[1].Molecular Cloning and Putative Functions of KIFC1 for Acrosome Formation and Nuclear Reshaping during Spermiogenesis in Schlegel’s Japanese Gecko Gekko japonicus[J].Asian Herpetological Research,2019,10(3):170-182.[doi:10.16373/j.cnki.ahr.180080]
　Shuangli HAO#,Liyue ZHANG#,Jun PING,et al.Molecular Cloning and Putative Functions of KIFC1 for Acrosome Formation and Nuclear Reshaping during Spermiogenesis in Schlegel’s Japanese Gecko Gekko japonicus[J].Asian Herpetological Research(AHR),2019,10(3):170-182.[doi:10.16373/j.cnki.ahr.180080]
点击复制

Molecular Cloning and Putative Functions of KIFC1 for Acrosome Formation and Nuclear Reshaping during Spermiogenesis in Schlegel’s Japanese Gecko Gekko japonicus()
分享到：

Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

卷:
10
期数:
2019年3期
页码:
170-182
栏目:
出版日期:
2019-09-23

文章信息/Info

Title:
Molecular Cloning and Putative Functions of KIFC1 for Acrosome Formation and Nuclear Reshaping during Spermiogenesis in Schlegel’s Japanese Gecko Gekko japonicus
文章编号:
AHR-2018-0080
Author(s):
Shuangli HAO1#;  Liyue ZHANG2#;  Jun PING1;  Xiaowen WU1;  Jianrao HU3 and Yongpu ZHANG1*
1 College of Life and Environmental Sciences, Wenzhou University, Wenzhou 325035, China
2 College of Medicine, Zhejiang University, Hangzhou 310058, China
3 College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou 310036, China
Keywords:
Spermiogenesis;  KIFC1;  Kinesin;  Gekko japonicus
DOI:
10.16373/j.cnki.ahr.180080
Abstract:
Spermiogenesis, occurring in the male testis, is a complicated and highly-ordered developmental process resulting in the production of fertile mature sperm. In Gekko japonicus, this process occurs in 7 steps during which the spermatids undergo dramatic changes in the cytoskeleton and nucleus. Here, we cloned and sequenced the cDNA of the mammalian KIFC1 homologue in the testis of G. japonicus. The 2 344 bp full-length cDNA sequence contained a 191 bp 5’-untranslated region, a 134 bp 3’-untranslated region and a 2 019 bp open reading frame encoding a protein of 672 amino acids. Tissue expression analysis revealed the highest expression of kifc1 mRNA was in the testis. Fluorescence in situ hybridization revealed that the kifc1 mRNA signal was hardly detected in step 1 spermatids but became concentrated at the acrosome of step 2 spermatids and abundant in the nucleus of step 5 spermatids where the nucleus then undergoes dramatic elongation and compression. The kifc1 mRNA signal then gradually disappears in mature sperm. This expression of KIFC1 at specific stages of spermiogenesis in G. japonicus implies its important role in the major cytological transformations such as acrosome biogenesis and nucleus morphogenesis.

参考文献/References:

