962
Views
8
CrossRef citations to date
0
Altmetric
Commentary and Views

Formins: Actin nucleators that regulate cytoskeletal dynamics during spermatogenesis

, , , , , & show all
Article: e1066476 | Received 07 May 2015, Accepted 18 Jun 2015, Published online: 30 Jul 2015

References

  • Hess RA, de Franca LR. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 2008; 636:1-15; PMID:19856159; http://dx.doi.org/10.1007/978-0-387-09597-4_1
  • Clermont Y, Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 1972; 52:198-235; PMID:4621362
  • O'Donnell L, Nicholls PK, O'Bryan MK, McLachlan RI, Stanton PG. Spermiation: the process of sperm release. Spermatogenesis 2011; 1:14-35; PMID:21866274; http://dx.doi.org/10.4161/spmg.1.1.14525
  • Mruk DD, Silvestrini B, Cheng CY. Anchoring junctions as drug targets: Role in contraceptive development. Pharmacol Rev 2008; 60:146-80; PMID:18483144; http://dx.doi.org/10.1124/pr.107.07105
  • Cheng CY, Mruk DD. Cell junction dynamics in the testis: Sertoli-germ cell interactions and male contraceptive development. Physiol Rev 2002; 82, 825-74; PMID:12270945; http://dx.doi.org/10.1152/physrev.00009.2002
  • Mruk DD, Cheng CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25:747-806; PMID:15466940; http://dx.doi.org/10.1210/er.2003-0022
  • Russell LD. Movement of spermatocytes from the basal to the adluminal compartment of the rat testis. Am J Anat 1977; 148:313-28; PMID:857632; http://dx.doi.org/10.1002/aja.1001480303
  • Russell LD. Observations on rat Sertoli ectoplasmic (‘junctional’) specializations in their association with germ cells of the rat testis. Tissue Cell 1977; 9:475-98; PMID:929577; http://dx.doi.org/10.1016/0040-8166(77)90007-6
  • Vogl AW, Vaid KS, Guttman JA. The Sertoli cell cytoskeleton. Adv Exp Med Biol 2008; 636:186-211; PMID:19856169; http://dx.doi.org/10.1007/978-0-387-09597-4_11
  • Cheng CY, Mruk DD. The blood-testis barrier and its implication in male contraception. Pharmacol Rev 2012; 64:16-64; PMID:22039149; http://dx.doi.org/10.1124/pr.110.002790
  • Wong EWP, Mruk DD, Cheng CY. Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochem Biophys Acta 2008; 1778:692-708; PMID:18068662; http://dx.doi.org/10.1016/j.bbamem.2007.11.006
  • Cheng CY, Mruk DD. A local autocrine axis in the testes that regulates spermatogenesis. Nature Rev Endocrinol 2010; 6:380-395; PMID:20571538; http://dx.doi.org/10.1038/nrendo.2010.71
  • Rotkopf S, Hamberg Y, Aigaki T, Snapper SB, Shilo BZ, Schejter ED. The WASp-based actin polymerization machinery is required in somatic support cells for spermatid maturation and release. Development 2011; 138:2729-39; PMID:21652648; http://dx.doi.org/10.1242/dev.059865
  • Xiao X, Mruk DD, Tang EI, Massarwa R, Mok KW, Li N, Wong CK, Lee WM, Snapper SB, Shilo BZ, et al. N-WASP is required for structural integrity of the blood-testis barrier. Proc Natl Acad Sci USA 2013; 10:e1004447; PMID:24967734
  • Lie PPY, Chan AYN, Mruk DD, Lee WM, Cheng CY. Restricted Arp3 expression in the testis prevents blood-testis barrier disruption during junction restructuring at spermatogenesis. Proc Natl Acad Sci USA 2010; 107:11411-6; PMID:20534520; http://dx.doi.org/10.1073/pnas.1001823107
  • Li MWM, Xiao X, Mruk DD, Lam YL, Lee WM, Lui WY, Bonanomi M, Silvestrini B, Cheng CY, et al. Actin binding protein drebrin E is involved in junction dynamics during spermatogenesis. Spermatogenesis 2011; 1:123-36; PMID:22319661; http://dx.doi.org/10.4161/spmg.1.2.16393
