SEPT12/SPAG4/LAMINB1 complexes are required for maintaining the integrity of the nuclear envelope in postmeiotic male germ cells

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Yeh, Chung Hsin ^a,b   Kuo, Pao Lin ^c   Wang, Ya Yun ^c   Wu, Ying Yu ^d   Chen, Mei Feng ^e   Lin, Ding Yen ^f   Lai, Tsung Hsuan ^b,g,h   Chiang, Han Sun ^b,d   Lin, Ying Hung ^d  

^a SHIN KONG WU HO SU MEMORIAL HOSPITAL   (Taiwan)

^b FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^c NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^d FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^e CHANG GUNG UNIVERSITY   (Taiwan)

^f NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^g CATHAY GENERAL HOSPITAL   (Taiwan)

^h NATIONAL CENTRAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; PROTEIN LAMINB1; PROTEIN SEPT12; SPERM ASSOCIATED ANTIGEN 4; UNCLASSIFIED DRUG; CARRIER PROTEIN; LAMIN B; LAMIN B1; PROTEIN BINDING; SEPT12 PROTEIN, HUMAN; SEPTIN; SPAG4 PROTEIN, HUMAN;

ARTICLE; CELL NUCLEUS MEMBRANE; CENTROSOME; COMPLEX FORMATION; CONTROLLED STUDY; DNA DAMAGE; EMBRYO; GERM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPERMATID; SPERMATOGENESIS; SPERMATOZOON; CYTOLOGY; MEIOSIS; METABOLISM;

MUS;

CARRIER PROTEINS; HUMANS; LAMIN TYPE B; MALE; MEIOSIS; NUCLEAR ENVELOPE; PROTEIN BINDING; SEPTINS; SPERMATOGENESIS; SPERMATOZOA;

EID: 84924973730     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120722     Document Type: Article

References (47)

