Evidence for the role of KIF17 in fish spermatid reshaping: expression pattern of KIF17 in <i>Larimichthys polyactis</i> spermiogenesis -- Journal of Oceanology and Limnology,2021,39(6):2322-2335

	Cite this paper:
	Jingqian WANG, Xinming GAO, Xuebin ZHENG, Chen DU, Congcong HOU, Qingping XIE, Bao LOU, Feng LIU, Shan JIN, Junquan ZHU. Evidence for the role of KIF17 in fish spermatid reshaping: expression pattern of KIF17 in Larimichthys polyactis spermiogenesis[J]. Journal of Oceanology and Limnology, 2021, 39(6): 2322-2335

Evidence for the role of KIF17 in fish spermatid reshaping: expression pattern of KIF17 in Larimichthys polyactis spermiogenesis

Jingqian WANG¹, Xinming GAO¹, Xuebin ZHENG¹, Chen DU¹, Congcong HOU¹, Qingping XIE², Bao LOU², Feng LIU², Shan JIN¹, Junquan ZHU¹

1 Key Laboratory of Applied Marine Biotechnology by the Ministry of Education, School of Marine Sciences, Ningbo University, Ningbo 315211, China;
2 Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China

Abstract:

The homodimeric kinesin-2 protein KIF17 functions in intracellular transport and spermiogenesis in mammals. However, its role in fish spermiogenesis has not been reported. Here, we aimed to clone full-length kif17 cDNA and determine the molecular characteristics and expression patterns of KIF17 in Larimichthys polyactis spermiogenesis. The full-length cDNA of L. polyactis kif17 (Lp-kif17) was sequenced and found to contain a 332-bp 5' untranslated region, 480-bp 3' untranslated region, and 2 433-bp open reading frame encoding 810 amino acids. Bioinformatics analyses showed that L. polyactis KIF17 (Lp-KIF17) shared high sequence similarity with homologs in other animals and possessed an N-terminal motor domain with microtubule-binding sites and adenosine triphosphate (ATP) hydrolysis sites, a stalk domain containing two coiled-coil regions, and a C-terminal tail domain. The Lp-kif17 mRNA was widely expressed in various tissues, with the highest level in the brain, followed by that in the testis. Fluorescence in situ hybridization (FISH) analysis revealed that Lp-kif17 was continuously expressed in spermiogenesis, showing that it had potential functions in this process. Using immunofluorescence (IF) analysis, we found that Lp-KIF17 colocalized with tubulin and was transferred from the perinuclear cytoplasm to the side of spermatid where the tail forms during spermiogenesis. These findings suggested that KIF17 is involved in L. polyactis spermiogenesis. In particular, it may participate in nuclear shaping and tail formation by interacting with perinuclear microtubules during spermatid reshaping. In addition to providing evidence for the role of KIF17 in fish spermatid reshaping, this study provides important data for studies of reproductive biology in L. polyactis.

