Full Text:   <2967>

CLC number: Q78

On-line Access: 

Received: 2007-02-26

Revision Accepted: 2007-05-09

Crosschecked: 0000-00-00

Cited: 23

Clicked: 5727

Citations:  Bibtex RefMan EndNote GB/T7714

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2007 Vol.8 No.7 P.498-506

http://doi.org/10.1631/jzus.2007.B0498


Actin-based dynamics during spermatogenesis and its significance


Author(s):  XIAO Xiang, YANG Wan-xi

Affiliation(s):  The Sperm Laboratory, Institute of Cell Biology and Genetics, School of Life Sciences, Zhejiang University, Hangzhou 310058, China

Corresponding email(s):   wxyang@spermlab.org

Key Words:  Testis, Actin, Spermatogenesis, Nuclear shaping, Sertoli cell


XIAO Xiang, YANG Wan-xi. Actin-based dynamics during spermatogenesis and its significance[J]. Journal of Zhejiang University Science B, 2007, 8(7): 498-506.

@article{title="Actin-based dynamics during spermatogenesis and its significance",
author="XIAO Xiang, YANG Wan-xi",
journal="Journal of Zhejiang University Science B",
volume="8",
number="7",
pages="498-506",
year="2007",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.2007.B0498"
}

%0 Journal Article
%T Actin-based dynamics during spermatogenesis and its significance
%A XIAO Xiang
%A YANG Wan-xi
%J Journal of Zhejiang University SCIENCE B
%V 8
%N 7
%P 498-506
%@ 1673-1581
%D 2007
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.2007.B0498

TY - JOUR
T1 - Actin-based dynamics during spermatogenesis and its significance
A1 - XIAO Xiang
A1 - YANG Wan-xi
J0 - Journal of Zhejiang University Science B
VL - 8
IS - 7
SP - 498
EP - 506
%@ 1673-1581
Y1 - 2007
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.2007.B0498


Abstract: 
actin can be found in all kinds of eukaryotic cells, maintaining their shapes and motilities, while its dynamics in sperm cells is understood less than their nonmuscle somatic cell counterparts. spermatogenesis is a complicated process, resulting in the production of mature sperm from primordial germ cell. Significant structural and biochemical changes take place in the seminiferous epithelium of the adult testis during spermatogenesis. It was proved that all mammalian sperm contain actin, and that F-actin may play an important role during spermatogenesis, especially in nuclear shaping. Recently a new model for sperm head elongation based on the acrosome-acroplaxome-manchette complex has been proposed. In Drosophila, F-actin assembly is supposed to be very crucial during individualization. In this mini-review, we provide an overview of the structure, function, and regulation characteristics of actin cytoskeleton, and a summary of the current status of research of actin-based structure and movement is also provided, with emphasis on the role of actins in sperm head shaping during spermiogenesis and the cell junction dynamics in the testis. Research of the Sertoli ectoplasmic specialization is in the spotlight, which is a testis-specific actin-based junction very important for the movement of germ cells across the epithelium. Study of the molecular architecture and the regulating mechanism of the Sertoli ectoplasmic specialization has become an intriguing field. All this may lead to a new strategy for male infertility and, at the same time, a novel idea may result in devising much safer contraception with high efficiency. It is hoped that the advances listed in this review would give developmental and morphological researchers a favorable investigating outline and could help to enlarge the view of new strategies and models for actin dynamics during spermatogenesis.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1] Abou-Haila, A., Tulsiani, D.R., 2000. Mammalian sperm acrosome: formation, contents, and function. Arch. Biochem. Biophys., 379(2):173-182.

[2] Adema, C.M., 2002. Comparative study of cytoplasmic actin DNA sequences from six species of Planorbidae (Gastropoda: Basommatophora). J. Moll. Stud., 68(1):17-23.

[3] Alberts, B., Bray, D., Johnson, A., Lewis, J., Raff, M., Roberts, K., Watson, J.D., 1994. Molecular Biology of the Cell, 3rd Ed. Garland Publishing Inc., New York and London, p.787-1034.

[4] Anahara, R., Toyama, Y., Mori, C., 2004. Flutamide induces ultrastructural changes in spermatids and the ectoplasmic specialization between the Sertoli cell and spermatids in mouse testes. Reprod. Toxicol., 18(4):589-596.

