Identification and Expression Patterns of kif3bz during the Zebrafish Embryonic Development

  • Lee, A-Ram (Department of Biological Sciences, College of Biological Sciences, Chungnam National University) ;
  • Rhee, Myung-Chull (Department of Biological Sciences, College of Biological Sciences, Chungnam National University)
  • Published : 2009.12.31

Abstract

We are reporting the identification, expression patterns, and possible biological functions of zebrafish kif3b (kif3bz) encoding 475 amino acids. Kif3Bz contains the kinesin motor domain, catalytic domain, KISc domain, and one single coiled coil domain. Phylogenetic analysis indicates that kif3bz is a highly conserved gene among the tested vertebrates. First of all, both maternal and zygotic messages of kif3bz were evenly distributed in the blastomeres at 2-cell stage. Its ubiquitous expression throughout the blastomeres continued till 40% epiboly. However, kif3bz transcripts became restricted in Kupffer's vesicle at tailbud and 6-somite stages. At 13-somite stage, kif3bz expression pattern became specific to the telencephalon, diencephalon, trigeminal placode, and somites. Such expression patterns were further intensified in the telencephalon, diencephalons, hind brain, pronephric ducts, optic vesicles, and spinal cord neurons in the 23-somite stage embryos, and last till 24 hpf. We discussed possible functions of Kif3Bz related to the vertebrate embryonic development.

