Abstract
KIF3A and KIF3B are two N-terminal motor proteins belonging to the kinesin-II superfamily that play essential roles in spermiogenesis. To understand the roles played by KIF3A/3B during spermatogenesis of large yellow croaker Larimichthys crocea, we studied the testis characteristics at different developmental stages of L. crocea, and determined the spatiotemporal expression patterns of kif3a and kif3b during spermiogenesis. Quantitative real-time PCR (qRT-PCR) showed that the overall trends of kif3a/3b mRNA abundance during testis development are similar. From stage II to stage V, kif3a/3b mRNA abundances first increased and then fell after reaching a peak at stage IV. Interestingly, the mRNA abundances of both genes at stage V were higher than those at stages II and III. In addition, it is worth of noting that kif3b mRNA abundance was higher than that of kif3a at all stages. Fluorescence in situ hybridization results revealed that kif3a/3b mRNA abundance dynamics were consistent with the migration of mitochondria, the deformation of nucleus, and the formation of tail. The mRNA hybridization signals of both genes first appeared either around the nuclear periphery or on the side of the nuclei, then appeared at one side of nuclei, and finally were mainly on the tail during spermiogenesis. Our findings contributed to better understanding the molecular mechanisms of spermiogenesis in fish; and suggested that KIF3A and KIF3B may participate in the intracellular transport of mitochondria, nuclear deformation, and the formation of tail during the spermiogenesis in L. crocea.
Similar content being viewed by others
References
Berezuk, M. A., and Schroer, T. A., 2004. Fractionation and characterization of kinesin ii species in vertebrate brain. Traffic, 5 (7): 503–513.
Bot, N. L., Antony, C., White, J., Karsenti, E., and Vernos, I., 1998. Role of xklp3, a subunit of the xenopus kinesin ii heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the golgi apparatus. Journal of Cell Biology, 143 (6): 1559–1573.
Braubach, P., Lippmann, T., Raoult, D., Lagier, J. C., Anagnostopoulos, I., Zender, S., Länger, F. P., Kreipe, H. H., Kühnel, M. P., and Jonigk, D., 2017. Fluorescencein situhybridization for diagnosis of Whipple’s disease in formalin-fixed paraffin-embedded tissue. Frontiers in Medicine, 4: 87.
Brown, C. L., Maier, K. C., Stauber, T., Ginkel, L. M., Wordeman, L., Vernos, I., and Schroer, T. A., 2010. Kinesin-2 is a motor for late endosomes and lysosomes. Traffic, 6 (12): 1114–1124.
Campbell, P. D., and Marlow, F. L., 2013. Temporal and tissue specific gene expression patterns of the zebrafish kinesin-1 heavy chain family, kif5s, during development. Gene Expression Patterns, 13 (7): 271–279.
Chen, H., Lin, G. W., Liu, Z. K., Chen, W., Xie, Y. Q., and Wang, X. C., 2010. Study on growth characters of cultured Pseudosciaena crocea originated from eastern fujian. Marine Sciences, 34 (11): 1–5.
Cole, D. G., Chinn, S. W., Wedaman, K. P., Hall, K., Vuong, T., and Scholey, J. M., 1993. Novel heterotrimeric kinesin-related protein purified from sea urchin eggs. Nature, 366 (6452): 268–270.
Cooke, H., Hargreave, T., and Elliott, D., 1998. Understanding the genes involved in spermatogenesis: A progress report. Fertility & Sterility, 69 (6): 989–995.
Dang, R., Zhu, J. Q., Tan, F. Q., Wang, W., Zhou, H., and Yang, W. X., 2012. Molecular characterization of a KIF3B-like kinesin gene in the testis of Octopus tankahkeei (Cephalopoda, Octopus). Molecular Biology Reports, 39 (5): 5589–5598.
De, M. V, Burkhard, P., Le, B. N., Vernos, I., and Hoenger, A., 2001. Analysis of heterodimer formation by Xklp3A/B, a newly cloned kinesin-ii from Xenopus laevis. Embo Journal, 20 (13): 3370–3379.