Key words: KIF17|spermiogenesis|Larimichthys polyactis|spermatid reshaping

Received: 2020-08-23 Revised: 2020-10-27

Tools

PDF (3233 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by Jingqian WANG

Articles by Xinming GAO

Articles by Xuebin ZHENG

Articles by Chen DU

Articles by Congcong HOU

Articles by Qingping XIE

Articles by Bao LOU

Articles by Feng LIU

Articles by Shan JIN

Articles by Junquan ZHU

References:
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 modulatorregulated mRNAs in male germ cells. Proceedings of the National Academy of Sciences of the United States of America, 100(26):15566-15571, https://doi.org/10.1073/pnas.2536695100.
Chu P J, Rivera J F, Arnold D B. 2006. A role for KIF17 in transport of Kv4.2. Journal of Biological Chemistry, 281(1):365-373, https://doi.org/10.1074/jbc.M508897200.
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, https://doi.org/10.1016/j.gene.2018.10.021.
Grüter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber B K, Izaurralde E. 1998. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Molecular Cell, 1(5):649-659, https://doi.org/10.1016/S1097-2765(00)80065-9.
Hammond J W, Blasius T L, Soppina V, Cai D W, Verhey K J. 2010. Autoinhibition of the kinesin-2 motor KIF17 via dual intramolecular mechanisms. The Journal of Cell Biology, 189(6):1013-1025, https://doi.org/10.1083/jcb. 201001057.
Hirokawa N, Noda Y, Tanaka Y, Niwa S. 2009. Kinesin superfamily motor proteins and intracellular transport. Nature Reviews Molecular Cell Biology, 10(10):682-696, https://doi.org/10.1038/nrm2774.
Imanishi M, Endres N F, Gennerich A, Vale R D. 2006. Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. The Journal of Cell Biology, 174(7):931-937, https://doi.org/10.1083/jcb. 200605179.
Insinna C, Humby M, Sedmak T, Wolfrum U, Besharse J C. 2009. Different roles for KIF17 and kinesin Ⅱ in photoreceptor development and maintenance. Developmental Dynamics, 238(9):2211-2222, https://doi.org/10.1002/dvdy.21956.
Kang H W, Chung E Y, Chung J S, Lee K Y. 2013. Ultrastructural studies of spermatogenesis and the functions of Leydig cells and Sertoli cells associated with spermatogenesis in Larimichthys polyactis (Teleostei, Perciformes, Sciaenidae). Animal Cells and Systems, 17(4):250-258, https://doi.org/10.1080/19768354.2013.829783.
Kayadjanian N, Lee H S, Pina-Crespo J, Heinemann S F. 2007. Localization of glutamate receptors to distal dendrites depends on subunit composition and the kinesin motor protein KIF17. Molecular and Cellular Neuroscience, 34(2):219-230, https://doi.org/10.1016/j.mcn.2006.11.001.
Kierszenbaum A L, Tres L L. 2004. The acrosomeacroplaxome-manchette complex and the shaping of the spermatid head. Archives of Histology and Cytology, 67(4):271-284, https://doi.org/10.1679/aohc.67.271.
Kierszenbaum A L. 2001. Spermatid manchette:plugging proteins to zero into the sperm tail. Molecular Reproduction and Development, 59(4):347-349, https://doi.org/10.1002/mrd.1040.
Kierszenbaum A L. 2002. Intramanchette transport (IMT):managing the making of the spermatid head, centrosome, and tail. Molecular Reproduction and Development, 63(1):1-4, https://doi.org/10.1002/mrd.10179.
Kimmins S, Kotaja N, Fienga G, Kolthur U S, Brancorsini S, Hogeveen K, Monaco L, Sassone-Corsi P. 2004. A specific programme of gene transcription in male germ cells. Reproductive Biomedicine Online, 8(5):496-500, https://doi.org/10.1016/s1472-6483(10)61094-2.
Lehti M S, Kotaja N, Sironen A. 2013. KIF3A is essential for sperm tail formation and manchette function. Molecular and Cellular Endocrinology, 377(1-2):44-55, https://doi.org/10.1016/j.mce.2013.06.030.
Lehti M S, Sironen A. 2016. Formation and function of the manchette and flagellum during spermatogenesis. Reproduction, 151(4):R43-R54, https://doi.org/10.1530/REP-15-0310.
Ma D D, Wang D H, Yang W X. 2017. Kinesins in spermatogenesis. Biology of Reproduction, 96(2):267-276, https://doi.org/10.1095/biolreprod.116.144113.
MacAskill A F, Rinholm J E, Twelvetrees A E, ArancibiaCarcamo I L, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler J T. 2009. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron, 61(4):541-555, https://doi.org/10.1016/j.neuron.2009.01.030.
