[an error occurred while processing this directive]
Review

Research progress of proteins related to sperm tail development

Expand
  • Department of Histology and Embryology, School of Medicine, Yangzhou University, Yangzhou 225001, China

Received date: 2019-12-25

  Revised date: 2020-04-02

  Online published: 2020-05-07

Supported by

Supported by the National Natural Science Foundation of China No(81871205);the Natural Science Foundation of Jiangsu Province No(BK20131230)

Abstract

The structure of sperm tail is closely related to its motor function, which directly determines whether the sperm can be normally transported to fallopian tube and fertilize the ovum. The formation and development of sperm tail is a very complex process, which is finely regulated by various kinds of proteins. Research finds that defects of various sperm tail development related proteins can lead to oligospermia, asthenozoospermia and teratospermia. Based on the ultrastructure of sperm tail, we summarize the recent research progress of the proteins related to sperm tail development, thereby providing the theoretical basis and practical possibility for the diagnosis and treatment of male infertility.

Cite this article

Yanan Zhong, Changmin Niu, Mengmeng Xia, Ying Zheng . Research progress of proteins related to sperm tail development[J]. Hereditas(Beijing), 2020 , 42(6) : 524 -535 . DOI: 10.16288/j.yczz.19-309

References

[1] Eddy EM . The scaffold role of the fibrous sheath. Soc Reprod Fertil Suppl, 2007,65:45-62.
[2] Toure A, Rode B, Hunnicutt GR, Escalier D, Gacon G . Septins at the annulus of mammalian sperm. Biol Chem, 2011,392(8-9):799-803.
[3] Kissel H, Georgescu MM, Larisch S, Manova K, Hunnicutt GR, Steller H . The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell, 2005,8(3):353-364.
[4] Lin YH, Lin YM, Wang YY, Yu IS, Lin YW, Wang YH, Wu CM, Pan HA, Chao SC, Yen PH, Lin SW, Kuo PL . The expression level of septin12 is critical for spermiogenesis. Am J Pathol, 2009,174(5):1857-1868.
[5] Yassine S, Escoffier J, Abi Nahed R, Pierre V, Karaouzene T, Ray PF, Arnoult C . Dynamics of Sun5 localization during spermatogenesis in wild type and Dpy19l2 knock-out mice indicates that Sun5 is not involved in acrosome attachment to the nuclear envelope. PLoS One, 2015,10(3):e0118698.
[6] Shang YL, Zhu FX, Wang LN, Ouyang YC, Dong MZ, Liu C, Zhao HC, Cui XH, Ma DY, Zhang ZG, Yang XY, Guo YS, Liu F, Yuan L, Gao F, Guo XJ, Sun QY, Cao YX, Li W . Essential role for SUN5 in anchoring sperm head to the tail. eLife, 2017,6:e28199.
[7] Tokuhiro K, Isotani A, Yokota S, Yano Y, Oshio S, Hirose M, Wada M, Fujita K, Ogawa Y, Okabe M, Nishimune Y, Tanaka H . OAZ-t/OAZ3 is essential for rigid connection of sperm tails to heads in mouse. PLoS Genet, 2009,5(11):e1000712.
[8] Yuan SQ, Stratton CJ, Bao JQ, Zheng HL, Bhetwal BP, Yanagimachi R, Yan W . Spata6 is required for normal assembly of the sperm connecting piece and tight head-tail conjunction. Proc Natl Acad Sci USA, 2015,112(5):E430-E439.
[9] Baek N, Woo JM, Han C, Choi E, Park I, Kim DH, Eddy EM, Cho C . Characterization of eight novel proteins with male germ cell-specific expression in mouse. Reprod Biol Endocrinol, 2008,6:32.
[10] Kim J, Kwon JT, Jeong J, Kim J, Hong SH, Kim J, Park ZY, Chung KH, Eddy EM, Cho C . SPATC1L maintains the integrity of the sperm head-tail junction. EMBO Rep, 2018,19(9):e45991.
[11] Hussain MS, Baig SM, Neumann S, Nurnberg G, Farooq M, Ahmad I, Alef T, Hennies HC, Technau M, Altmuller J, Frommolt P, Thiele H, Noegel AA, Nurnberg P . A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am J Hum Genet, 2012,90(5):871-878.