Ambrish R., Alper K., Yang Z. 2010. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc, 5: 725–738
Chennathukuzhi V., Morales C. R., El-Alfy M., Hecht N. B. 2003. The kinesin KIF17b and RNA-binding protein TB-RBP transport specific cAMP responsive element modulator-regulated mRNAs inmale germ cells. Proc Natl Acad Sci USA, 100: 15566–15571
Dang R., Zhu J. Q., Tan F. Q., Wang W., Zhou H., Yang W. X. 2012. Molecular characterization of a KIF3B-like kinesin gene in the testis of Octopus tankahkeei (Cephalopoda, Octopus). Mol Biol Rep, 39: 5589–5598
Gao X. M., Mu D. L., Hou C. C., Zhu J. Q., Jin S., Wang C. L. 2019. Expression and putative functions of KIFC1 for nuclear reshaping and midpiece formation during spermiogenesis of Phascolosoma esculenta. Gene, 683:169–183
Gribbins K. M. 2011. Reptilian spermatogenesis: A histological and ultrastructural perspective. Spermatogenesis, 1: 250–269
Helfand B. T., Mikami A., Vallee R. B. Goldman R. D. 2002. A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J Cell Biol, 157: 795–806
Hermo L., Pelletier R. M., Cyr D. G., Smith C. E. 2010. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 2: changes in spermatid organelles associated with development of spermatozoa. Microsc Res Tech, 73: 279–319
Hess R. A., de Renato F. L. 2008. Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol, 636: 1–15
Hirokawa N., Noda Y., Tanaka Y., Niwa S. 2009. Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol, 10: 682–696
Hu J. R., Liu M., Wang D. H., Hu Y. J., Tan F. Q., Yang W. X. 2013. Molecular characterization and expression analysis of a KIFC1-like kinesin gene in the testis of Eumeces chinensis. Mol Biol Rep, 40: 6645–6655
Hu J. R., Xu N., Tan F. Q., Wang D. H., Liu M., Yang W. X. 2012. Molecular characterization of a KIF3A-like kinesin gene in the testis of the Chinese fire-bellied newt Cynops orientalis. Mol Biol Rep, 39: 4207–4214
Karki S., Ligon L. A., Desantis J., Holzbaur E. L. F. 2002. PLAC-24 is a cytoplasmic dyneinbinding protein that is recruited to sites of cell-cell contact. Mol Biol Cell, 13: 1722–1734
Kikkawa M. 2008. The role of microtubules in processive kinesin movement. Trends Cell Biol, 18: 128–135
Kotaja N., de Cesare D., Macho B., Monaco l., Brancorsini S., Goossens E., Tournaye H., Gansmuller A., Sassone-Corsi P. 2004. Abnormal sperm in mice with targeted deletion of the act (activator of cAMP-responsive element modulator in testis) gene. Proc Natl Acad Sci USA, 101: 10620–10625
Lawrence C. J., Dawe R. K., Christie K. R. Cleveland D. W., Dawson S. C., Endow S. A., Goldstein L. S. B., Goodson H. V., Hirokawa N., Howard J., Malmberg R. L., Mchntosh R., Miki H., Mitchison T. J., Okada Y., Reddy A. S. N., Saxton W. M., Schliwa M., Scholey J. M., Vale r. d., Walczak C. E., Wordeman L. 2004. A standardized kinesin nomenclature. J Cell Biol, 167: 19–22
Lehti M. S., Kotaj N., Sironen A. 2013. KIF3A is essential for sperm tail formation and manchette function. Mol Cell Endocrinol, 377: 44–55
Leopold P. L., McDowall A. W., Pfister K. K., Bloom G. S., Brady S. T. 1992. Association of kinesin with characterized membrane-bound organelles. Cell Motil Cytoskeleton, 23: 19–33
Liu X. S., Zhao X. D., Wang X., Yao Y. X., Zhang L. L., Shu R. Z., Ren W. H., Huang Y., Gu M. M., Kuang Y., Wang L., Lu S. Y., Chi J., Fen J.S., Wang Y. F., Fei J., Dai W., Wang Z. G. 2010. Germinal cell aplasia in Kif18a mutant male mice due to impaired chromosome congression and dysregulated BubRI and CENP-E. Genes Cancer, 1: 26–39
Ma D. D., Bi L., Yang W. X. 2017. KIFC1 is essential for acrosome formation and nuclear shaping during spermiogenesis in the lobster Procambarus clarkii. Oncotarget, 8(22): 36082–36098
Ma D. D., Pan M. Y., Hou C. C., Tan F. Q., Yang W. X. 2017. KIFC1 and myosin Va: two motors for acrosomal biogenesis and nuclear shaping during spermiogenesis of Portunus trituberculatus. Cell Tissue Res, 369(3): 625–640
Mannowetz N., Kartarius S., Wennemuth G., Montenarh M. 2010. Protein kinase CK2 and new binding partners during spermatogenesis. Cell Mol Life Sci, 67: 3905–3913
Mountain V., Simerly C., Howard L., Ando A., Schatten G., Compton D. A.1999. The kinesin-related protein, HSET, opposes the activity of Eg5 and cross-links microtubules in the mammalian mitotic spindle. J Cell Biol, 147: 351–365
Moreno R. D., Ramalho-Santos J., Sutovsky P., Chan E. K., Schatten G. 2000. Vesicular traffic and golgi apparatus dynamics during mammalian spermatogenesis: implications for acrosome architecture. Biol Reprod, 63: 89–98