  • Lie PPY, Mruk DD, Lee WM, Cheng CY. Epidermal growth factor receptor pathway substrate 8 (Eps8) is a novel regulator of cell adhesion and the blood-testis barrier integrity in the seminiferous epithelium. FASEB J 2009; 23:2555-67; PMID:19293393; http://dx.doi.org/10.1096/fj.06-070573
  • Qian X, Mruk DD, Cheng YH, Cheng CY. Actin cross-linking protein palladin and spermatogenesis. Spermatogenesis 2013; 3:e23473; PMID:23687615; http://dx.doi.org/10.4161/spmg.23473
  • Su WH, Mruk DD, Lie PPY, Lui WY, Cheng CY. Filamin A is a regulator of blood-testis barrier assembly during postnatal development in the rat testis. Endocrinology 2012; 153:5023-35; PMID:22872576; http://dx.doi.org/10.1210/en.2012-1286
  • Su WH, Mruk DD Cheng CY. Filamin A: a regulator of blood-testis barrier assembly during post-natal development. Spermatogenesis 2012; 2:73-8; PMID:22670216; http://dx.doi.org/10.4161/spmg.20223
  • Cheng CY, Lie PPY, Wong EWP, Mruk DD. Focal adhesion kinase and actin regulatory/binding proteins that modulate F-actin organization at the tissue barrier. Lession from the testis. Tissue Barriers 2013; 1:e24252.; PMID:24665388; http://dx.doi.org/10.4161/tisb.24252
  • Zeller R, Haramis AG, Zuniga A, McGuigan C, Dono R, Davidson G, Chabanis S, Gibson T. Formin defines a large family of morphorgulatory genes and functions in establishment of the polarising region. Cell Tissue Res 1999; 296:85-93; PMID:10199968; http://dx.doi.org/10.1007/s004410051269
  • Bartolini F, Gundersen GG. Formins and microtubules. Biochem Biophys Acta 2010; 1803:164-73; PMID:19631698; http://dx.doi.org/10.1016/j.bbamcr.2009.07.006
  • Baarlink C, Brandt D, Grosse R. SnapShot: Formins. Cell 2010; 142:172; PMID:20603022; http://dx.doi.org/10.1016/j.cell.2010.06.030
  • Higgs HN, Peterson KJ. Phylogenetic analysis of the formin homology 2 domain. Mol Biol Cell 2005; 16:1-13; PMID:15509653; http://dx.doi.org/10.1091/mbc.E04-07-0565
  • Kerkhoff E. Actin dynamics at intracellular membranes: the Spir/formin nucleator complex. Eur J Cell Biol 2011; 90:922-5; PMID:21129813; http://dx.doi.org/10.1016/j.ejcb.2010.10.011
  • Yang C, Svitkina T. Filopoldia initiation. Focus on the Arp2/3 complex and formins. Cell Adh Migr 2011; 5:402-8; PMID:21975549; http://dx.doi.org/10.4161/cam.5.5.16971
  • Woychik RP, Maas RL, Zeller R, Vogt TF, Leder P. ‘Formins’: proteins deduced from the alternative transcripts of the limb deformity gene. Nature 1990; 346:850-3; PMID:2392150; http://dx.doi.org/10.1038/346850a0
  • Chesarone MA, DuPage AG, Goode BL. Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rev Mol Cell Biol 2010; 11:62-74; PMID:19997130; http://dx.doi.org/10.1038/nrm2816
  • Chesarone MA, Goode BL. Actin nucleation and elgonation factors: mechanisms and interplay. Curr Opin Cell Biol 2009; 21:28-37; PMID:19168341; http://dx.doi.org/10.1016/j.ceb.2008.12.001
  • Nurnberg A, Kitzing T, Grosse R. Nucleating actin for invasion. Nat Rev Cancer 2011; 11:177-87; PMID:21326322; http://dx.doi.org/10.1038/nrc3003
  • Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008; 321:1807-12; PMID:18772396; http://dx.doi.org/10.1126/science.1164382
  • Jones S, Zhang X, Parsons DW, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Kamiyama H, Jimeno A, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analysis. Science 2008; 321:1801-6; PMID:18772397; http://dx.doi.org/10.1126/science.1164368