[12] Sha YW, Xu XH, Mei LB, Li P, Su ZY, He XQ, Li L . A homozygous CEP135 mutation is associated with multiple morphological abnormalities of the sperm flagella (MMAF). Gene, 2017,633:48-53.
[13] Sha YW, Wang X, Xu X, Su ZY, Cui Y, Mei LB, Huang XJ, Chen J, He XM, Ji ZY, Bao H, Yang X, Li P, Li L . Novel mutations in CFAP44 and CFAP43 cause multiple morphological abnormalities of the sperm flagella (MMAF). Reprod Sci, 2019,26(1):26-34.
[14] Lehti MS, Sironen A . Formation and function of the manchette and flagellum during spermatogenesis. Reproduction, 2016,151(4):R43-R54.
[15] Martins LR, Bung RK, Koch S, Richter K, Schwarzmüller L, Terhardt D, Kurtulmus B, Niehrs C, Rouhi A, Lohmann I, Pereira G, Frohling S, Glimm H, Scholl C . Stk33 is required for spermatid differentiation and male fertility in mice. Dev Biol, 2018,433(1):84-93.
[16] Rosenbaum JL, Witman GB . Intraflagellar transport. Nat Rev Mol Cell Biol, 2002,3(11):813-25.
[17] Lehti MS, Kotaja N, Sironen A . KIF3A is essential for sperm tail formation and manchette function. Mol Cell Endocrinol, 2013,377(1-2):44-55.
[18] Okuda H, DeBoer K, O'Connor AE, Merriner DJ, Jamsai D, O'Bryan MK. LRGUK1 is part of a multiprotein complex required for manchette function and male fertility. FASEB J, 2017,31(3):1141-1152.
[19] Kuo PL, Chiang HS, Wang YY, Kuo YC, Chen MF, Yu IS, Teng YN, Lin SW, Lin YH . SEPT12-microtubule complexes are required for sperm head and tail formation. Int J Mol Sci, 2013,14(11):22102-22116.
[20] Zhang Z, Shen X, Gude DR, Wilkinson BM, Justice MJ, Flickinger CJ, Herr JC, Eddy EM, Strauss JF . MEIG1 is essential for spermiogenesis in mice. Proc Natl Acad Sci USA, 2009,106(40):17055-17060.
[21] Dong FN, Amiri-Yekta A, Martinez G, Saut A, Tek J, Stouvenel L, Lores P, Karaouzene T, Thierry-Mieg N, Satre V, Brouillet S, Daneshipour A, Hosseini SH, Bonhivers M, Gourabi H, Dulioust E, Arnoult C, Toure A, Ray PF, Zhao H, Coutton C . Absence of CFAP69 causes male infertility due to multiple morphological abnormalities of the flagella in human and mouse. Am J Hum Genet, 2018,102(4):636-648.
[22] Liu CY, Lv MR, He XJ, Zhu Y, Amiri-Yekta A, Li WY, Wu H, Kherraf ZE, Liu WJ, Zhang JJ, Tan Q, Tang SY, Zhu YJ, Zhong YD, Li CH, Tian SX, Zhang ZG, Jin L, Ray P, Zhang F, Cao YX . Homozygous mutations in SPEF2 induce multiple morphological abnormalities of the sperm flagella and male infertility. J Med Genet, 2020,57(1):31-37.
[23] Sironen A, Hansen J, Thomsen B, Andersson M, Vilkki J, Toppari J, Kotaja N . Expression of SPEF2 during mouse spermatogenesis and identification of IFT20 as an interacting protein. Biol Reprod, 2010,82(3):580-590.
[24] Coutton C, Martinez G, Kherraf ZE, Amiri-Yekta A, Boguenet M, Saut A, He X, Zhang F, Cristou-Kent M, Escoffier J, Bidart M, Satre V, Conne B, Fourati Ben Mustapha S, Halouani L, Marrakchi O, Makni M, Latrous H, Kharouf M, Pernet-Gallay K, Bonhivers M, Hennebicq S, Rives N, Dulioust E, Toure A, Gourabi H, Cao Y, Zouari R, Hosseini SH, Nef S, Thierry-Mieg N, Arnoult C, Ray PF . Bi-allelic mutations in ARMC2 lead to severe astheno-teratozoospermia due to sperm flagellum malformations in humans and mice. Am J Hum Genet, 2019,104(2):331-340.
[25] Teves ME, Nagarkatti-Gude DR, Zhang Z, Strauss JF . Mammalian axoneme central pair complex proteins: Broader roles revealed by gene knockout phenotypes. Cytoskeleton (Hoboken), 2016,73(1):3-22.
[26] Bower R, Tritschler D, Vanderwaal K, Perrone CA, Mueller J, Fox L, Sale WS, Porter ME . The N-DRC forms a conserved biochemical complex that maintains outer doublet alignment and limits microtubule sliding in motile axonemes. Mol Biol Cell, 2013,24(8):1134-1152.
