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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)

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Abstract

Spermiogenesis is a developmental process undergoing continuous differentiation to drive a diploid spermatogonium towards a haploid sperm cell. This striking transformation from spermatogonium to spermatozoa is made possible by the stage-specific adaption of cytoskeleton and associated molecular motor proteins. KIFC1 is a C-terminal kinesin motor found to boast essential roles in acrosome biogenesis and nuclear reshaping during spermiogenesis in rat. To explore its functions during the same process in Macrobrachium nipponense, we have cloned and sequenced the cDNA of a mammalian KIFC1 homologue (termed mn-KIFC1) from the total RNA of the testis. The 2,296 bp mn-KIFC1 cDNA contained a 87 bp 5′ untranslated region, a 211 bp 3′ untranslated region and a 1,998 bp open reading frame. Protein alignment demonstrated that mn-KIFC1 had 37.7, 58.7, 38.4, 37.2, 38.9 and 37.8% identity with its homologues in Salmo salar, Eriocheir sinensis, Homo sapiens, Mus musculus, Danio rerio and Xenopus laevis respectively. The phylogenetic tree revealed that mn-KIFC1 is most related to E. Sinensis KIFC1 among the examined species. Tissue expression analysis showed the presence of mn-KIFC1 in the testis, hepatopancreas, gill, muscle and heart. In situ hybridization showed that the mn-KIFC1 mRNA was localized at the periphery of the nuclear membrane and in the proacrosomal vesicle in early and middle spermatids. In late spermatids and spermatozoa, mn-KIFC1 was expressed in the acrosome and in the spike. In situ hybridization also indicated that KIFC1 works together with lamellar complex (LCx) and acroframosome (AFS) to drive acrosome formation and cellular transformation. LCx and AFS have both been previously proved to have essential roles during spermiogenesis in M. nipponense. In conclusion, the expression of mn-kifc1 at specific stages of spermiogenesis suggests a role in cellular transformations in M. nipponense.

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References

  1. Fawcett DW (1975) The mammalian spermatozoon. Dev Biol 44:394–436

    Article  PubMed  CAS  Google Scholar 

  2. Wang R, Sperry AO (2008) Identification of a novel Leucine-rich repeat protein and candidate PP1 regulatory subunit expressed in developing spermatids. BMC Cell Biol 9:9

    Article  PubMed  Google Scholar 

  3. Kimmins S, Kotaja N, Fienga G, Kolthur US, Brancorsini S, Hogeveen K, Monaco L, Sassone-Corsi P (2004) A specific programme of gene transcription in male germ cells. Reprod Biomed Online 8(5):496–500

    Article  PubMed  Google Scholar 

  4. Lui WY, Cheng CY (2008) Transcription regulation in spermatogenesis. Adv Exp Med Biol 636:115–132

    Article  PubMed  CAS  Google Scholar 

  5. Zou Y, Millette CF, Sperry AO (2002) KRP3A and KRP3B: candidate motors in spermatid maturation in the seminiferous epithelium. Biol Reprod 66:843–855

    Article  PubMed  CAS  Google Scholar 

  6. Vale RD, Hotani H (1988) Formation of membrane networks in vitro by kinesin-driven microtubule movement. J Cell Biol 107:2233–2241

    Article  PubMed  CAS  Google Scholar 

  7. Hirokawa N (1996) Organelle transport along microtubules—the role of KIFs. Trends Cell Biol 6:135–141

    Article  PubMed  CAS  Google Scholar 

  8. Hirokawa N, Noda Y, Okada Y (1998) Kinesin and dynein superfamily proteins in organelle transport and cell division. Curr Opin Cell Biol 10:60–73

    Article  PubMed  CAS  Google Scholar 

  9. Miki H, Okada Y, Hirokawa N (2005) Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15:467–476

    Article  PubMed  CAS  Google Scholar 

  10. Roof DM, Meluh PB, Rose MD (1992) Kinesin-related proteins required for assembly of the mitotic spindle. J Cell Biol 118:95–108

    Article  PubMed  CAS  Google Scholar 

  11. Sharp DJ, Rogers GC, Scholey JM (2000) Microtubule motors in mitosis. Nature 407:41–47

    Article  PubMed  CAS  Google Scholar 

  12. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43:513–525

    Article  PubMed  CAS  Google Scholar 

  13. Hirokawa N, Takemura R (2004) Kinesin superfamily proteins and their various functions and dynamics. Exp Cell Res 301:50–59

    Article  PubMed  CAS  Google Scholar 

  14. Kikkawa M (2008) The role of microtubules in processive kinesin movement. Trends Cell Biol 18(3):128–135

    Article  PubMed  CAS  Google Scholar 

  15. Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Natl Rev Mol Cell Biol 10:682–696

    Article  CAS  Google Scholar 

  16. Sperry AO, Zhao LP (1996) Kinesin-related proteins in the mammalian testes: candidate motors for meiosis and morphogenesis. Mol Biol Cell 7:289–305

    PubMed  CAS  Google Scholar 

  17. Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LS, Goodson HV, Hirokawa N, Howard J, Malmberg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy AS, Saxton WM, Schliwa M, Scholey JM, Vale RD, Walczak CE, Wordeman L (2004) A standardized kinesin nomenclature. J Cell Biol 167:19–22

    Article  PubMed  CAS  Google Scholar 

  18. Zhang Y, Sperry AO (2004) Comparative analysis of two C-terminal kinesin motor proteins: KIFC1 and KIFC5A. Cell Motil Cytoskeleton 58:213–230