Keywords

References

  1. Alexander J and Stainier DY (1999) A molecular pathway leading to endoderm formation in zebrafish. Curr Biol 9: 1147-1157 https://doi.org/10.1016/S0960-9822(00)80016-0
  2. Amack JD and Yost HJ (2004) The T box transcription factor, no tail in ciliated cells controls zebrafish left-right asymmetry. Cur Biol 14: 685-690 https://doi.org/10.1016/j.cub.2004.04.002
  3. Bowerman B (1998) Maternal control of pattern formation in early Caenorhabditis elegans embryos. Curr Topics Dev Biol 39: 73-117 https://doi.org/10.1016/S0070-2153(08)60453-6
  4. Bisgrove BW, Essner JJ, and Yost HJ (1999) Regulation of midline development by antagonism of lefty and nodal signaling. Development 126: 3253-3262
  5. Brendza RP, Serbus LR, Duffy JB, and Saxton WM (2000) A function for kinesin I in the posterior transport of oskar mRNA and Staufen protein. Science 289: 2120-2122 https://doi.org/10.1126/science.289.5487.2120
  6. de Robertis EM, Larrain J, Oelgeschlager M, and Wessely O (2000) The establishment of spemann's organizer and patterning of the vertebrate embryo. Nature Review Genetics 1: 171-181 https://doi.org/10.1038/35042039
  7. Chana MS, Tripet BP, Mant CT, and Hodges R (2005) Stability and specificity of heterodimer formation for the coiled-coil neck regions of the motor proteins Kit3A and Kit3B: the role of unstructured oppositely charged regions. J Pept Res 65: 209-220
  8. Chen SR and Kimelman D (2000) The role of the yolk syncytial layer in germ later patterning in zebrafish. Development 127: 4681-4689
  9. Cooper MS and D'Amico LA (1996) A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 180: 184-198 https://doi.org/10.1006/dbio.1996.0294
  10. Corbit KC, Shyer AE, Dowdle WE, Gaulden J, Singla V, Chen MH, Chuang PT, and Reiter JF (2008) Kit3a constrains betaCatenin-dependent Wnt signaling through dual ciliary and non-ciliary mechanisms. Nat Cell Biol 10(1): 70-76 https://doi.org/10.1038/ncb1670
  11. De Robertis EM (2009) Spemarm's organizer and the selfregulation of embryonic fields. Mech Dev 126: 925-941 https://doi.org/10.1016/j.mod.2009.08.004
  12. Diefenbach RJ, Mackay JP, Armati PJ, and Cunningham AL (1998) The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochemistry 37: 16663-16670 https://doi.org/10.1021/bi981163r
  13. Dougan ST, Warga RM, Kane DA, Schier AF, and Talbot WS (2003) The role of the zebrafish Nodal-related genes squint and cyclops in patterning of mesendoderm. Development 130: 1837-1851 https://doi.org/10.1242/dev.00400
  14. Essner JJ, Amack JD, Nyholm MK, Harris EB, and Yost HJ (2005) Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132: 1247-1260 https://doi.org/10.1242/dev.01663
  15. Farzan SF, Ascano M Jr, Ogden SK, Sanial M, Brigul A, Plessis A, and Robbins DJ (2008) Costal2 functions as a kinesin-like protein in the Hedgehog signal transduction pathway. Curr Biol 18: 1215-1220 https://doi.org/10.1016/j.cub.2008.07.026
  16. Fuentealba LC, Eivers E, Ikeda A, Hurtado D, Kuroda H, Pera EM, and De Robertis EM (2007) Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Cell 131: 980-993 https://doi.org/10.1016/j.cell.2007.09.027
  17. Gerdes JM and Katsanis N (2008) Ciliary function and Wnt signal modulation. Curr Top Dev Biol 85: 175-195 https://doi.org/10.1016/S0070-2153(08)00807-7
  18. Goldstein LS (2001a) Molecular motors: from one motor many tails to one motor may tales. Trends Cell Biol 11: 477-482 https://doi.org/10.1016/S0962-8924(01)02143-2
  19. Goldstein LS (2001b) Kinesin molecular motors: Transport pathways, receptors, human disease. Proc Natl Acad Sci USA 98: 6999-7003 https://doi.org/10.1073/pnas.111145298
  20. Guzik BW and Goldstein LS (2004) Microtubule-dependent transport in neurons: steps towards an understanding of regulation, function and dysfunction. Curr Opin Cell Biol 16(4): 443-450 https://doi.org/10.1016/j.ceb.2004.06.002
  21. Hamada T (2007) Microtubue-associated proteins in higher plants. J Plant Res 20: 79-98
  22. Haraguchi K, Hayashi T, Jimbo T, Yamamoto T, and Akiyama T (2006) Role of the kinesin-2 family protein, KIF3, during mitosis. J Biol Chem 281(7): 4094-4099 https://doi.org/10.1074/jbc.M507028200
  23. Heasman J (1997) Patterning the Xenopus blastula. Development 124: 4179-4191
  24. Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519-526 https://doi.org/10.1126/science.279.5350.519
  25. Hirokawa N, Tanaka Y, Okada Y, and Takeda S (2006) Nodal flow and the generation ofleft-right asymmetry. Cell 125: 33-45 https://doi.org/10.1016/j.cell.2006.03.002
  26. Jesuthasan S and Strahle U (1996) Dynamic microtubules and specification of the zebrafish embryonic axis. Curr Bio 7: 31-42 https://doi.org/10.1016/S0960-9822(06)00025-X
  27. Jimeno D, Lillo C, Roberts EA, Goldstein LS, and Williams DS (2006) Kinesin-2 and photoreceptor cell death: requirement of motor subunits. Exp Eye Res 82(2): 351-353 https://doi.org/10.1016/j.exer.2005.10.026
  28. Karcher RL, Deacon SW, and Gelfand VI (2002) Motor-cargo interactions: the key to transport specificity. Trends Cell Biol 12: 21-27 https://doi.org/10.1016/S0962-8924(01)02184-5
  29. Kikuchi Y, Agathon A, Alexander J, Thisse C, Waldron S, Telon D, Thisse B, and Stainier DY (2001) casanova encodes a novel Sox-related protein necessary and sufficient for early endoderm formation in zebrafish. Genes Dev 15: 1493-1505 https://doi.org/10.1101/gad.892301
  30. Kim E-J, Ro H, Huh T-L, Lee CJ, Choi J, and Rhee M (2008) A novel kinesin-like protein, Surhe is associated with dorsalization in the zebrafish embryos. Ani Cell Sys 12: 219-230 https://doi.org/10.1080/19768354.2008.9647176