[27] Castaneda JM, Hua R, Miyata H, Oji A, Guo YS, Cheng YW, Zhou T, Guo XJ, Cui YQ, Shen B, Wang ZB, Hu ZB, Zhou ZM, Sha JH, Prunskaite-Hyyrylainen R, Yu ZF, Ramirez-Solis R, Ikawa M, Matzuk MM, Liu MX . TCTE1 is a conserved component of the dynein regulatory complex and is required for motility and metabolism in mouse spermatozoa. Proc Natl Acad Sci USA, 2017,114(27):E5370-E5378.
[28] Abbasi F, Miyata H, Shimada K, Morohoshi A, Nozawa K, Matsumura T, Xu Z, Pratiwi P, Ikawa M . RSPH6A is required for sperm flagellum formation and male fertility in mice. J Cell Sci, 2018,131(19).
[29] Kott E, Legendre M, Copin B, Papon JF, Dastot-Le Moal F, Montantin G, Duquesnoy P, Piterboth W, Amram D, Bassinet L, Beucher J, Beydon N, Deneuville E, Houdouin V, Journel H, Just J, Nathan N, Tamalet A, Collot N, Jeanson L, Le Gouez M, Vallette B, Vojtek AM, Epaud R, Coste A, Clement A, Housset B, Louis B, Escudier E, Amselem S. Loss-of-function mutations in RSPH1 cause primary ciliary dyskinesia with central-complex and radial- spoke defects. Am J Hum Genet, 2013,93(3):561-570.
[30] Ben Khelifa M, Coutton C, Zouari R, Karaouzène T, Rendu J, Bidart M, Yassine S, Pierre V, Delaroche J, Hennebicq S, Grunwald D, Escalier D, Pernet-Gallay K, Jouk PS, Thierry-Mieg N, Touré A, Arnoult C, Ray PF . Mutations in DNAH1, which encodes an inner arm heavy chain dynein, lead to male infertility from multiple morphological abnormalities of the sperm flagella. Am J Hum Genet, 2014,94(1):95-104.
[31] Li Y, Sha YW, Wang X, Ding L, Liu WS, Ji ZY, Mei LB, Huang XJ, Lin SB, Kong SB, Lu JH, Qin WB, Zhang XZ, Zhuang JM, Tang YG, Lu ZX . DNAH2 is a novel candidate gene associated with multiple morphological abnormalities of the sperm flagella. Clin Genet, 2019,95(5):590-600.
[32] H?ben IM, Hjeij R, Olbrich H, Dougherty GW, Nothe- Menchen T, Aprea I, Frank D, Pennekamp P, Dworniczak B, Wallmeier J, Raidt J, Nielsen KG, Philipsen MC, Santamaria F, Venditto L, Amirav I, Mussaffi H, Prenzel F, Wu K, Bakey Z, Schmidts M, Loges NT, Omran H . Mutations in C11orf70 cause primary ciliary dyskinesia with randomization of Left/Right body asymmetry due to defects of outer and inner dynein arms. Am J Hum Genet, 2018,102(5):973-984.
[33] Dong F, Shinohara K, Botilde Y, Nabeshima R, Asai Y, Fukumoto A, Hasegawa T, Matsuo M, Takeda H, Shiratori H, Nakamura T, Hamada H . Pih1d3 is required for cytoplasmic preassembly of axonemal dynein in mouse sperm. J Cell Biol, 2014,204(2):203-213.
[34] Gastmann O, Burfeind P, Günther E, Hameister H, Szpirer C, Hoyer-Fender S . Sequence, expression, and chromosomal assignment of a human sperm outer dense fiber gene. Mol Reprod Dev, 1993,36(4):407-418.
[35] Shao X, Murthy S, Demetrick DJ, van der Hoorn FA . Human outer dense fiber gene, ODF2, localizes to chromosome 9q34. Cytogenet Cell Genet, 1998,83(3-4):221-223.
[36] Petersen C, Aumüller G, Bahrami M, Hoyer-Fender S . Molecular cloning of Odf3 encoding a novel coiled-coil protein of sperm tail outer dense fibers. Mol Reprod Dev, 2002,61(1):102-112.
[37] Wei Y, Wang X, Fu G, Yu L . Testis specific serine/threonine kinase 4 (Tssk4) maintains its kinase activity by phosphorylating itself at Thr-197. Mol Biol Rep, 2013,40(1):439-447.
[38] Wang X, Wei Y, Fu G, Li H, Saiyin H, Lin G, Wang Z, Chen S, Yu L . Tssk4 is essential for maintaining the structural integrity of sperm flagellum. Mol Hum Reprod, 2015,21(2):136-145.
[39] Zhou J, Yang F, Leu NA, Wang PJ . MNS1 is essential for spermiogenesis and motile ciliary functions in mice. PLoS Genet, 2012,8(3):e1002516.