  • Zhu XL, Liang L, Ding YQ. Overexpression of FMN2 is closely related to metastasis of colorectal cancer. Intern J Colorectal Dis 2008; 23:1041-7; PMID:18665374; http://dx.doi.org/10.1007/s00384-008-0520-2
  • Pruyne D, Evangelista M, Yang C, Bi E, Zigmond S, Bretscher A, Boone C. Role of formins in actin assembly: nucleation and barbed-end association. Science 2002; 297:612-5; PMID:12052901; http://dx.doi.org/10.1126/science.1072309
  • Sagot I, Rodal AA, Moseley J, Goode BL, Pellman D. An actin nucleation mechanism mediated by Bni1 and Profilin. Nat Cell Biol 2002; 4:626-31; PMID:12134165
  • Kovar DR. Molecular details of formin-mediated actin assembly. Curr Opin Cell Biol 2006; 18, 11-7; PMID:16364624; http://dx.doi.org/10.1016/j.ceb.2005.12.011
  • Hofmann K, Bucher P. The rsp5-domain is shared by proteins of diverse functions. FEBS Lett 1995; 358:153-7; PMID:7828727; http://dx.doi.org/10.1016/0014-5793(94)01415-W
  • Andre B, Springael JY. WWP, a new amino oacid motif present in single or multiple coplies in various proteins including dystrophin and the SH3-binding Yes-associated protein YAP65. Biochem Biophys Res Commun 1994; 205:1201-5; PMID:7802651; http://dx.doi.org/10.1006/bbrc.1994.2793
  • Rotin D. WW (WWP) domains: from structure to function. Curr Top Microbiol Immunol 1998; 228:115-33; PMID:9401204
  • Rivero F, Muramoto T, Meyer AK, Urushihara H, Uyeda TQ, Kitayama C. A comparative sequence analysis reveals a common GBD/FH3-FH1-FH2-DAD architecture in formins from Dictyostelium, fungi and metazoa. BMC Genomics 2005; 6:28; PMID:15740615; http://dx.doi.org/10.1186/1471-2164-6-28
  • Goode BL, Eck MJ. Mechanism and function of formins in the control of actin assembly. Annu Rev Biochem 2007; 76:593-627; PMID:17373907; http://dx.doi.org/10.1146/annurev.biochem.75.103004.142647
  • Breitsprecher D, Jaiswal R, Bombardier JP, Gould CJ, Gelles J, Goode BL. Rocket launcher mechanism of collaborative actin assemboly defined by single-molecule imaging. Science 2012; 336:1164-8; PMID:22654058; http://dx.doi.org/10.1126/science.1218062
  • Breitsprecher D, Goode BL. Formins at a glance. J Cell Sci 2013; 126:1-7; PMID:23516326; http://dx.doi.org/10.1242/jcs.107250
  • Neidt EM, Skau CT, Kovar DR. The cytokinesis formins from the nematode worm and fission yeast differentially mediate actin filament assembly. J Biol Chem 2008; 283:23872-83; PMID:18577519; http://dx.doi.org/10.1074/jbc.M803734200
  • Baarlink C, Wang H, Grosse R. Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 2013; 340:864-7; PMID:23558171; http://dx.doi.org/10.1126/science.1235038
  • Li N, Mruk DD, Wong CK, Han D, Lee WM, Cheng CY. Formin 1 regulates ectoplamic specialization in the rat testis through its actin nucleation and bundling activity. Endocrinology 2015; in press; PMID:25901598
  • Zuniga A, Michos O, Spitz F, Haramis AP, Panman L, Galli A, Vintersten K, Klasen C, Mansfield W, Kuc S, et al. Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev 2004; 8:1553-64; PMID:15198975; http://dx.doi.org/10.1101/gad.299904
  • Kobielak A, Pasolli HA, Fuchs E. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 2004; 6:21-30; PMID:14647292; http://dx.doi.org/10.1038/ncb1075
  • Zhou F, Leder P, Martin SS. Formin-1 protein associates with microtubules through a peptide domain encoded by exon-2. Exp Cell Res 2006; 312:1119-26; PMID:16480715; http://dx.doi.org/10.1016/j.yexcr.2005.12.035
  • Vogl AW, Young JS, Du M. New insights into roles of tubulobulbar complexes in sperm release and turnover of blood-testis barrier. Int Rev Cell Mol Biol 2013; 303:319-55; PMID:23445814; http://dx.doi.org/10.1016/B978-0-12-407697-6.00008-8