[5] Anahara, R., Toyama, Y., Maekawa, M., Yoshida, M., Kai, M., Ishino, F., Toshimori, K., Mori, C., 2006a. Anti-estrogen ICI 182.780 and anti-androgen flutamide induce tyrosine phosphorylation of cortactin in the ectoplasmic specialization between the Sertoli cell and spermatids in the mouse testis. Biochem. Biophys. Res. Commun., 346(1):276-280.

[6] Anahara, R., Yoshida, M., Toyama, Y., Maekawa, M., Kai, M., Ishino, F., Toshimori, K., Mori, C., 2006b. Estrogen agonists, 17beta-estradiol, bisphenol A, and diethyl-stilbestrol, decrease cortactin expression in the mouse testis. Arch. Histol. Cytol., 69(2):101-107.

[7] Ayscough, K.R., Winder, S.J., 2004. Two billion years of actin. EMBO Rep., 5(10):947-952.

[8] Billadeau, D.D., Burkhardt, J.K., 2006. Regulation of cytoskeletal dynamics at the immune synapse: new stars join the actin troupe. Traffic, 7(11):1451-1460.

[9] Breitbart, H., Cohen, G., Rubinstein, S., 2005. Role of actin cytoskeleton in mammalian sperm capacitation and the acrosome reaction. Reproduction, 129(3):263-268.

[10] Campa, F., Machuy, N., Klein, A., Rudel, T., 2006. A new interaction between Abi-1 and betaPIX involved in PDGF-activated actin cytoskeleton reorganisation. Cell Res., 16(9):759-770.

[11] Cappuccinelli, P., 1987. Motility of Living Cells, Outline Studies in Biology. Science Press, Beijing, p.24-30 (in Chinese).

[12] Carraway, K.L., Carraway, C.A.C., 2000. Cytoskeleton: Signaling and Cell Regulation. Oxford University Press, New York, p.1-121.

[13] Cheng, C.Y., Mruk, D.D., 2002. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol. Rev., 82(4):825-874.

[14] Cheng, C.Y., Mruk, D.D., Silvestrini, B., Bonanomi, M., Wong, C.H., Siu, M.K., Lee, N.P., Lui, W.Y., Mo, M.Y., 2005. AF-2364 1-(2,4-dichlorobenzyl)-1H-indazole-3-carbohydrazide] is a potential male contraceptive: a review of recent data. Contraception, 72(4):251-261.

[15] Choudhuri, J., Aleem, M., Padwal, V., Das Gupta, P., Souza, R.D., Pathak, S., Balasinor, N., Gill-Sharma, M.K., 2005. Effect of estradiol on expression of cytoskeletal proteins during spermatogenesis in testis of sexually mature rats. Indian J. Exp. Biol., 43(11):1068-1079.

[16] Costa, M.L., Escaleira, R., Cataldo, A., Oliveira, F., Mermelstein, C.S., 2004. Desmin: molecular interactions and putative functions of the muscle intermediate filament protein. Braz. J. Med. Biol. Res., 37(12):1819-1830.

[17] Diez, S., Gerisch, G., Anderson, K., Muller-Taubenberger, A., Bretschneider, T., 2005. Subsecond reorganization of the actin network in cell motility and chemotaxis. Proc. Natl. Acad. Sci. USA, 102(21):7601-7606.

[18] Fahrni, J.F., Bolivar, I., Berney, C., Nassonova, E., Smirnov, A., Pawlowski, J., 2003. Phylogeny of lobose amoebae based on actin and small-subunit ribosomal RNA genes. Mol. Biol. Evol., 20(11):1881-1886.

[19] Fouquet, J., Kann, M., Soues, S., Melki, R., 2000. ARP1 in Golgi organisation and attachment of manchette microtubules to the nucleus during mammalian spermatogenesis. J. Cell Sci., 113(Pt 5):877-886.

[20] Ghosh-Roy, A., Desai, B.S., Ray, K., 2005. Dynein light chain 1 regulates dynamin-mediated F-actin assembly during sperm individualization in Drosophila. Mol. Biol. Cell, 16(7):3107-3116.

[21] Gilbert, S.F., 2000. Developmental Biology, 6th Ed. Sinauer Associates Inc., Sunderland, Massachusetts, p.185-216.

