SEPT12-Microtubule complexes are required for sperm head and tail formation

International Journal of Molecular Sciences

Volumn 14, Issue 11, 2013, Pages 22102-22116

  Kuo, Pao Lin ^a   Chiang, Han Sun ^b   Wang, Ya Yun ^a   Kuo, Yung Che ^a   Chen, Mei Feng ^c   Yu, I Shing ^d   Teng, Yen Ni ^e   Lin, Shu Wha ^f   Lin, Ying Hung ^b  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^e NATIONAL UNIVERSITY OF TAINAN   (Taiwan)

^f NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

Microtubules; SEPT12; Spermiogenesis

Indexed keywords

ACTIN; ALPHA TUBULIN; BETA TUBULIN; CYTOSKELETON PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MOLECULAR MOTOR; SEPTIN; SHORT HAIRPIN RNA;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHENOSPERMIA; BINDING SITE; CELL CYCLE PROGRESSION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL POLARITY; CELL STRUCTURE; CELL VACUOLE; CHIMERA; COMPLEX FORMATION; CYTOSKELETON; EMBRYONIC STEM CELL; GENE DELETION; GENE DISRUPTION; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; GENE LOSS; GENE MUTATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; IMMUNOPRECIPITATION; IN VIVO STUDY; INFERTILITY; MALE; MICROTUBULE; MITOSIS; MOUSE; NONHUMAN; OLIGOSPERMIA; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN STRUCTURE; SEPT12 GENE; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON ABNORMALITY; SPERMATOZOON COUNT; SPERMATOZOON HEAD; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; TARGET CELL; TRANSGENIC MOUSE; VAS DEFERENS;

ANIMALS; INFERTILITY, MALE; MALE; MICE; MICROTUBULES; MULTIPROTEIN COMPLEXES; SEPTINS; SPERM HEAD; SPERM TAIL; SPERMATOGENESIS; SPERMATOZOA;

EID: 84887400317     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms141122102     Document Type: Article

References (46)