Nath S., Bananis E., Sarkar S., Stockert R. J., Sperry A. O., Murray J. W., Wolkoff A. W. 2007. Kif5B and KIFC1 interact and are required for motility and fission of early endocytic vesicles in mouse liver. Mol Biol Cell, 18: 1839–1849
Navolanic P. M., SperryA. O. 2000. Identification of isoforms of a mitotic motor in mammalian spermatogenesis. Biol Reprod, 62: 1360–1369
Nonaka S., Shiratori H., Saijoh Y., Hmada H. 2002. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature, 418: 96–99
Qin H., Rosenbaum J. L., Barr M. M. 2001. An autosomal recessive polycystic kidney disease gene homolog is involved in intraflagellar transport in C. elegans ciliated sensory neurons. Curr Biol, 11: 457–461
Russell L. D., Hikim S. A. P., Ettlin R. A., Clegg E. D. 1990. Histological and histopathological evaluation of the testis. Clearwater Fl: Cache River Press.
Shea T. B., Flanagan L. A. 2001. Kinesin, dynein and neurofilament transport. Trends Neurosci, 24: 644–648
Tan F. Q., Ma X. X., Zhu J. Q., Yang W. X. 2013. The expression pattern of the C-terminal kinesin gene kifc1 during the spermatogenesis of Sepiella maindroni. Gene, 532(1):53–62
Vaid K. S., Guttman J. A., Singaraja R. R., Vogl A. W. 2007. A kinesin is present at unique sertoli/spermatid adherens junctions in rat and mouse testes. Biol Reprod, 77: 1037–1048
Wang R., Sperry A. O. 2008. Identification of a novel leucine-rich repeat protein and candidate PP1 regulatory subunit expressed in developing spermatids. BMC Cell Biol, 9: 9
Wang D. H., Yang W. X. 2010. Molecular cloning and characterization of KIFC1-like kinesin gene (es-KIFC1) in the testis of the Chinese mitten crab Eriocheir sinensis. Comp Biochem Physiol A, 157: 123–131
Wang W., Zhu J. Q., Yu H. M., Tan F. Q., Yang W. X. 2010a. KIFC1-like motor protein associates with the cephalopod manchette and participates in sperm nuclear morphogenesis in Octopus tankahkeei. PLoS One, 5: e15616
Wang W., Zhu J. Q., Yang W. X. 2010b. Molecular cloning and characterization of KIFC1-like kinesin gene (ot-KIFC1) from Octopus tankahkeei. Comp Biochem Physiol B, 156: 174–182
Wang W., Dang R., Zhu J. Q., Yang W. X. 2010c. Identification and dynamic transcription of KIF3A homologue gene in spermiogenesis of Octopus tankahkeei. Comp Biochem Physiol A, 157: 237–245
Wang Y. T., Mao H., Hou C. C., Sun X., Wang D. H., Zhou H., Yang W. X. 2012. Characterization and expression pattern of KIFC1-like kinesin gene in the testis of the Macrobrachium nipponense with discussion of its relationship with structure lamellar complex (LCx) and acroframosome (AFS). Mol Biol Rep, 39: 7591–7598
Watters J. W., Dewar K., Lehoczky J., Boyartchuk V., Dietrich W. F. 2001. Kif1C, a kinesin-like motor protein, mediates mouse macrophage resistance to anthrax lethal factor. Curr Biol, 11: 1503–1511
Yang W. X. 2007. Ultrastructural analysis of kinesin-related motor proteins during spermatogenesis. Methods Mol Biol, 392: 133–141
Yang W. X., Jefferson H., Sperry A. O. 2006. The molecular motor KIFC1 associates with a complex containing nucleoporin NUP62 that is regulated during development and by the small GTPase RAN. Biol Reprod, 74: 684–690
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
Yoshinaga K., Toshimori K. 2003. Organization and modifications of sperm acrosomal molecules during spermatogenesis and epididymal maturation. Microsc Res Tech, 61: 39–45
Yu K., HouL., Zhu J. Q., Ying X. P., Yang W. X. 2009. KIFC1 participates in acrosomal biogenesis, with discussion of its importance for the perforatorium in the Chinese mitten crab Eriocheir sinensis. Cell Tissue Res, 337: 113–123
Zhang C., Niu Y., Liu J. 2014. Functions and regulatory mechanisms of vesicular transport. Chin J Cell Biol, 36:1218–1226
Zhang D. D., Gao X. M., Zhao Y. Q., Hou C. C., Zhu J. Q. 2017. The C-terminal kinesin motor KIFC1 may participate in nuclear reshaping and flagellum formation during spermiogenesis of Larimichthys crocea. Fish Physiol Biochem, 43(5):1351–1371
Zhang Y. G., Sperry A. O. 2004. Comparative analysis of two C-terminal kinesin motor proteins: KIFC1 and KIFC5A. Cell Motil Cytoskeleton, 58:213–230
Zhu C. J., Zhao J., Bibikova M., Leverson J. D., Bossy-Wetzel E., Fan J. B., Abranham R. T., Jiang W. 2005. Functional analysis of human microtubule-based motor proteins, the kinesins and dyneins, in mitosis/cytokinesis using RNA interference. Mol Biol Cell, 16: 3187–3199
Zou Y., Millette C. F., Sperry A. O. 2002. KRP3A and KRP3B: candidate motors in spermatid maturation in the seminiferous epithelium. Biol Reprod, 66: 843–855

更新日期/Last Update: 2019-09-25