[22] Gilk, S.D., Raviv, Y., Hu, K., Murray, J.M., Beckers, C.J., Ward, G.E., 2006. Identification of PhIL1, a novel cytoskeletal protein of the Toxoplasma gondii pellicle, through photosensitized labeling with 5-[125I]iodonaph-thalene-1-azide. Eukaryot. Cell, 5(10):1622-1634.

[23] Goley, E.D., Welch, M.D., 2006. The ARP2/3 complex: an actin nucleator comes of age. Nat. Rev. Mol. Cell Biol., 7(10):713-726.

[24] Goley, E.D., Ohkawa, T., Mancuso, J., Woodruff, J.B., D'Alessio, J.A., Cande, W.Z., Volkman, L.E., Welch, M.D., 2006. Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science, 314(5798):464-467.

[25] Hirohashi, N., Vacquier, V.D., 2003. Store-operated calcium channels trigger exocytosis of the sea urchin sperm acrosomal vesicle. Biochem. Biophys. Res. Commun., 304(2):285-292.

[26] Hitchcock-DeGregori, S.E., Greenfield, N.J., Singh, A., 2007. Tropomyosin: regulator of actin filaments. Adv. Exp. Med. Biol., 592:87-97.

[27] Howes, E.A., Hurst, S.M., Jones, R., 2001. Actin and actin-binding proteins in bovine spermatozoa: potential role in membrane remodeling and intracellular signaling during epididymal maturation and the acrosome reaction. J. Androl., 22(1):62-72.

[28] Jégou, B., 1992. The Sertoli cell in vivo and in vitro. Cell Biol. Toxicol., 8(3):49-54.

[29] Kaksonen, M., Toret, C.P., Drubin, D.G., 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol., 7(6):404-414.

[30] Khatchadourian, K., Smith, C.E., Metzler, M., Gregory, M., Hayden, M.R., Cyr, D.G., Hermo, L., 2007. Structural abnormalities in spermatids together with reduced sperm counts and motility underlie the reproductive defect in HIP1−/− mice. Mol. Reprod. Dev., 74(3):341-359.

[31] Kierszenbaum, A.L., Tres, L.L., 2004. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch. Histol. Cytol., 67(4):271-284.

[32] Kierszenbaum, A.L., Rivkin, E., Tres, L.L., 2003a. The actin-based motor myosin Va is a component of the acroplaxome, an acrosome-nuclear envelope junctional plate, and of manchette-associated vesicles. Cytogenet. Genome Res., 103(3-4):337-344.

[33] Kierszenbaum, A.L., Rivkin, E., Tres, L.L., 2003b. Acroplaxome, an F-actin-keratin-containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol. Biol. Cell, 14(11):4628-4640.

[34] Kierszenbaum, A.L., Tres, L.L., Rivkin, E., Kang-Decker, N., van Deursen, J.M., 2004. The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/b-containing proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids. Biol. Reprod., 70(5):1400-1410.

[35] Lee, N.P., Cheng, C.Y., 2004. Ectoplasmic specialization, a testis-specific cell-cell actin-based adherens junction type: is this a potential target for male contraceptive development? Hum. Reprod. Update, 10(4):349-369.

[36] Lehmann, M.J., Sherer, N.M., Marks, C.B., Pypaert, M., Mothes, W., 2005. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J. Cell Biol., 170(2):317-325.

[37] Liu, D.Y., Martic, M., Clarke, G.N., Dunlop, M.E., Baker, H.W., 1999. An important role of actin polymerization in the human zona pellucida-induced acrosome reaction. Mol. Hum. Reprod., 5(10):941-949.

[38] Liu, D.Y., Martic, M., Clarke, G.N., Grkovic, I., Garrett, C., Dunlop, M.E., Baker, H.W., 2002. An anti-actin monoclonal antibody inhibits the zona pellucida-induced acrosome reaction and hyperactivated motility of human sperm. Mol. Hum. Reprod., 8(1):37-47.

[39] Lora-Lamia, C., Castellani-Ceresa, L., Andreetta, F., Cotelli, F., Brivio, M., 1986. Localization and distribution of actin in mammalian sperm heads. J. Ultrastruct. Mol. Struct. Res., 96(1-3):12-21.

