijing), 2023, 45(5): 379-394.
	张楠, 张珏, 林戈. 哺乳动物卵母细胞的DNA损伤与修复研究进展. 遗传, 2023, 45(5): 379-394.
[23]	Kuru-Schors M, Haemmerle M, Gutschner T. The cohesin complex and its interplay with non-coding RNAs. Noncoding RNA, 2021, 7(4): 67.
[24]	Litwin I, Pilarczyk E, Wysocki R. The emerging role of cohesin in the DNA damage response. Genes (Basel), 2018, 9(12): 581.
[25]	Zhang Y, Fang YD. Progresses on the structure and function of cohesin. Hereditas (Beijing), 2020, 42(1): 57-72.
	张雨, 方玉达. Cohesin结构及功能研究进展. 遗传, 2020, 42(1): 57-72.
[26]	Yokobayashi S, Yamamoto M, Watanabe Y. Cohesins determine the attachment manner of kinetochores to spindle microtubules at meiosis I in fission yeast. Mol Cell Biol, 2003, 23(11): 3965-3973. doi: 10.1128/MCB.23.11.3965-3973.2003 pmid: 12748297
[27]	Rittenhouse NL, Dowen JM. Cohesin regulation and roles in chromosome structure and function. Curr Opin Genet Dev, 2024, 85: 102159.
[28]	Lu YJ, Zhou CY, Xiong B. Functional diversity of chromosome cohesion proteins. SCI SIN Vitae, 2022, 52(12): 1844-1857.
	卢亚娟, 周长银, 熊波. 染色体黏合蛋白功能的多样性. 中国科学:生命科学, 2022, 52(12): 1844-1857.
[29]	Minamino M, Higashi TL, Bouchoux C, Uhlmann F. Topological in vitro loading of the budding yeast cohesin ring onto DNA. Life Sci Alliance, 2018, 1(5): e201800143.
[30]	Kitajima TS, Miyazaki Y, Yamamoto M, Watanabe Y. Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. EMBO J, 2003, 22(20): 5643-5653. pmid: 14532136
[31]	Takahashi TS, Yiu PY, Chou MF, Gygi S, Walter JC. Recruitment of xenopus Scc2 and cohesin to chromatin requires the pre-replication complex. Nat Cell Biol, 2004, 6(10): 991-996. doi: 10.1038/ncb1177 pmid: 15448702
[32]	Parisi S, Mckay MJ, Molnar M, Thompson MA, van der Spek PJ, van Drunen-Schoenmaker E, Kanaar R, Lehmann E, Hoeijmakers JH, Kohli J. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol Cell Biol, 1999, 19(5): 3515-3528. doi: 10.1128/MCB.19.5.3515 pmid: 10207075
[33]	Kitajima TS, Kawashima SA, Watanabe Y. The conserved kinetochore protein shugoshin protects centromeric cohesion during meiosis. Nature, 2004, 427(6974): 510-517.
[34]	Watanabe Y, Nurse P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature, 1999, 400(6743): 461-464.
[35]	Miyazaki S, Kim J, Yamagishi Y, Ishiguro T, Okada Y, Tanno Y, Sakuno T, Watanabe Y. Meikin-associated polo-like kinase specifies Bub1 distribution in meiosis I. Genes Cells, 2017, 22(6): 552-567. doi: 10.1111/gtc.12496 pmid: 28497540
[36]	Tanaka K, Li Chang H, Kagami A, Watanabe Y. CENP-C functions as a scaffold for effectors with essential kinetochore functions in mitosis and meiosis. Dev Cell, 2009, 17(3): 334-343. doi: 10.1016/j.devcel.2009.08.004 pmid: 19758558
[37]	Ishiguro KI, Shimada R. MEIOSIN directs initiation of meiosis and subsequent meiotic prophase program during spermatogenesis. Genes Genet Syst, 2022, 97(1): 27-39.
[38]	Nimmo ER, Pidoux AL, Perry PE, Allshire RC. Defective meiosis in telomere-silencing mutants of Schizosaccharomyces pombe. Nature, 1998, 392(6678): 825-828.
[39]	Ding DQ, Haraguchi T, Hiraoka Y. Chromosomally- retained RNA mediates homologous pairing. Nucleus, 2012, 3(6): 516-519.
[40]	Menees TM, Ross-Macdonald PB, Roeder GS. mei4, a meiosis-specific yeast gene required for chromosome synapsis. Mol Cell Biol, 1992, 12(3): 1340-1351. doi: 10.1128/mcb.12.3.1340-1351.1992 pmid: 1545815
[41]	Kumar R, Bourbon HM, De Massy B. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev, 2010, 24(12): 1266-1280.
[42]	Zhou Z, Sang Q, Wang L. Physiological and pathological mechanisms of oocyte meiosis. Hereditas(Beijing), 2023, 45(12): 1087-1099. doi: 10.16288/j.yczz.23-170 pmid: 38764273
	周舟, 桑庆, 王磊. 人类卵母细胞减数分裂的生理和病理机制. 遗传, 2023, 45(12): 1087-1099.
[43]	Takahashi K, Murakami S, Chikashige Y, Funabiki H, Niwa O, Yanagida M. A low copy number central sequence with strict symmetry and unusual chromatin structure in fission yeast centromere. Mol Biol Cell, 1992, 3(7): 819-835. pmid: 1515677
[44]	Kimata Y, Kitamura K, Fenner N, Yamano H. Mes1 controls the meiosis I to meiosis II transition by distinctly regulating the anaphase-promoting complex/cyclosome coactivators Fzr1/Mfr1 and Slp1 in fission yeast. Mol Biol Cell, 2011, 22(9): 1486-1494. doi: 10.1091/mbc.E10-09-0774 pmid: 21389117
[45]	Izawa D, Goto M, Yamashita A, Yamano H, Yamamoto M. Fission yeast Mes1p ensures the onset of meiosis II by blocking degradation of cyclin Cdc13p. Nature, 2005, 434(7032): 529-533.
[46]	Ogushi S, Rattani A, Godwin J, Metson J, Schermelleh L, Nasmyth K. Loss of sister kinetochore co-orientation and peri-centromeric cohesin protection after meiosis I depends on cleavage of centromeric REC8. Dev Cell, 2021, 56(22): 3100-3114.e4. doi: 10.1016/j.devcel.2021.10.017 pmid: 34758289
[47]	Sakuno T, Hiraoka Y. Rec8 cohesin: a structural platform for shaping the meiotic chromosomes. Genes (Basel), 2022, 13(2). 200.
[48]	Ma W, Zhou JW, Chen J, Carr AM, Watanabe Y. Meikin synergizes with shugoshin to protect cohesin Rec8 during meiosis I. Genes Dev, 2021, 35(9-10): 692-697.
[49]	Mehta G, Anbalagan GK, Bharati AP, Gadre P, Ghosh SK. An interplay between Shugoshin and Spo13 for centromeric cohesin protection and sister kinetochore mono-orientation during meiosis I in Saccharomyces cerevisiae. Curr Genet, 2018, 64(5): 1141-1152.

