Kid, a novel kinesin-like DNA binding protein, is localized to chromosomes and the mitotic spindle (original) (raw)

. 1996 Feb 1;15(3):457–467.

Abstract

Microtubule-associated motor proteins are thought to be involved in spindle formation and chromosome movements in mitosis/meiosis. We have molecularly cloned cDNAs for a gene that codes for a novel member of the kinesin family of proteins. Nucleotide sequencing reveals that the predicted gene product is a 73 kDa protein and is related to some extent to the Drosophila node gene product, which is involved in chromosomal segregation during meiosis. A sequence similar to the microtubule binding motor domain of kinesin is present in the N-terminal half of the protein, and its ability to bind to microtubules is demonstrated. Furthermore we show that its C-terminal half contains a putative nuclear localization signal similar to that of Jun and is able to bind to DNA. Accordingly, the protein was termed Kid (kinesin-like DNA binding protein). Indirect immunofluorescence studies show that Kid colocalizes with mitotic chromosomes and that it is enriched in the kinetochore at anaphase. Thus, we propose that Kid might play a role(s) in regulating the chromosomal movement along microtubules during mitosis.

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  1. Afshar K., Barton N. R., Hawley R. S., Goldstein L. S. DNA binding and meiotic chromosomal localization of the Drosophila nod kinesin-like protein. Cell. 1995 Apr 7;81(1):129–138. doi: 10.1016/0092-8674(95)90377-1. [DOI] [PubMed] [Google Scholar]
  2. Bloom G. S., Wagner M. C., Pfister K. K., Brady S. T. Native structure and physical properties of bovine brain kinesin and identification of the ATP-binding subunit polypeptide. Biochemistry. 1988 May 3;27(9):3409–3416. doi: 10.1021/bi00409a043. [DOI] [PubMed] [Google Scholar]
  3. Bloom K. The centromere frontier: kinetochore components, microtubule-based motility, and the CEN-value paradox. Cell. 1993 May 21;73(4):621–624. doi: 10.1016/0092-8674(93)90242-i. [DOI] [PubMed] [Google Scholar]
  4. Brady S. T. A novel brain ATPase with properties expected for the fast axonal transport motor. Nature. 1985 Sep 5;317(6032):73–75. doi: 10.1038/317073a0. [DOI] [PubMed] [Google Scholar]
  5. Carpenter A. T. A meiotic mutant defective in distributive disjunction in Drosophila melanogaster. Genetics. 1973 Mar;73(3):393–428. doi: 10.1093/genetics/73.3.393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Endow S. A., Henikoff S., Soler-Niedziela L. Mediation of meiotic and early mitotic chromosome segregation in Drosophila by a protein related to kinesin. Nature. 1990 May 3;345(6270):81–83. doi: 10.1038/345081a0. [DOI] [PubMed] [Google Scholar]
  8. Enos A. P., Morris N. R. Mutation of a gene that encodes a kinesin-like protein blocks nuclear division in A. nidulans. Cell. 1990 Mar 23;60(6):1019–1027. doi: 10.1016/0092-8674(90)90350-n. [DOI] [PubMed] [Google Scholar]
  9. Fujii M., Tsuchiya H., Seiki M. HTLV-1 Tax has distinct but overlapping domains for transcriptional activation and for enhancer specificity. Oncogene. 1991 Dec;6(12):2349–2352. [PubMed] [Google Scholar]
  10. Fujisawa J., Toita M., Yoshimura T., Yoshida M. The indirect association of human T-cell leukemia virus tax protein with DNA results in transcriptional activation. J Virol. 1991 Aug;65(8):4525–4528. doi: 10.1128/jvi.65.8.4525-4528.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fuller M. T., Wilson P. G. Force and counterforce in the mitotic spindle. Cell. 1992 Nov 13;71(4):547–550. doi: 10.1016/0092-8674(92)90587-3. [DOI] [PubMed] [Google Scholar]
  12. Gelfand V. I., Scholey J. M. Cell biology. Every motion has its motor. Nature. 1992 Oct 8;359(6395):480–482. doi: 10.1038/359480a0. [DOI] [PubMed] [Google Scholar]
  13. Goldstein L. S. With apologies to scheherazade: tails of 1001 kinesin motors. Annu Rev Genet. 1993;27:319–351. doi: 10.1146/annurev.ge.27.120193.001535. [DOI] [PubMed] [Google Scholar]
  14. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hackney D. D. Kinesin ATPase: rate-limiting ADP release. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6314–6318. doi: 10.1073/pnas.85.17.6314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hagan I., Yanagida M. Novel potential mitotic motor protein encoded by the fission yeast cut7+ gene. Nature. 1990 Oct 11;347(6293):563–566. doi: 10.1038/347563a0. [DOI] [PubMed] [Google Scholar]