1. WHO (1992) World Health Organization: Laboratory manual for the Examination of Human Semen and Semen-Cervical. Mucus Interaction. 1992;3-21 p.
2. Palermo G, Joris H, Devroey P, Van Steirteghem AC (1992) Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340:17-18. PMID: 1351601
3. Silber SJ (2000) Evaluation and treatment of male infertility. Clin Obstet Gynecol 43:854-888. PMID: 11100302
4. Javed M, Esfandiari N, Casper RF (2010) Failed fertilization after clinical intracytoplasmic sperm injection. Reprod Biomed Online 20:56-67. doi: 10.1016/j.rbmo.2009.10.010 PMID: 20158989
5. Mostowy S, Cossart P (2012) Septins: the fourth component of the cytoskeleton. Nat Rev Mol Cell Biol 13:183-194. doi: 10.1038/nrm3284 PMID: 22314400
6. Sirajuddin M, Farkasovsky M, Hauer F, Kuhlmann D, Macara IG, et al. (2007) Structural insight into filament formation by mammalian septins. Nature 449:311-315. PMID: 17637674
7. Kinoshita M, Field CM, Coughlin ML, Straight AF, Mitchison TJ (2002) Self- and actin-templated assembly of Mammalian septins. Dev Cell 3:791-802. PMID: 12479805
8. Hall PA, Jung K, Hillan KJ, Russell SE (2005) Expression profiling the human septin gene family. J Pathol 206:269-278. PMID: 15915442
9. Hall PA, Russell SE (2004) The pathobiology of the septin gene family. J Pathol 204:489-505. PMID: 15495264
10. Lin YH, Kuo YC, Chiang HS, Kuo PL (2011) The role of the septin family in spermiogenesis. Spermatogenesis 1:298-302. PMID: 22332113
11. Ihara M, Kinoshita A, Yamada S, Tanaka H, Tanigaki A, et al. (2005) Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev Cell 8:343-352. PMID: 15737930
12. Kissel H, Georgescu MM, Larisch S, Manova K, Hunnicutt GR, et al. (2005) The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev Cell 8:353-364. PMID: 15737931
13. Lhuillier P, Rode B, Escalier D, Lores P, Dirami T, et al. (2009) Absence of annulus in human asthenozoospermia: case report. Hum Reprod 24:1296-1303. doi: 10.1093/humrep/dep020 PMID: 19221096
14. Sugino Y, Ichioka K, Soda T, Ihara M, Kinoshita M, et al. (2008) Septins as diagnostic markers for a subset of human asthenozoospermia. J Urol 180:2706-2709. doi: 10.1016/j.juro.2008.08.005 PMID: 18951558
15. Lin YH, Lin YM, Wang YY, Yu IS, Lin YW, et al. (2009) The expression level of septin12 is critical for spermiogenesis. Am J Pathol 174:1857-1868. doi: 10.2353/ajpath.2009.080955 PMID: 19359518
16. Lin YH, Lin YM, Teng YN, Hsieh TY, Lin YS, et al. (2006) Identification of ten novel genes involved in human spermatogenesis by microarray analysis of testicular tissue. Fertil Steril 86:1650-1658. PMID: 17074343
17. Lin YH, Chou CK, Hung YC, Yu IS, Pan HA, et al. (2011) SEPT12 deficiency causes sperm nucleus damage and developmental arrest of preimplantation embryos. Fertil Steril 95:363-365. doi: 10.1016/j.fertnstert.2010.07.1064 PMID: 20801438
18. Kuo YC, Lin YH, Chen HI, Wang YY, Chiou YW, et al. (2012) SEPT12 mutations cause male infertility with defective sperm annulus. Hum Mutat 33:710-719. doi: 10.1002/humu.22028 PMID: 22275165
19. Lin YH, Wang YY, Chen HI, Kuo YC, Chiou YW, et al. (2012) SEPTIN12 genetic variants confer susceptibility to teratozoospermia. PLoS One 7:e34011. doi: 10.1371/journal.pone.0034011 PMID: 22479503
20. Kuo PL, Chiang HS, Wang YY, Kuo YC, Chen MF, et al. (2013) SEPT12-Microtubule Complexes Are Required for Sperm Head and Tail Formation. Int J Mol Sci 14:22102-22116. doi: 10.3390/ijms141122102 PMID: 24213608
21. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, et al. (2009) SUN1/2 and Syne/Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64:173-187. doi: 10.1016/j.neuron. 2009.08.018 PMID: 19874786
22. Crisp M, Liu Q, Roux K, Rattner JB, Shanahan C, et al. (2006) Coupling of the nucleus and cytoplasm: role of the LINC complex. J Cell Biol 172:41-53. PMID: 16380439
23. Haque F, Lloyd DJ, Smallwood DT, Dent CL, Shanahan CM, et al. (2006) SUN1 interacts with nuclear lamin A and cytoplasmic nesprins to provide a physical connection between the nuclear lamina and the cytoskeleton. Mol Cell Biol 26:3738-3751. PMID: 16648470
24. Padmakumar VC, Libotte T, Lu W, Zaim H, Abraham S, et al. (2005) The inner nuclear membrane protein Sun1 mediates the anchorage of Nesprin-2 to the nuclear envelope. J Cell Sci 118:3419-3430. PMID: 16079285
25. Ding X, Xu R, Yu J, Xu T, Zhuang Y, et al. (2007) SUN1 is required for telomere attachment to nuclear envelope and gametogenesis in mice. Dev Cell 12:863-872. PMID: 17543860