Metrics

Comments

www.chinagene.cn
备案号：京ICP备09063187号

菌株名称	基因型
PW632	h⁺ pat1^-114 3pk-moa1
PW1	h⁺ pat1-114 natMX6-3pk-moa1
M1	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg
M2	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg
M3	h⁹⁰ mei4::hyg
PM11	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-S143K T150K
PM12	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-S143K T150K
PM21	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-S143D T150E
PM22	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-S143D T150E
PM31	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-E165K
PM32	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-E165K
PM41	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-D167K E168K
PM42	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-D167K E168K
PM51	h^- leu1 imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-I170K L171K
PM52	h⁺ mes1-B44 rec8-2A<<Kan rec12::hyg natMX6-3pk-moa1-I170K L171K
LM1	h^- leu1imr1L-GFP mes1-B44 rec8-2A<<Kan rec12::bsdr moa1::natr
LM2	h⁺ mes1-B44 rec8-2A<<Kan rec12::bsdr moa1::natr
PM-W	h⁹⁰ mei4::hyg natMX6-GFP-3pk-moa1
PM36	h⁹⁰ mei4::hyg natMX6-GFP-3pk-moa1-E165K
PM37	h⁹⁰ mei4::hyg natMX6-GFP-3pk-moa1-D167K E168K
PM38	h⁹⁰ mei4::hyg natMX6-GFP-3pk-moa1-I170K L171K