[40] Lui, W.Y., Mruk, D., Lee, W.M., Cheng, C.Y., 2003. Sertoli cell tight junction dynamics: their regulation during spermatogenesis. Biol. Reprod., 68(4):1087-1097.

[41] Luk, J.M., Lee, N.P., Shum, C.K., Lam, B.Y., Siu, A.F., Che, C.M., Tam, P.C., Cheung, A.N., Yang, Z.M., Lin, Y.N., Matzuk, M.M., Lee, K.F., Yeung, W.S., 2006. Acrosome-specific gene AEP1: identification, characterization and roles in spermatogenesis. J. Cell. Physiol., 209(3):755-766.

[42] Ma, P., Wang, H., Guo, R., Ma, Q., Yu, Z., Jiang, Y., Ge, Y., Ma, J., Xue, S., Han, D., 2006. Stage-dependent Dishevelled-1 expression during mouse spermatogenesis suggests a role in regulating spermatid morphological changes. Mol. Reprod. Dev., 73(6):774-783.

[43] Maier, B., Medrano, S., Sleight, S.B., Visconti, P.E., Scrable, H., 2003. Developmental association of the synaptic activity-regulated protein arc with the mouse acrosomal organelle and the sperm tail. Biol. Reprod., 68(1):67-76.

[44] Malacombe, M., Bader, M.F., Gasman, S., 2006. Exocytosis in neuroendocrine cells: new tasks for actin. Biochim. Biophys. Acta, 1763(11):1175-1183.

[45] Marston, D.J., Goldstein, B., 2006. Actin-based forces driving embryonic morphogenesis in Caenorhabditis elegans. Curr. Opin. Genet. Dev., 16(4):392-398.

[46] Mruk, D.D., Cheng, C.Y., 2004a. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr. Rev., 25(5):747-806.

[47] Mruk, D.D., Cheng, C.Y., 2004b. Cell-cell interactions at the ectoplasmic specialization in the testis. Trends. Endocrinol. Metab., 15(9):439-447.

[48] Mruk, D.D., Lau, A.S., Conway, A.M., 2005. Crosstalk between Rab GTPases and cell junctions. Contraception, 72(4):280-290.

[49] Mruk, D.D., Wong, C.H., Silvestrini, B., Cheng, C.Y., 2006. A male contraceptive targeting germ cell adhesion. Nat. Med., 12(11):1323-1328.

[50] Noguchi, T., Miller, K.G., 2003. A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development, 130(9):1805-1816.

[51] Obermann, H., Raabe, I., Balvers, M., Brunswig, B., Schulze, W., Kirchhoff, C., 2005. Novel testis-expressed profilin IV associated with acrosome biogenesis and spermatid elongation. Mol. Hum. Reprod., 11(1):53-64.

[52] O'Donnell, L., Stanton, P.G., Bartles, J.R., Robertson, D.M., 2000. Sertoli cell ectoplasmic specializations in the seminiferous epithelium of the testosterone-suppressed adult rat. Biol. Reprod., 63(1):99-108.

[53] Percipalle, P., Visa, N., 2006. Molecular functions of nuclear actin in transcription. J. Cell Biol., 172(7):967-971.

[54] Robalo, J.I., Almada, V.C., Levy, A., Doadrio, I., 2007. Re-examination and phylogeny of the genus Chondrostoma based on mitochondrial and nuclear data and the definition of 5 new genera. Mol. Phylogenet. Evol., 42(2):362-372.

[55] Sahara, K., Kawamura, N., 2004. Roles of actin networks in peristaltic squeezing of sperm bundles in Bombyx mori. J. Morphol., 259(1):1-6.

[56] Sanders, S., Debuse, M., 2003. Endocrine & Reproductive Systems, 2nd Ed. Elsevier Science Ltd., London, p.149-156.

[57] Siu, M.K., Cheng, C.Y., 2004. Extracellular matrix: recent advances on its role in junction dynamics in the seminiferous epithelium during spermatogenesis. Biol. Reprod., 71(2):375-391.

[58] Spungin, B., Margalit, I., Breitbart, H., 1995. Sperm exocytosis reconstructed in a cell-free system: evidence for the involvement of phospholipase C and actin filaments in membrane fusion. J. Cell Sci., 108 (Pt 6):2525-2535.

[59] Stehn, J.R., Schevzov, G., O'Neill, G.M., Gunning, P.W., 2006. Specialisation of the tropomyosin composition of actin filaments provides new potential targets for chemotherapy. Curr. Cancer Drug Targets, 6(3):245-256.