  31. Koyama E, Young B, Nagayama M, Shibukawa Y, EnomotoIwamoto M, Iwamoto M, Maeda Y, Lanske B, Song B, Serra R, and Pacifici M (2007) Conditional Kit3a ablation causes abnormal hedgehog signaling topography, growth plate dysfunction, and excessive bone and cartilage formation during mouse skeletogenesis. Development 134(11): 2159-2169 https://doi.org/10.1242/dev.001586
  32. Kull FJ, Sablin EP, Lau R, Fletterick RJ, and Vale RD (1996) Crystal structure of the kinesin motor domain reveals. Nature 380: 550-555 https://doi.org/10.1038/380550a0
  33. Larabell CA, Torres M, Rowning BA, Yost C, Miller JR, Wu M, Kimelman D, and Moon RT (1997) Establishment of the dorso-ventral axis in Xenopus embryos in presaged by early asymmetries in beta-Catenin that are modulated by the Wnt signaling pathway. J Cell Biol 136: 1123-1136 https://doi.org/10.1083/jcb.136.5.1123
  34. Marszalek JR, Ruiz-Lozano P, Roberts E, Chien KR, and Goldstein LS (1999) Situs inversys and embryonic ciliary morphogenesis defects in mouse mutants lacking the KIF3A subunit of kinesin-II. Proc Natl Acad Sci USA 96: 5043-5048 https://doi.org/10.1073/pnas.96.9.5043
  35. Mizuno T, Yamaha E, Kuroiw A, and Takeda H (1999) Removal of vegetal yolk causes dorsal deficiencies and impairs dorsal-inducing ability of the yolk cell in zebrafish. Mech Dev 81: 51-63 https://doi.org/10.1016/S0925-4773(98)00202-0
  36. Moore JD and Endow SA (1996) Kinesin proteins: a phylum of motors for microtubule-based motility. BioEssays 18: 207-219 https://doi.org/10.1002/bies.950180308
  37. Nakagawa T, Setou M, Seog DH, Ogasawara K, Dohmae N, Takio K, Ober EA, and Schulte-Merker S (1999) Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish. Dev Biol 215: 167-181 https://doi.org/10.1006/dbio.1999.9455
  38. Okabe N, Xu B, and Burdine RD (2008) Fluid dynamics in zebrafish Kupffer's vesicule. Dev Dyn 237: 3602-3612 https://doi.org/10.1002/dvdy.21730
  39. Ray RP and Schupbach T (1996) Intracellular signaling and polarization ofbody axes during Drosophila oogenesis. Genes Dev 10: 1711-1723 https://doi.org/10.1101/gad.10.14.1711
  40. Reed AA, Loh NY, Terryn S, Lippiat JD, Partridge CJ, Galvanovskis J, Williams SE, Jouret F, Wu FT, Courtoy PJ, Nesbit MA, Rorsman P, Devuyst O, Ashcroft FM, and Thakker RV (2009) CLC-5 and KIF3B interact to facilitate CLC-5 plasma membrane expression, endocytosis and microtubular transport:relevance to pathophysiology of Dent's disease. Am J Physiol Renal Physiol Nov 25.[Epub ahead ofprint] https://doi.org/10.1152/ajprenal.00038.2009
  41. Rowning BA, Wells J, Wu M, Gerhart JC, Moon RT, and Larabell CA (1997) Micro-tubule-mediated transport of organelles and localization of beta-Catenin to the future dorsal side of Xenopus eggs. Proc Natl Acad Sci USA 94: 1224-1229 https://doi.org/10.1073/pnas.94.4.1224
  42. Schneider S, Steinbeisser H, Warga RM, and Hausen P (1996) beta-Catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Dev 57: 191-198 https://doi.org/10.1016/0925-4773(96)00546-1
  43. Schonteich E, Wilson GM, Burden J, Hopkins CR, Anderson K, Goldenring JR, and Prekeris R (2008) The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J Cell Sci 121: 3824-3833 https://doi.org/10.1242/jcs.032441
  44. Takeda S, Yonekawa Y, Tanaka Y, Okada Y, Nonaka N, and Hirokawa N (1999) Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A-1 - mice analysis. J Cell Biol 145: 825-836 https://doi.org/10.1083/jcb.145.4.825
  45. Teng J, Rai T, Tanaka Y, Takei Y, Nakata T, Hirasawa M, Kulkarni AB, and Hirokawa N (2005) The KIF3 motor transports N-cadherin and organizes the developing neuroepithelium. Nat Cell Biol 7(5): 474-482 https://doi.org/10.1038/ncb1249
  46. Tanuma N, Nomura M, Ikeda M, Kasugai I, Tsubaki Y, Takagaki K, Kawamura T, Yamashita Y, Sato I, Sato M, Katakura R, Kikuchi K, and Shima H (2009) Protein phosphatase Dusp26 associates with KIF3 motor and promotes N-cadherinmediated cell-cell adhesion. Oncogene 28(5): 752-761 https://doi.org/10.1038/onc.2008.431
  47. Zhang Y and Hancock WO (2004) The two motor domains of KIF3A/B coordinate for processive motility and move at different speeds. Biophys J 87: 1795-1804 https://doi.org/10.1529/biophysj.104.039842
  48. Vale RD and Fletterick RJ (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13: 745-747 https://doi.org/10.1146/annurev.cellbio.13.1.745
  49. Varjosalo M and Taipale J (2008) Hedgehog: functions and mechanisms. Genes Dev 22(18): 2454-2472 https://doi.org/10.1101/gad.1693608
  50. Verhey KJ, Meyer D, Deehan R, Blenis J, Schnapp BJ, Rapoport TA, and Margolis B (2001) Cargo of kinesin identified as JIP scaffolding proteins and associated signaling moecules. J Cell Biol 152: 959-970 https://doi.org/10.1083/jcb.152.5.959
  51. Verhey KJ and Rapoport TA (2001) Kinesin carries the signal. Trends Biochem Sci 26: 545-549 https://doi.org/10.1016/S0968-0004(01)01931-4
  52. Weaver C, Farr GH III, Pan W, Rowning BA, Wang J, Mao J, Wu D, Li L, Larabell CA, and Kimelman D (2003) GBP binds kinesin light chain and translocates during cortical rotation in Xenopus eggs. Development 30: 5426-5436 https://doi.org/10.1242/dev.00737
  53. Westerfield, M (1995) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio), 3 Eugene, OR USA: University of Oregon Press
  54. Wilkie GS and Davis I (2001) Drosophila singless and pair-rule transcripts localize apically by dynein-mediated transport of RNA particles. Cell 105: 209-219 https://doi.org/10.1016/S0092-8674(01)00312-9
  55. Wong SY, Seol AD, So PL, Ermilov AN, Bichakjian CK, Epstein EH Jr, Dlugosz AA, and Reiter JF (2009) Primary cilia can both mediate and suppress Hedgehog pathway-dependent tumorigenesis. Nat Med 15(9): 1055-1061 https://doi.org/10.1038/nm.2011
  56. Wylie C, Kofron M, Payne C, Anderson R, Hosobuchi M, Joseph E, and Heasman J (1996) Maternal beta-Catenin establishes a dorsal signal in early Xenopus embryos. Development 122: 2987-2996