Macho B, Brancorsini S, Fimia G M, Setou M, Hirokawa N, Sassone-Corsi P. 2002. CREM-Dependent transcription in male germ cells controlled by a kinesin. Science, 298(5602):2388-2390, https://doi.org/10.1126/science. 1077265.
Miki H, Okada Y, Hirokawa N. 2005. Analysis of the kinesin superfamily:insights into structure and function. Trends in Cell Biology, 15(9):467-476, https://doi.org/10.1016/j.tcb.2005.07.006.
Milic B, Andreasson J O L, Hogan D W, Block S M. 2017. Intraflagellar transport velocity is governed by the number of active KIF17 and KIF3AB motors and their motility properties under load. Proceedings of the National Academy of Sciences of the United States of America, 114(33):E6830-E6838, https://doi.org/10.1073/pnas.1708157114.
Mochida K, Tres L L, Kierszenbaum A L. 1999. Structural and biochemical features of fractionated spermatid manchettes and sperm axonemes of the Azh/Azh mutant mouse. Molecular Reproduction and Development, 52(4):434-444, https://doi.org/10.1002/(SICI)1098-2795(199904) 52:4<434::AID-MRD13>3.0.CO;2-D.
Nakagawa T, Tanaka Y, Matsuoka E, Kondo S, Okada Y, Noda Y, Kanai Y, Hirokawa N. 1997. Identification and classification of 16 new kinesin superfamily (KIF) proteins in mouse genome. Proceedings of the National Academy of Sciences of the United States of America, 94(18):9654-9659, https://doi.org/10.1073/pnas.94.18.9654.
Olson G E, Winfrey V P. 1990. Mitochondria-cytoskeleton interactions in the sperm midpiece. Journal of Structural Biology, 103(1):13-22, https://doi.org/10.1016/1047-8477(90)90081-M.
Saade M, Irla M, Govin J, Victorero G, Samson M, Nguyen C. 2007. Dynamic distribution of Spatial during mouse spermatogenesis and its interaction with the kinesin KIF17b. Experimental Cell Research, 313(3):614-626, https://doi.org/10.1016/j.yexcr.2006.11.011.
Setou M, Nakagawa T, Seog D H, Hirokawa N. 2000. Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science, 288(5472):1796-1802, https://doi.org/10.1126/science.288.5472.1796.
Silverman M A, Leroux M R. 2009. Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends in Cell Biology, 19(7):306-316, https://doi.org/10.1016/j.tcb.2009.04.002.
Tabish M, Siddiqui Z K, Nishikawa K, Siddiqui S S. 1995. Exclusive expression of C. elegans osm-3 kinesin gene in chemosnsory neurons open to the external environment. Journal of Molecular Biology, 247(3):377-389, https://doi.org/10.1006/jmbi.1994.0146.
Takano K, Miki T, Katahira J, Yoneda Y. 2007. NXF2 is involved in cytoplasmic mRNA dynamics through interactions with motor proteins. Nucleic Acids Research, 35(8):2513-2521, https://doi.org/10.1093/nar/gkm125.
Wang J Q, Gao X M, Zheng X B, Hou C C, Xie Q P, Lou B, Zhu J Q. 2019. Expression and potential functions of KIF3A/3B to promote nuclear reshaping and tail formation during Larimichthys polyactis spermiogenesis. Development Genes and Evolution, 229(4):161-181, https://doi.org/10.1007/s00427-019-00637-5.
Wong-Riley M T T, Besharse J C. 2012. The kinesin superfamily protein KIF17:one protein with many functions. Biomolecular Concepts, 3(3):267-282, https://doi.org/10.1515/bmc-2011-0064.
Yamazaki H, Nakata T, Okada Y, Hirokawa N. 1995. KIF3A/B:a heterodimeric kinesin superfamily protein that works as a microtubule plus end-directed motor for membrane organelle transport. The Journal of Cell Biology, 130(6):1387-1399, https://doi.org/10.1083/jcb.130.6.1387.
Yan W. 2009. Male infertility caused by spermiogenic defects:lessons from gene knockouts. Molecular and Cellular Endocrinology, 306(1-2):24-32, https://doi.org/10.1016/j.mce.2009.03.003.
Zhang B D, Xue D X, Wang J, Li Y L, Liu B J, Liu J X. 2016. Development and preliminary evaluation of a genomewide single nucleotide polymorphisms resource generated by RAD-seq for the small yellow croaker (Larimichthys polyactis). Molecular Ecology Resources, 16(3):755-768, https://doi.org/10.1111/1755-0998.12476.
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 Physiology and Biochemistry, 43(5):1351-1371, https://doi.org/10.1007/s10695-017-0377-9.
Zhao Y Q, Mu D L, Wang D, Han Y L, Hou C C, Zhu J Q. 2018. Analysis of the function of KIF3A and KIF3B in the spermatogenesis in Boleophthalmus pectinirostris. Fish Physiology and Biochemistry, 44(3):769-788, https://doi.org/10.1007/s10695-017-0461-1.
Zhao Y Q, Yang H Y, Zhang D D, Han Y L, Hou C C, 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, https://doi.org/10.1016/j.anireprosci. 2017.06.017.