1. Hall, P.A.; Jung, K.; Hillan, K.J.; Russell, S.E. Expression profiling the human septin gene family. J. Pathol. 2005, 206, 269-278.
2. Kinoshita, M.; Field, C.M.; Coughlin, M.L.; Straight, A.F.; Mitchison, T.J. Self-and actin-templated assembly of Mammalian septins. Dev. Cell 2002, 3, 791-802.
3. Kremer, B.E.; Haystead, T.; Macara, I.G. Mammalian septins regulate microtubule stability through interaction with the microtubule-binding protein MAP4. Mol. Biol. Cell 2005, 16, 4648-4659.
4. Hall, P.A.; Russell, S.E. The pathobiology of the septin gene family. J. Pathol. 2004, 204, 489-505.
5. Lin, Y.H.; Kuo, Y.C.; Chiang, H.S.; Kuo, P.L. The role of the septin family in spermiogenesis. Spermatogenesis 2011, 1, 298-302.
6. Bi, E.; Maddox, P.; Lew, D.J.; Salmon, E.D.; McMillan, J.N.; Yeh, E.; Pringle, J.R. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 1998, 142, 1301-1312.
7. Kinoshita, M.; Kumar, S.; Mizoguchi, A.; Ide, C.; Kinoshita, A.; Haraguchi, T.; Hiraoka, Y.; Noda, M. Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures. Genes Dev. 1997, 11, 1535-1547.
8. Xie, H.; Surka, M.; Howard, J.; Trimble, W.S. Characterization of the mammalian septin H5: Distinct patterns of cytoskeletal and membrane association from other septin proteins. Cell Motil. Cytoskelet. 1999, 43, 52-62.
9. Vega, I.E.; Hsu, S.C. The septin protein Nedd5 associates with both the exocyst complex and microtubules and disruption of its GTPase activity promotes aberrant neurite sprouting in PC12 cells. Neuroreport 2003, 14, 31-37.
10. Joo, E.; Surka, M.C.; Trimble, W.S. Mammalian SEPT2 is required for scaffolding nonmuscle myosin II and its kinases. Dev. Cell 2007, 13, 677-690.
11. Spiliotis, E.T.; Kinoshita, M.; Nelson, W.J. A mitotic septin scaffold required for Mammalian chromosome congression and segregation. Science 2005, 307, 1781-1785.
12. Zhu, M.; Wang, F.; Yan, F.; Yao, P.Y.; Du, J.; Gao, X.; Wang, X.; Wu, Q.; Ward, T.; Li, J.; et al. Septin 7 interacts with centromere-associated protein E and is required for its kinetochore localization. J. Biol. Chem. 2008, 283, 18916-18925.
13. Surka, M.C.; Tsang, C.W.; Trimble, W.S. The mammalian septin MSF localizes with microtubules and is required for completion of cytokinesis. Mol. Biol. Cell 2002, 13, 3532-3545.
14. Nagata, K.; Kawajiri, A.; Matsui, S.; Takagishi, M.; Shiromizu, T.; Saitoh, N.; Izawa, I.; Kiyono, T.; Itoh, T.J.; Hotani, H.; et al. Filament formation of MSF-A, a mammalian septin, in human mammary epithelial cells depends on interactions with microtubules. J. Biol. Chem. 2003, 278, 18538-18543.
15. Greenbaum, M.P.; Ma, L.; Matzuk, M.M. Conversion of midbodies into germ cell intercellular bridges. Dev. Biol. 2007, 305, 389-396.
16. Ihara, M.; Kinoshita, A.; Yamada, S.; Tanaka, H.; Tanigaki, A.; Kitano, A.; Goto, M.; Okubo, K.; Nishiyama, H.; Ogawa, O.; et al. Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev. Cell 2005, 8, 343-352.
17. Kissel, H.; Georgescu, M.M.; Larisch, S.; Manova, K.; Hunnicutt, G.R.; Steller, H. The Sept4 septin locus is required for sperm terminal differentiation in mice. Dev. Cell 2005, 8, 353-364.
18. Steels, J.D.; Estey, M.P.; Froese, C.D.; Reynaud, D.; Pace-Asciak, C.; Trimble, W.S. Sept12 is a component of the mammalian sperm tail annulus. Cell Motil. Cytoskelet. 2007, 64, 794-807.
19. Lhuillier, P.; Rode, B.; Escalier, D.; Lores, P.; Dirami, T.; Bienvenu, T.; Gacon, G.; Dulioust, E.; Toure, A. Absence of annulus in human asthenozoospermia: Case report. Hum. Reprod. 2009, 24, 1296-1303.
20. Sugino, Y.; Ichioka, K.; Soda, T.; Ihara, M.; Kinoshita, M.; Ogawa, O.; Nishiyama, H. Septins as diagnostic markers for a subset of human asthenozoospermia. J. Urol. 2008, 180, 2706-2709.
21. Lin, Y.H.; Lin, Y.M.; Teng, Y.N.; Hsieh, T.Y.; Lin, Y.S.; Kuo, P.L. Identification of ten novel genes involved in human spermatogenesis by microarray analysis of testicular tissue. Fertil Steril 2006, 86, 1650-1658.
22. Lin, Y.H.; Lin, Y.M.; Wang, Y.Y.; Yu, I.S.; Lin, Y.W.; Wang, Y.H.; Wu, C.M.; Pan, H.A.; Chao, S.C.; Yen, P.H.; et al. The expression level of septin12 is critical for spermiogenesis. Am. J. Pathol. 2009, 174, 1857-1868.
23. Lin, Y.H.; Chou, C.K.; Hung, Y.C.; Yu, I.S.; Pan, H.A.; Lin, S.W.; Kuo, P.L. SEPT12 deficiency causes sperm nucleus damage and developmental arrest of preimplantation embryos. Fertil Steril 2011, 95, 363-365.