  • Vogl AW, Du M, Wang XY, Young JS. Novel clathrin/actin-based endocytic machinery associated with junction turnover in the seminiferous epithelium. Semin Cell Dev Biol 2014; 30:55-64; PMID:24280271; http://dx.doi.org/10.1016/j.semcdb.2013.11.002
  • Xiao X, Mruk DD, Wong CKC, Cheng CY. Germ cell transport across the seminiferous epithelium during spermatogenesis. Physiology 2014; 29:286-98; PMID:24985332; http://dx.doi.org/10.1152/physiol.00001.2014
  • Bohnert KA, Willet AH, Kovar DR, Gould KL. Formin-based control of the actin cytoskeleton during cytokinesis. Biochem Soc Trans 2013; 41:1750-4; PMID:24256286
  • O'Donnell L, O'Bryan MK. Microtubules and spermatogenesis. Semin Cell Dev Biol 2014; 30:45-54; PMID:24440897; http://dx.doi.org/10.1016/j.semcdb.2014.01.003
  • Lie PPY, Mruk DD, Lee WM, Cheng CY. Cytoskeletal dynamics and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 2010; 365:1581-92; PMID:20403871; http://dx.doi.org/10.1098/rstb.2009.0261
  • Tang EI, Mruk DD, Cheng CY. MAP/microtubule affinity-regulating kinases, microtubule dynamics, and spermatogenesis. J Endocrinol 2013; 217:R13-23; PMID:23449618; http://dx.doi.org/10.1530/JOE-12-0586
  • Clermont Y, Morales C, Hermo L. Endocytic activities of Sertoli cells in the rat. Ann NY Acad Sci 1987; 513:1-15; PMID:3328532; http://dx.doi.org/10.1111/j.1749-6632.1987.tb24994.x
  • Seth A, Otomo C, Rosen MK. Autoinhibition regulates cellular localization and actin assembly activity of the diaphanous-related formins FRLalpha and mDia1. J Cell Biol 2006; 174:701-13; PMID:16943183; http://dx.doi.org/10.1083/jcb.200605006
  • Bartolini F, Ramalingam N, Gundersen GG. Actin-capping protein promotes microtubule stability by antagonizing the actin activity of mDia1. Mol Biol Cell 2012; 23:4032-40; PMID:22918941; http://dx.doi.org/10.1091/mbc.E12-05-0338
  • Shi Y, Zhang J, Mullin M, Dong B, Alberts AS, Siminovitch KA. The mDial formin is required for neutrophil polarization, migration, and activation of the LARG/RhoA/ROCK signaling axis during chemotaxis. J Immunol 2009; 182:3837-45; PMID:19265163; http://dx.doi.org/10.4049/jimmunol.0803838
  • DeWard AD, Leali K, West RA, Prendergast GC, Alberts AS. Loss of RhoB expression enhances the myelodysplastic phenotype of mammalian diaphanous-related Formin mDia1 knockout mice. PLoS One 2009; 4:e7102; PMID:19768111; http://dx.doi.org/10.1371/journal.pone.0007102
  • Eisenmann KM, West RA, Hildebrand D, Kitchen SM, Peng J, Sigler R, Zhang J, Siminovitch KA, Alberts AS. T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice. J Biol Chem 2007; 282:25152-8; PMID:17595162; http://dx.doi.org/10.1074/jbc.M703243200
  • Ercan-Sencicek AG, Jambi S, Franjic D, Nishimura S, Li M, El-Fishawy P, Morgan TM, Sanders SJ, Bilguvar K, Suri M, et al. Homozygous loss of DIAPH1 is a novel cause of microcephaly in humans. Eur J Hum Genet 2015; 23:165-172; PMID:24781755; http://dx.doi.org/10.1038/ejhg.2014.82
  • Wallar BJ, Deward AD, Resau JH, Alberts AS. RhoB and the mammalian Diaphanous-related formin mDia2 in endosome trafficking. Exp Cell Res 2007; 313:560-71; PMID:17198702; http://dx.doi.org/10.1016/j.yexcr.2006.10.033
  • Bartolini F, Moseley JB, Schmoranzer J, Cassimeris L, Goode BL, Gundersen GG. The formin mDia2 stabilizes microtubules independently of its actin nucleation activity. J Cell Biol 2008; 181:523-36; PMID:18458159; http://dx.doi.org/10.1083/jcb.200709029