26. Chi YH, Cheng LI, Myers T, Ward JM, Williams E, et al. (2009) Requirement for Sun1 in the expression of meiotic reproductive genes and piRNA. Development 136:965-973. doi: 10.1242/dev. 029868 PMID: 19211677
27. Gob E, Schmitt J, Benavente R, Alsheimer M (2010) Mammalian sperm head formation involves different polarization of two novel LINC complexes. PLoS One 5:e12072. doi: 10.1371/journal.pone. 0012072 PMID: 20711465
28. Kracklauer MP, Wiora HM, Deery WJ, Chen X, Bolival B Jr., et al. (2010) The Drosophila SUN protein Spag4 cooperates with the coiled-coil protein Yuri Gagarin to maintain association of the basal body and spermatid nucleus. J Cell Sci 123:2763-2772. doi: 10.1242/jcs.066589 PMID: 20647369
29. Frohnert C, Schweizer S, Hoyer-Fender S (2011) SPAG4L/SPAG4L-2 are testis-specific SUN domain proteins restricted to the apical nuclear envelope of round spermatids facing the acrosome. Mol Hum Reprod. 17:207-18 doi: 10.1093/molehr/gaq099 PMID: 21159740
30. Shao X, Tarnasky HA, Lee JP, Oko R, Van Der Hoorn FA (1999) Spag4, a novel sperm protein, binds outer dense-fiber protein Odf1 and localizes to microtubules of manchette and axoneme. Dev Biol 211:109-123. PMID: 10373309
31. Hasan S, Guttinger S, Muhlhausser P, Anderegg F, Burgler S, et al. (2006) Nuclear envelope localization of human UNC84A does not require nuclear lamins. FEBS Lett 580:1263-1268. PMID: 16445915
32. Hsu CC, Lee YC, Yeh SH, Chen CH, Wu CC, et al. (2012) 58-kDa microspherule protein (MSP58) is novel Brahma-related gene 1 (BRG1)-associated protein that modulates p53/p21 senescence pathway. J Biol Chem 287:22533-22548. doi: 10.1074/jbc. M111.335331 PMID: 22563078
33. Tasi YC, Chao HC, Chung CL, Liu XY, Lin YM, et al. (2013) Characterization of 3-hydroxyisobutyrate dehydrogenase, HIBADH, as a sperm-motility marker. J Assist Reprod Genet 30:505-512. doi: 10. 1007/s10815-013-9954-8 PMID: 23423614
34. Lin YH, Lin YM, Kuo YC, Wang YY, Kuo PL (2011) Identification and characterization of a novel Rab GTPase-activating protein in spermatids. Int J Androl 34:e358-367. doi: 10.1111/j.1365-2605.2010. 01126.x PMID: 21128978
35. Chao HC, Lin YH, Kuo YC, Shen CJ, Pan HA, et al. (2010) The expression pattern of SEPT7 correlates with sperm morphology. J Assist Reprod Genet 27:299-307. doi: 10.1007/s10815-010-9409-4 PMID: 20352323
36. Tzur YB, Wilson KL, Gruenbaum Y (2006) SUN-domain proteins: 'Velcro' that links the nucleoskeleton to the cytoskeleton. Nat Rev Mol Cell Biol 7:782-788. PMID: 16926857
37. Turgay Y, Ungricht R, Rothballer A, Kiss A, Csucs G, et al. (2010) A classical NLS and the SUN domain contribute to the targeting of SUN2 to the inner nuclear membrane. EMBO J 29:2262-2275. doi: 10. 1038/emboj.2010.119 PMID: 20551905
38. Nagata K, Asano T, Nozawa Y, Inagaki M (2004) Biochemical and cell biological analyses of a mammalian septin complex, Sept7/9b/11. J Biol Chem 279:55895-55904. PMID: 15485874
39. Martinez C, Sanjuan MA, Dent JA, Karlsson L, Ware J (2004) Human septin-septin interactions as a prerequisite for targeting septin complexes in the cytosol. Biochem J 382:783-791. PMID: 15214843
40. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, et al. (2001) Haploinsufficiency of protamine-1 or -2 causes infertility in mice. Nat Genet 28:82-6. PMID: 11326282
41. Mansfeld J, Güttinger S, Hawryluk-Gara LA, Panté N, Mall M, et al., (2006) The conserved transmembrane nucleoporin NDC1 is required for nuclear pore complex assembly in vertebrate cells. Mol Cell 22:93-103. PMID: 16600873
42. Dammermann A, Merdes A (2002) Assembly of centrosomal proteins and microtubule organization depends on PCM-1. J Cell Biol 159:255-66. PMID: 12403812
43. Geisler SB, Robinson D, Hauringa M, Raeker MO, Borisov AB, et al., (2007) Obscurin-like 1, OBSL1, is a novel cytoskeletal protein related to obscurin. Genomics 89:521-31 PMID: 17289344
44. Spiliotis ET, Kinoshita M, Nelson WJ (2005) A mitotic septin scaffold required for Mammalian chromosome congression and segregation. Science 307:1781-1785. PMID: 15774761
45. Zhu M, Wang F, Yan F, Yao PY, Du J, et al. (2008) Septin 7 interacts with centromere-associated protein E and is required for its kinetochore localization. J Biol Chem 283:18916-18925. doi: 10.1074/jbc. M710591200 PMID: 18460473
46. Kremer BE, Adang LA, Macara IG (2007) Septins regulate actin organization and cell-cycle arrest through nuclear accumulation of NCK mediated by SOCS7. Cell 130:837-850. PMID: 17803907
47. Kinoshita M, Takeda S (2007) Connecting the dots between septins and the DNA damage checkpoint. Cell 130:777-779. PMID: 17803900