24. Kuo, Y.C.; Lin, Y.H.; Chen, H.I.; Wang, Y.Y.; Chiou, Y.W.; Lin, H.H.; Pan, H.A.; Wu, C.M.; Su, S.M.; Hsu, C.C.; et al. SEPT12 mutations cause male infertility with defective sperm annulus. Hum. Mutat. 2012, 33, 710-719.
25. Lin, Y.H.; Wang, Y.Y.; Chen, H.I.; Kuo, Y.C.; Chiou, Y.W.; Lin, H.H.; Wu, C.M.; Hsu, C.C.; Chiang, H.S.; Kuo, P.L. SEPTIN12 genetic variants confer susceptibility to teratozoospermia. PLoS One 2012, 7, e34011.
26. Mochida, K.; Tres, L.L.; Kierszenbaum, A.L. Isolation of the rat spermatid manchette and its perinuclear ring. Dev. Biol. 1998, 200, 46-56.
27. Moreno, R.D.; Schatten, G. Microtubule configurations and post-translational alpha-tubulin modifications during mammalian spermatogenesis. Cell Motil. Cytoskelet. 2000, 46, 235-246.
28. Tachibana, M.; Terada, Y.; Murakawa, H.; Murakami, T.; Yaegashi, N.; Okamura, K. Dynamic changes in the cytoskeleton during human spermiogenesis. Fertil Steril 2005, 84, 1241-1248.
29. Cole, A.; Meistrich, M.L.; Cherry, L.M.; Trostle-Weige, P.K. Nuclear and manchette development in spermatids of normal and azh/azh mutant mice. Biol. Reprod. 1988, 38, 385-401.
30. Russell, L.D.; Russell, J.A.; MacGregor, G.R.; Meistrich, M.L. Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am. J. Anat. 1991, 192, 97-120.
31. Kierszenbaum, A.L. Spermatid manchette: Plugging proteins to zero into the sperm tail. Mol. Reprod. Dev. 2001, 59, 347-349.
32. Kierszenbaum, A.L. Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol. Reprod. Dev. 2002, 63, 1-4.
33. Kierszenbaum, A.L.; Rivkin, E.; Tres, L.L. Molecular biology of sperm head shaping. Soc. Reprod. Fertil. Suppl. 2007, 65, 33-43.
34. Qi, Y.; Jiang, M.; Yuan, Y.; Bi, Y.; Zheng, B.; Guo, X.; Huang, X.; Zhou, Z.; Sha, J. ADP-ribosylation factor-like 3, a manchette-associated protein, is essential for mouse spermiogenesis. Mol. Hum. Reprod. 2013, 19, 327-335.
35. Bao, J.; Zhang, J.; Zheng, H.; Xu, C.; Yan, W. UBQLN1 interacts with SPEM1 and participates in spermiogenesis. Mol. Cell. Endocrinol. 2010, 327, 89-97.
36. Mochida, K.; Tres, L.L.; Kierszenbaum, A.L. Structural and biochemical features of fractionated spermatid manchettes and sperm axonemes of the azh/azh mutant mouse. Mol. Reprod. Dev. 1999, 52, 434-444.
37. Lin, Y.H.; Lin, Y.M.; Kuo, Y.C.; Wang, Y.Y.; Kuo, P.L. Identification and characterization of a novel Rab GTPase-activating protein in spermatids. Int. J. Androl. 2011, 34, e358-e367.
38. Hall, P.A.; Russell, S.E. Mammalian septins: Dynamic heteromers with roles in cellular morphogenesis and compartmentalization. J. Pathol. 2012, 226, 287-299.
39. Silverman-Gavrila, R.V.; Silverman-Gavrila, L.B. Septins: New microtubule interacting partners. Sci. World J. 2008, 8, 611-620.
40. Hanai, N.; Nagata, K.; Kawajiri, A.; Shiromizu, T.; Saitoh, N.; Hasegawa, Y.; Murakami, S.; Inagaki, M. Biochemical and cell biological characterization of a mammalian septin, Sept11. FEBS Lett. 2004, 568, 83-88.
41. Spiliotis, E.T.; Hunt, S.J.; Hu, Q.; Kinoshita, M.; Nelson, W.J. Epithelial polarity requires septin coupling of vesicle transport to polyglutamylated microtubules. J. Cell Biol. 2008, 180, 295-303.
42. Hu, J.; Bai, X.; Bowen, J.R.; Dolat, L.; Korobova, F.; Yu, W.; Baas, P.W.; Svitkina, T.; Gallo, G.; Spiliotis, E.T. Septin-driven coordination of actin and microtubule remodeling regulates the collateral branching of axons. Curr. Biol. CB 2012, 22, 1109-1115.
43. Bowen, J.R.; Hwang, D.; Bai, X.; Roy, D.; Spiliotis, E.T. Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J. Cell Biol. 2011, 194, 187-197.
44. Walenta, J.H.; Didier, A.J.; Liu, X.; Kramer, H. The Golgi-associated hook3 protein is a member of a novel family of microtubule-binding proteins. J. Cell Biol. 2001, 152, 923-934.
45. Mendoza-Lujambio, I.; Burfeind, P.; Dixkens, C.; Meinhardt, A.; Hoyer-Fender, S.; Engel, W.; Neesen, J. The Hook1 gene is non-functional in the abnormal spermatozoon head shape (azh) mutant mouse. Hum. Mol. Genet. 2002, 11, 1647-1658.
46. Kierszenbaum, A.L.; Tres, L.L. Bypassing natural sperm selection during fertilization: The azh mutant offspring experience and the alternative of spermiogenesis in vitro. Mol. Cell. Endocrinol. 2002, 187, 133-138.