Dishinger, J. F., Kee, H. L., Jenkins, P. M., Fan, S., Hurd, T. W., Hammond, J. W., Truong, T. T., Margoils, B., Martens, J. R., and Verhey, K. J., 2010. Ciliary entry of the kinesin-2 motor KIF17 is regulated by importin-β2 and Ran-GTP. Nature Cell Biology, 12 (7): 703.
Duangtum, N., Junking, M., Sawasdee, N., Cheunsuchon, B., Limjindaporn, T., and Yenchitsomanus, P. T., 2011. Human kidney anion exchanger 1 interacts with kinesin family member 3B (KIF3B). Biochemical & Biophysical Research Communications, 413 (1): 69–74.
Fu, S. Y., Jiang, J. H., Yang, W. X., and Zhu, J. Q., 2016. A histological study of testis development and ultrastructural features of spermatogenesis in cultured Acrossocheilus fasciatus. Tissue & Cell, 48 (1): 49–62.
Ge, S. Q., Kang, X. J., Liu, G. R., and Mu, S. M., 2008. Genes involved in spermatogenesis. Hereditas, 30 (1): 3.
Gross, S. P., Tuma, M. C., Deacon, S. W., Serpinskaya, A. S., Reilein, A. R., and Gelfand, V. I., 2002. Interactions and regulation of molecular motors in Xenopus melanophores. Journal of Cell Biology, 156 (5): 855.
Heinrich, B., and Deshler, J., 2009. RNA localization to the balbiani body in Xenopus oocytes is regulated by the energy state of the cell and is facilitated by kinesin II. Rna-A Publication of the Rna Society, 15 (4): 524.
Henson, J. H., Cole, D. G., Roesener, C. D., Capuano, S., Mendola, R. J., and Scholey, J. M., 1997. The heterotrimeric motor protein kinesin-II localizes to the midpiece and flagellum of sea urchin and sand dollar sperm. Cell Motility & the Cytoskeleton, 38 (1): 29–37.
Hirokawa, N., 2010. Stirring up development with the heterotrimeric kinesin KIF3. Traffic, 1 (1): 29–34.
Hirokawa, N., and Noda, Y., 2008. Intracellular transport and kinesin superfamily proteins, KIFs: Structure, function, and dynamics. Physiological Reviews, 88 (3): 1089.
Hirokawa, N., and Takemura, R., 2004. Kinesin superfamily proteins and their various functions and dynamics. Experimental Cell Research, 301 (1): 50.
Hirokawa, N., and Tanaka, Y., 2015. Kinesin superfamily proteins (KIFs): Various functions and their relevance for important phenomena in life and diseases. Experimental Cell Research, 334 (1): 16–25.
Hirokawa, N., Noda, Y., and Okada, Y., 1998. Kinesin and dynein superfamily proteins in organelle transport and cell division. Current Opinion in Cell Biology, 10 (1): 60.
Hu, J. R., Xu, N., Tan, F. Q., Wang, D. H., Liu, M., and Yang, W. X., 2012. Molecular characterization of a KIF3A-like kinesin gene in the testis of the chinese fire-bellied newt Cynops orientalis. Molecular Biology Reports, 39 (4): 4207–4214.
Hu, M., Miao, L., Li, M. Y. L. I., Zhang, H., Wang, J. H., Wang, T. Z., and Pan, N., 2014. Observation and comparison on the ultrastructure of the spermatozoon of Nibea albiflora and Pseudosciaena crocea. Journal of Biology, 31 (2): 1–4 (in Chinese with English abstract).
Huszno, J., and Klag, J., 2012. The reproductive cycle in the male gonads of Danio rerio (teleostei, cyprinidae). Stereological analysis. Micron, 43 (5): 666–672.
Junco, A., Bhullar, B., Tarnasky, H. A., and Fa, V. D. H., 2001. Kinesin light-chain KLC3 expression in testis is restricted to spermatids, Biology of Reproduction, 64 (5): 1320–1330.