    Article  PubMed  CAS  Google Scholar 

  19. Walczak CE, Verma S, Mitchison TJ (1997) XCTK2: a kinesin-related protein that promotes mitotic spindle assembly in Xenopus laevis egg extracts. J Cell Biol 136(4):859–870

    Article  PubMed  CAS  Google Scholar 

  20. Ems-McClung SC, Zheng YX, Walczak CE (2004) Importin α/β and Ran-GTP regulate XCTK2 microtubule binding through a bipartite nuclear localization signal. Mol Biol Cell 15:46–57

    Article  PubMed  CAS  Google Scholar 

  21. Goshima G, Vale RD (2005) Cell cycle-dependent dynamics and regulation of mitotic kinesins in Drosophila S2 cells. Mol Biol Cell 16:3896–3907

    Article  PubMed  CAS  Google Scholar 

  22. Cai S, Weaver LN, Ems-McClung SC, Walczak CE (2009) Kinesin-14 family proteins HSET/XCTK2 control spindle length by cross-linking and sliding microtubules. Mol Biol Cell 20:1348–1359

    Article  PubMed  CAS  Google Scholar 

  23. Zhu C, Zhao J, Bibikova M, Leverson JD, Bossy-Wetzel E, Fan JB, Abraham RT, 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

    Article  PubMed  CAS  Google Scholar 

  24. Yang WX, Sperry AO (2003) C-Terminal kinesinmotor KIFC1 participates in acrosome biogenesis and vesicle transport. Biol Reprod 69:1719–1729

    Article  PubMed  CAS  Google Scholar 

  25. Nath S, Bananis E, Sarkar S, Stockert RJ, Sperry AO, Murray JW, Wolkoff AW (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

    Article  PubMed  CAS  Google Scholar 

  26. Yu K, Hou L, Zhu JQ, Ying XP, Yang WX (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(1):113–123

    Article  PubMed  CAS  Google Scholar 

  27. Wang DH, Yang WX (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 Mol Integr Physiol 157(2):123–131

    Article  PubMed  Google Scholar 

  28. Yang WX (1998) Study on changes in three organelle during spermiogenesis of Macrobrachium nipponense (de Haan). Chin J Appl Environ Biol 4(1):49–54

    Google Scholar 

  29. Li Z, Pan CY, Zheng BH, Xiang L, Yang WX (2010) Immunocytochemical studies on the acroframosome during spermiogenesis of the caridean shrimp Macrobrachium nipponense (Crustacea, Natantia). Invertebr Reprod Dev 54(3):121–131

    Article  CAS  Google Scholar 

  30. Wang W, Zhu JQ, Yang WX (2010) Molecular cloning and characterization of KIFC1-like kinesin gene (ot-kifc1) from Octopus tankahkeei. Comp Biochem Physiol B Biochem Mol Biol 156(3):174–182

    Article  PubMed  Google Scholar 

  31. Hu JR, Xu N, Tan FQ, Wang DH, Liu M, Yang WX (2011) Molecular characterization of a KIF3A-like kinesin gene in the testis of the Chinese fire-bellied newt Cynops orientalis. Mol Biol Rep. doi:10.1007/s11033-011-1206-3

  32. Gimenez-bonafé P, Ribes E, Zamora MJ, Kasinsky HE, Chiva M (2002) Evolution of octopod sperm I: comparison of nuclear morphogenesis in Eledone and Octopus. Mol Reprod Dev 62:357–362

    Article  PubMed  Google Scholar 

  33. Hess RA, Renato FL (2008) Spermatogenesis and cycle of the seminiferous epithelium. Adv Exp Med Biol 636:1–15

    Article  PubMed  Google Scholar 

  34. Lie PP, Cheng CY, Mruk DD (2009) Coordinating cellular events during spermatogenesis: a biochemical model. Trends Biochem Sci 34(7):366–373

    Article  PubMed  CAS  Google Scholar 

  35. Yang WX, Jefferson H, Sperry AO (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

    Article  PubMed  CAS  Google Scholar 

  36. Endow SA, Komma DJ (1997) Spindle dynamics during meiosis in Drosophila oocytes. J Cell Biol 137:1321–1336

    Article  PubMed  CAS  Google Scholar 

  37. Noda Y, Sato-Yoshitake R, Kondo S, Nangaku M, Hirokawa N (1995) KIF2 is a new microtubule-based anterograde motor that transports membranous organelles distinct from those carried by kinesin heavy chain or KIF3A/B. J Cell Biol 129:157–167

    Article  PubMed  CAS  Google Scholar 

  38. Navolanic PM, Sperry AO (2000) Identification of isoforms of a mitotic motor in mammalian spermatogenesis. Biol Reprod 62:1360–1369

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to all members of the Sperm Laboratory at Zhejiang University for their helpful suggestion. This project was supported in part by National Natural Science Foundation of China (No. 31072198 and 40776079).

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Authors and Affiliations

  1. The Sperm Laboratory, College of Life Sciences, Zhejiang University, 866 Yu Hang Tang Road, Hangzhou, 310058, Zhejiang, China

    Yan-Ting Wang, Huan Mao, Cong-Cong Hou, Xiao Sun, Da-Hui Wang, Hong Zhou & Wan-Xi Yang

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  1. Yan-Ting Wang
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  2. Huan Mao
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  3. Cong-Cong Hou
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  7. Wan-Xi Yang
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Correspondence to Wan-Xi Yang.

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Wang, YT., Mao, H., Hou, CC. et al. 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 (2012). https://doi.org/10.1007/s11033-012-1593-0

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