[60] Stevens, J.M., Galyov, E.E., Stevens, M.P., 2006. Actin-dependent movement of bacterial pathogens. Nat. Rev. Microbiol., 4(2):91-101.

[61] Talbot, P., Kleve, M.G., 1978. Hamster sperm cross react with anti-actin. J. Exp. Zool., 204(1):131-136.

[62] Toyama, Y., Hosoi, I., Ichikawa, S., Maruoka, M., Yashiro, E., Ito, H., Yuasa, S., 2001. Beta-estradiol 3-benzoate affects spermatogenesis in the adult mouse. Mol. Cell. Endocrinol., 178(1-2):161-168.

[63] Toyama, Y., Suzuki-Toyota, F., Maekawa, M., Ito, C., Toshimori, K., 2004. Adverse effects of bisphenol A to spermiogenesis in mice and rats. Arch. Histol. Cytol., 67(4):373-381.

[64] Virtanen, I., Badley, R.A., Paasivuo, R., Lehto, V.P., 1984. Distinct cytoskeletal domains revealed in sperm cells. J. Cell Biol., 99(3):1083-1091.

[65] Vogl, A.W., 1989. Distribution and function of organized concentrations of actin filaments in mammalian spermatogenic cells and Sertoli cells. Int. Rev. Cytol., 119:1-56.

[66] Weis, W.I., Nelson, W.J., 2006. Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem., 281(47):35593-35597.

[67] Wolski, K.M., Haller, E., Cameron, D.F., 2005. Cortactin and phagocytosis in isolated Sertoli cells. J. Negat. Results Biomed., 4(1):11.

[68] Wolski, K.M., Mruk, D.D., Cameron, D.F., 2006. The Sertoli-spermatid junctional complex adhesion strength is affected in vitro by adjudin. J. Androl., 27(6):790-794.

[69] Wong, C.H., Cheng, C.Y., 2005a. Mitogen-activated protein kinases, adherens junction dynamics, and spermatogenesis: a review of recent data. Dev. Biol., 286(1):1-15.

[70] Wong, C.H., Cheng, C.Y., 2005b. The blood-testis barrier: its biology, regulation, and physiological role in spermatogenesis. Curr. Top. Dev. Biol., 71:263-296.

[71] Wong, C.H., Xia, W., Lee, N.P., Mruk, D.D., Lee, W.M., Cheng, C.Y., 2005. Regulation of ectoplasmic specialization dynamics in the seminiferous epithelium by focal adhesion-associated proteins in testosterone-suppressed rat testes. Endocrinology, 146(3):1192-1204.

[72] Xia, W., Wong, C.H., Lee, N.P., Lee, W.M., Cheng, C.Y., 2005. Disruption of Sertoli-germ cell adhesion function in the seminiferous epithelium of the rat testis can be limited to adherens junctions without affecting the blood-testis barrier integrity: an in vivo study using an androgen suppression model. J. Cell. Physiol., 205(1):141-157.

[73] Yan, H.H., Cheng, C.Y., 2005. Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. Proc. Natl. Acad. Sci. USA, 102(33):11722-11727.

[74] Yan, H.H., Mruk, D.D., Lee, W.M., Cheng, C.Y., 2007. Ectoplasmic specialization: a friend or a foe of spermatogenesis? Bioessays, 29(1):36-48.

[75] Yang, W.X., Sperry, A.O., 2003. C-terminal kinesin motor KIFC1 participates in acrosome biogenesis and vesicle transport. Biol. Reprod., 69(5):1719-1729.

[76] Yao, R., Ito, C., Natsume, Y., Sugitani, Y., Yamanaka, H., Kuretake, S., Yanagida, K., Sato, A., Toshimori, K., Noda, T., 2002. Lack of acrosome formation in mice lacking a Golgi protein, GOPC. Proc. Natl. Acad. Sci. USA, 99(17):11211-11216.

[77] Yu, R., Ono, S., 2006. Dual roles of tropomyosin as an F-actin stabilizer and a regulator of muscle contraction in Caenorhabditis elegans body wall muscle. Cell Motil. Cytoskeleton, 63(11):659-672.

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2024 Journal of Zhejiang University-SCIENCE