Le, B. N., Claude, A., Jamie, W., Eric, K., and Isabelle, V., 1998. Role of Xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the Endoplasmic Reticulum and the Golgi Apparatus. Journal of Cell Biology, 143 (6): 1559.
Lehti, M. S., Kotaja, N., and Sironen, A., 2013. KIF3A is essential for sperm tail formation and manchette function. Molecular & Cellular Endocrinology, 377 (1–2): 44.
Li, B., Qi, X. Q., Chen, X., Huang, X., Liu, G. Y., Chen, H. R., Huang, C. G., Luo, C., and Lu, Y. C., 2010. Expression of targeting protein for Xenopus kinesin-like protein 2 is associated with progression of human malignant astrocytoma. Brain Research, 1352 (1): 200–207.
Li, J. C., Jian, M. L., Jing, C., Ye, H. G., Zuo, R. Y., Dai, S. H., Zuo, M. Z., and Jia, H. S., 2003. NYD-SP16, a novel gene associated with spermatogenesis of human testis1. Biology of Reproduction, 68 (1): 190–198.
Lolkema, M. P., Mans, D. A., Snijckers, C. M., van Noort, M., van Beest, M., Voest, E. E., and Giles, R. H., 2007. The von Hippel-Lindau tumour suppressor interacts with microtubules through kinesin-2. Febs Letters, 581 (24): 4571–4576.
Lopes, V. S., Jimeno, D., Khanobdee, K., Song, X., Chen, B., Nusinowitz, S., and Williams, D. S., 2010. Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death. Molecular Biology of the Cell, 21 (23): 4076–4088.
Lu, Y., Wang, Q., Wang, D. H., Zhou, H., Hu, Y. J., and Yang, W. X., 2014. Functional analysis of kIF3A and KIF3B during spermiogenesis of Chinese mitten crab Eriocheir sinensis. PLoS One, 9 (5): e97645.
Marszalek, J. R., and Goldstein, L. S., 2000. Understanding the functions of kinesin-II. Biochimica et Biophysica Acta, 1496 (1): 142.
Morris, R. L., and Scholey, J. M., 1997. Heterotrimeric kinesin-II is required for the assembly of motile 9+2 ciliary axonemes on sea urchin embryos. Journal of Cell Biology, 138 (5): 1009.
Nishimura, T., Kato, K., Yamaguchi, T., Fukata, Y., Ohno, S., and Kaibuchi, K., 2004. Role of the PAR-3-KIF3 complex in the establishment of neuronal polarity. Nature Cell Biology, 6 (4): 328–334.
O’donnell, L., and O’bryan, M. K., 2014. Microtubules and spermatogenesis. Seminars in Cell & Developmental Biology, 30 (6): 45.
Papah, M. B., Kisia, S. M., Ojoo, R. O., Makanya, A. N., Wood, C. M., Kavembe, G. D., Maina, J. N., Johannsson, O. E., Bergman, H. L., and Laurent, P., 2013. Morphological evaluation of spermatogenesis in lake magadi tilapia (Alcolapia grahami): A fish living on the edge. Tissue & Cell, 45 (6): 371–382.
Raghupathy, R. K., Zhang, X., Alhasani, R. H., Zhou, X., Mullin, M., Reilly, J., Li, W., Liu, M., and Shu, X., 2016. Abnormal photoreceptor outer segment development and early retinal degeneration in KIF3A mutant zebrafish. Cell Biochemistry & Function, 34 (6): 429–440.
Takeda, S., Yamazaki, H., Seog, D. H., Kanai, Y., Terada, S., and Hirokawa, N., 2000. Kinesin superfamily protein 3 (KIF3A) motor transports fodrin-associating vesicles important for neurite building. Journal of Cell Biology, 148 (6): 1255–1265.
Trivedi, D., Colin, E., Louie, C. M., and Williams, D. S., 2012. Live-cell imaging evidence for the ciliary transport of rod photoreceptor opsin by heterotrimeric kinesin-2. Journal of Neuroscience the Official Journal of the Society for Neuroscience, 32 (31): 10587.