[40] Hirokawa N, Nitta R, Okada Y . The mechanisms of kinesin motor motility: lessons from the monomeric motor KIF1A. Nat Rev Mol Cell Biol, 2009,10(12):877-884.
[41] Zhang Y, Ou Y, Cheng M, Saadi HS, Thundathil JC, van der Hoorn FA, . KLC3 is involved in sperm tail midpiece formation and sperm function. Dev Biol, 2012,366(2):101-110.
[42] Bhullar B, Zhang Y, Junco A, Oko R, van der Hoorn FA, . Association of kinesin light chain with outer dense fibers in a microtubule-independent fashion. J Biol Chem, 2003,278(18):16159-16168.
[43] Zhang Y, Oko R, van der Hoorn FA . Rat kinesin light chain 3 associates with spermatid mitochondria. Dev Biol, 2004,275(1):23-33.
[44] Vadnais ML, Lin AM, Gerton GL . Mitochondrial fusion protein MFN2 interacts with the mitostatin-related protein MNS1 required for mouse sperm flagellar structure and function. Cilia, 2014,3:5.
[45] Li WY, He XJ, Yang SM, Liu CY, Wu H, Liu WJ, Lv MR, Tang DD, Tan J, Tang SY, Chen YJ, Wang JJ, Zhang ZG, Wang HY, Jin L, Zhang F, Cao YX . Biallelic mutations of CFAP251 cause sperm flagellar defects and human male infertility. J Hum Genet, 2019,64(1):49-54.
[46] Liu W, Wu H, Wang L, Yang X, Liu C, He X, Li W, Wang J, Chen Y, Wang H, Gao Y, Tang S, Yang S, Jin L, Zhang F, Cao Y . Homozygous loss-of-function mutations in FSIP2 cause male infertility with asthenoteratospermia. J Genet Genomics, 2019,46(1):53-56.
[47] Fiedler SE, Dudiki T, Vijayaraghavan S, Carr DW . Loss of R2D2 proteins ROPN1 and ROPN1L causes defects in murine sperm motility, phosphorylation, and fibrous sheath integrity. Biol Reprod, 2013,88(2):41.
[48] Newell AE, Fiedler SE, Ruan JM, Pan J, Wang PJ, Deininger J, Corless CL, Carr DW . Protein kinase A RII-like (R2D2) proteins exhibit differential localization and AKAP interaction. Cell Motil Cytoskeleton, 2008,65(7):539-552.
[49] Catalano RD, Hillhouse EW, Vlad M . Developmental expression and characterization of FS39, a testis complementary DNA encoding an intermediate filament-related protein of the sperm fibrous sheath. Biol Reprod, 2001,65(1):277-287.
[50] Choi E, Cho C . Expression of a sperm flagellum component encoded by the Als2cr12 gene. Gene Expr Patterns, 2011,11(5-6):327-333.
[51] Modarressi MH, Behnam B, Cheng M, Taylor KE, Wolfe J, van der Hoorn FA . Tsga10 encodes a 65-kilodalton protein that is processed to the 27-kilodalton fibrous sheath protein. Biol Reprod, 2004,70(3):608-615.
[52] Hamada K, Shimizu T, Matsui T, Tsukita S, Hakoshima T . Structural basis of the membrane-targeting and unmasking mechanisms of the radixin FERM domain. EMBO J, 2000,19(17):4449-4462.
[53] Nakamura N, Dai QS, Williams J, Goulding EH, Willis WD, Brown PR, Eddy EM . Disruption of a spermatogenic cell-specific mouse enolase 4 (eno4) gene causes sperm structural defects and male infertility. Biol Reprod, 2013,88(4):90.
[54] Hoppeler-Lebel A, Celati C, Bellett G, Mogensen MM, Klein-Hitpass L, Bornens M, Tassin AM . Centrosomal CAP350 protein stabilises microtubules associated with the Golgi complex. J Cell Sci, 2007,120(Pt 18):3299-3308.
[55] Weidemann M, Schuster-Gossler K, Stauber M, Wrede C, Hegermann J, Ott T, Boldt K, Beyer T, Serth K, Kremmer E, Blum M, Ueffing M, Gossler A . CFAP157 is a murine downstream effector of FOXJ1 that is specifically required for flagellum morphogenesis and sperm motility. Development, 2016,143(24):4736-4748.
[56] Krausz C, Escamilla AR, Chianese C . Genetics of male infertility: from research to clinic. Reproduction, 2015,150(5):R159-R174.
[57] Ruan J, Du WD . Male infertility and gene defects. Hereditas(Beijing), 2010,32(5):411-422.
[57] 阮健, 杜卫东 . 男性不育与基因缺陷. 遗传, 2010,32(5):411-422.
Outlines

/