Functional roles of the interaction of Moa1 with CENP-C and Rec8 in meiosis of Schizosaccharomyces pombe

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 6

References 49

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	Zihan Ni, Yu Min, Lingling Ma, Yoshinori Watanabe. The effect of centromere protein Fta2 phosphorylation during meiosis [J]. Hereditas(Beijing), 2024, 46(7): 552-559.
[2]	Yan Jingliang, Ma Lingling, Watanabe Yoshinori. Ssu72 phosphatase deficiency leads to spindle crossing during the second meiotic division process [J]. Hereditas(Beijing), 2024, 46(6): 502-508.
[3]	Xiangjiang Lv, Jing Guo, Ge Lin. Novel mutations in TRIP13 lead to female infertility with oocyte maturation arrest [J]. Hereditas(Beijing), 2023, 45(6): 514-525.
[4]	Zhou Zhou, Qing Sang, Lei Wang. Physiological and pathological mechanisms of oocyte meiosis [J]. Hereditas(Beijing), 2023, 45(12): 1087-1099.
[5]	Yuxuan Guo, Shunping Yan, Yingxiang Wang. Recent advances in functional conservation and divergence of recombinase RAD51 and DMC1 [J]. Hereditas(Beijing), 2022, 44(5): 398-413.
[6]	Yuanyuan Li, Lei Guo, Zhiming Han. Roles of NEK family in cell cycle regulation [J]. Hereditas(Beijing), 2021, 43(7): 642-653.
[7]	Hui Nie, Yiwen Zhang, Jianing Li, Nannan Wang, Lan Xu. Progress on the correlation between the abnormal synaptonemal complex and infertility [J]. Hereditas(Beijing), 2021, 43(12): 1142-1148.
[8]	Na Wang, Zhilian Jia, Qiang Wu. RFX5 regulates gene expression of the Pcdhα cluster [J]. Hereditas(Beijing), 2020, 42(8): 760-774.
[9]	Yu Zhang, Yuda Fang. Progresses on the structure and function of cohesin [J]. Hereditas(Beijing), 2020, 42(1): 57-72.
[10]	Fan Li, Rongpei Yu, Dan Sun, Jihua Wang, Shenchong Li, Jiwei Ruan, Qinli Shan, Pingli Lu, Guoxian Wang. Molecular mechanisms of meiotic recombination suppression in plants [J]. Hereditas(Beijing), 2019, 41(1): 52-65.
[11]	Yaping Liao,Chunjing Wang,Meng Liang,Xiaomei Hu,Qi Wu. Analysis of genetic characteristics and reproductive risks of balanced complex chromosome rearrangement carriers in China [J]. Hereditas(Beijing), 2017, 39(5): 396-412.
[12]	Yanan Zhai, Quan Xu, Ya Guo, Qiang Wu. Characterization of a cluster of CTCF-binding sites in a protocadherin regulatory region [J]. HEREDITAS(Beijing), 2016, 38(4): 323-336.
[13]	Shanshan Yue,Laixin Xia. Identification of C(2)M interacting proteins by yeast two-hybrid screening [J]. HEREDITAS(Beijing), 2015, 37(11): 1160-1166.
[14]	ZHANG Bao-Le GAO Dian-Shuai XU Yin-Xue. G protein-coupled receptor 3: a key factor in the regulation of the nervous system and follicle development [J]. HEREDITAS, 2013, 35(5): 578-586.
[15]	XIE Wen-Jun, SHI Dian-Yi, CAI Ze-Xi, CHEN Xiao-Yang, JIN Wei-Wei. Organization, function and genetic controlling of synaptonemal complex [J]. HEREDITAS, 2012, 34(2): 167-176.