  • Watanabe S, De Zan T, Ishizaki T, Yasuda S, Kamijo H, Yamada D, Aoki T, Kiyonari H, Kaneko H, Shimizu R, Yamamoto M, Goshima G, Narumiya S. Loss of a Rho-regulated actin nucleator, mDia2, impairs cytokinesis during mouse fetal erythropoiesis. Cell Rep 2013; 5:926-32; PMID:18815276; http://dx.doi.org/10.1016/j.celrep.2013.10.021
  • Yasuda S, Oceguera-Yanez F, Kato T, Okamoto M, Yonemura S, Terada Y, Ishizaki T, Narumiya S. Cdc42 and mDia3 regulate microtubule attachment to kinetochores. Nature 2004; 428:767-71; PMID:15085137; http://dx.doi.org/10.1038/nature02452
  • Cheng L, Zhang J, Ahmad S, Rozier L, Yu H, Deng H, Mao Y. Aurora B regulates formin mDia3 in achieving metaphase chromosome alignment. Dev Cell 2011; 20:342-52; PMID:21397845; http://dx.doi.org/10.1016/j.devcel.2011.01.008
  • Shinohara R, Thumkeo D, Kamijo H, Kaneko N, Sawamoto K, Watanabe K, Takebayashi H, Kiyonari H, Ishizaki T, Furuyashiki T, et al. A role for mDia, a Rho-regulated actin nucleator, in tangential migration of interneuron precursors. Nat Neurosci 2012; 15:373-80, S371-372; PMID:22246438; http://dx.doi.org/10.1038/nn.3020
  • Kida YS, Sato T, Miyasaka KY, Suto A, Ogura T. Daam1 regulates the endocytosis of EphB during the convergent extension of the zebrafish notochord. Proc Natl Acad Sci U S A 2007; 104:6708-13; PMID:17412835; http://dx.doi.org/10.1073/pnas.0608946104
  • Miller RK, Canny SG, Jang CW, Cho K, Ji H, Wagner DS, Jones EA, Habas R, McCrea PD. Pronephric tubulogenesis requires Daam1-mediated planar cell polarity signaling. J Am Soc Nephrol 2011; 22:1654-64; PMID:21804089; http://dx.doi.org/10.1681/ASN.2010101086
  • Li D, Hallett MA, Zhu W, Rubart M, Liu Y, Yang Z, Chen H, Haneline LS, Chan RJ, Schwartz RJ, et al. Dishevelled-associated activator of morphogenesis 1 (Daam1) is required for heart morphogenesis. Development 2011; 138:303-15; PMID:21177343; http://dx.doi.org/10.1242/dev.055566
  • Gomez TS, Kumar K, Medeiros RB, Shimizu Y, Leibson PJ, Billadeau DD. Formins regulate the actin-related protein 2/3 complex-independent polarization of the centrosome to the immunological synapse. Immunity 2007; 26:177-90; PMID:17306570; http://dx.doi.org/10.1016/j.immuni.2007.01.008
  • Naj X, Hoffmann AK, Himmel M, Linder S. The formins FMNL1 and mDia1 regulate coiling phagocytosis of Borrelia burgdorferi by primary human macrophages. Infect Immun 2013; 81:1683-95; PMID:23460512; http://dx.doi.org/10.1128/IAI.01411-12
  • Zhou F, Leder P, Zuniga A, Dettenhofer M. Formin1 disruption confers oligodactylism and alters Bmp signaling. Hum Mol Genet 2009; 18:2472-82; PMID:19383632; http://dx.doi.org/10.1093/hmg/ddp185
  • Young KG, Thurston SF, Copeland S, Smallwood C, Copeland JW. INF1 is a novel microtubule-associated formin. Mol Biol Cell 2008; 19:5168-80; PMID:18815276; http://dx.doi.org/10.1091/mbc.E08-05-0469
  • Mironova E, Millette CF. Expression of the diaphanous-related formin proteins mDia1 and mDia2 in the rat testis. Dev Dyn 2008; 237:2170-6; PMID:18651670 http://dx.doi.org/10.1002/dvdy.21622
  • Behnen M, Murk K, Kursula P, Cappallo-Obermann H, Rothkegel M, Kierszenbaum AL, Kirchhoff C. Testis-expressed profilins 3 and 4 show distinct functional characteristics and localize in the acroplaxome-manchette complex in spermatids. BMC Cell Biol 2009; 10:34; PMID:19419568; http://dx.doi.org/10.1186/1471-2121-10-34

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.