Wang, W., Dang, R., Zhu, J. Q., and Yang, W. X., 2010. Identification and dynamic transcription of KIF3A homologue gene in spermiogenesis of Octopus tankahkeei. Comparative Biochemistry & Physiology Part A Molecular & Integrative Physiology, 157 (3): 237–245.
Yamazaki, H., Nakata, T., Okada, Y., and Hirokawa, N., 1994. KIF3B forms a heterodimer with KIF3A and works as a new microtubule-based anterograde motor of membrane organelle transport. Neuroscience Research Supplements, 19: S84.
Yamazaki, H., Nakata, T., Okada, Y., and Hirokawa, N., 1996. Cloning and characterization of KAP3: A novel kinesin superfamily-associated protein of KIF3A/3B. Proceedings of the National Academy of Sciences of the United States of America, 93 (16): 8443–8448.
Yang, W. X., Jefferson, H., and 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. Biology of Reproduction, 74 (4): 684.
Yang, Z., and Goldstein, L. S., 1998. Characterization of the KIF3C neural kinesin-like motor from mouse. Molecular Biology of the Cell, 9 (2): 249.
You, Y., Lin, D., and Chen, L., 2001. Spermatogenesis of teleosts, Pseudosciaena crocea. Zoological Research, 22 (6): 461–466 (in Chinese).
Zhang, D. D., Gao, X. M., Zhao, Y. Q., Hou, C. C., and Zhu, J. Q., 2017. The C-terminal kinesin motor KIFC1 may participate in nuclear reshaping and flagellum formation during spermiogenesis of Larimichthys crocea. Fish Physiology & Biochemistry, 43 (5): 1351–1371.
Zhang, Y., Ou, Y., Cheng, M., Saadi, H. S., Thundathil, J. C., and Fa, V. D. H., 2012. KLC3 is involved in sperm tail mid-piece formation and sperm function. Developmental Biology, 366 (2): 101–110.
Zhao, C., Omori, Y., Brodowska, K., Kovach, P., and Malicki, J., 2012. Kinesin-2 family in vertebrate ciliogenesis. Proceedings of the National Academy of Sciences of the United States of America, 109 (7): 2388–2393.
Zhao, Y. Q., Yang, H. Y., Zhang, D. D., Han, Y. L., Hou, C. C., and Zhu, J. Q., 2017. Dynamic transcription and expression patterns of KIF3A and KIF3B genes during spermiogenesis in the shrimp. Palaemon carincauda. Animal Reproduction Science, 184: 59–77.
Zhou, H., Dong, Y., and Sun, Y., 2013. Detection of KIF2A mRNA in male ejaculate by real-time fluorescence quantitative RTPCR. Acta Universitatis Medicinalis Anhui, 48 (11): 1387–1390.
Zhu, J. Q., Yang, W. X., You, Z. J., Wang, W., and Jiao, H. F., 2006. Ultrastructure of spermatogenesis of Octopus tankahkeei. Journal of Fisheries of China, 4 (2): 161–169 (in Chinese with English abstract).
Zou, Y., Millette, C., and Sperry, A., 2002. KRP3A and KRP3B: Candidate motors in spermatid maturation in the seminiferous epithelium. Biology of Reproduction, 66 (3): 843–855.
Acknowledgements
We would like to acknowledge Dr. Yaru Xu for the in situ hybridization technical assistance and Mr. Youfa Wang for valuable suggestions on picture processing. This work was financially supported by the Scientific and Technical Project of Zhejiang Province (Nos. 2016C02055-7, LY18C190007), the Ningbo Natural Science Foundation (No. 2016A610081), the Scientific and Technical Project of Ningbo (No. 2015C110005), the National Natural Science Foundation of China (No. 31602140), the Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, and the K. C. Wong Magna Fund in Ningbo University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mu, D., Du, C., Fu, S. et al. Molecular Characterization, Tissue Distribution and Localization of Larimichthys crocea Kif3a and Kif3b and Expression Analysis of Their Genes During Spermiogenesis. J. Ocean Univ. China 18, 1451–1469 (2019). https://doi.org/10.1007/s11802-019-3987-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-019-3987-2