  17. Hatsumi M., Endow S. A. The Drosophila ncd microtubule motor protein is spindle-associated in meiotic and mitotic cells. J Cell Sci. 1992 Dec;103(Pt 4):1013–1020. doi: 10.1242/jcs.103.4.1013. [DOI] [PubMed] [Google Scholar]
  18. Hirokawa N., Pfister K. K., Yorifuji H., Wagner M. C., Brady S. T., Bloom G. S. Submolecular domains of bovine brain kinesin identified by electron microscopy and monoclonal antibody decoration. Cell. 1989 Mar 10;56(5):867–878. doi: 10.1016/0092-8674(89)90691-0. [DOI] [PubMed] [Google Scholar]
  19. Hoyt M. A., He L., Loo K. K., Saunders W. S. Two Saccharomyces cerevisiae kinesin-related gene products required for mitotic spindle assembly. J Cell Biol. 1992 Jul;118(1):109–120. doi: 10.1083/jcb.118.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hyman A. A., Middleton K., Centola M., Mitchison T. J., Carbon J. Microtubule-motor activity of a yeast centromere-binding protein complex. Nature. 1992 Oct 8;359(6395):533–536. doi: 10.1038/359533a0. [DOI] [PubMed] [Google Scholar]
  21. Inoue J., Takahara T., Akizawa T., Hino O. Bcl-3, a member of the I kappa B proteins, has distinct specificity towards the Rel family of proteins. Oncogene. 1993 Aug;8(8):2067–2073. [PubMed] [Google Scholar]
  22. Ishii S., Imamoto F., Yamanashi Y., Toyoshima K., Yamamoto T. Characterization of the promoter region of the human c-erbB-2 protooncogene. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4374–4378. doi: 10.1073/pnas.84.13.4374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Knowles B. A., Hawley R. S. Genetic analysis of microtubule motor proteins in Drosophila: a mutation at the ncd locus is a dominant enhancer of nod. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7165–7169. doi: 10.1073/pnas.88.16.7165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kodama T., Fukui K., Kometani K. The initial phosphate burst in ATP hydrolysis by myosin and subfragment-1 as studied by a modified malachite green method for determination of inorganic phosphate. J Biochem. 1986 May;99(5):1465–1472. doi: 10.1093/oxfordjournals.jbchem.a135616. [DOI] [PubMed] [Google Scholar]
  25. Koshland D. Mitosis: back to the basics. Cell. 1994 Jul 1;77(7):951–954. doi: 10.1016/0092-8674(94)90432-4. [DOI] [PubMed] [Google Scholar]
  26. Kuznetsov S. A., Vaisberg Y. A., Rothwell S. W., Murphy D. B., Gelfand V. I. Isolation of a 45-kDa fragment from the kinesin heavy chain with enhanced ATPase and microtubule-binding activities. J Biol Chem. 1989 Jan 5;264(1):589–595. [PubMed] [Google Scholar]
  27. Le Guellec R., Paris J., Couturier A., Roghi C., Philippe M. Cloning by differential screening of a Xenopus cDNA that encodes a kinesin-related protein. Mol Cell Biol. 1991 Jun;11(6):3395–3398. doi: 10.1128/mcb.11.6.3395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Liao H., Li G., Yen T. J. Mitotic regulation of microtubule cross-linking activity of CENP-E kinetochore protein. Science. 1994 Jul 15;265(5170):394–398. doi: 10.1126/science.8023161. [DOI] [PubMed] [Google Scholar]
  29. Maruyama K., Sugano S. Oligo-capping: a simple method to replace the cap structure of eukaryotic mRNAs with oligoribonucleotides. Gene. 1994 Jan 28;138(1-2):171–174. doi: 10.1016/0378-1119(94)90802-8. [DOI] [PubMed] [Google Scholar]
  30. Masumoto H., Sugimoto K., Okazaki T. Alphoid satellite DNA is tightly associated with centromere antigens in human chromosomes throughout the cell cycle. Exp Cell Res. 1989 Mar;181(1):181–196. doi: 10.1016/0014-4827(89)90192-4. [DOI] [PubMed] [Google Scholar]
  31. Matsuzawa Y., Semba K., Kawamura-Tsuzuku J., Sudo T., Ishii S., Toyoshima K., Yamamoto T. Characterization of the promoter region of the c-yes proto-oncogene: the importance of the GC boxes on its promoter activity. Oncogene. 1991 Sep;6(9):1561–1567. [PubMed] [Google Scholar]
  32. McDonald H. B., Goldstein L. S. Identification and characterization of a gene encoding a kinesin-like protein in Drosophila. Cell. 1990 Jun 15;61(6):991–1000. doi: 10.1016/0092-8674(90)90064-l. [DOI] [PubMed] [Google Scholar]
  33. Meluh P. B., Rose M. D. KAR3, a kinesin-related gene required for yeast nuclear fusion. Cell. 1990 Mar 23;60(6):1029–1041. doi: 10.1016/0092-8674(90)90351-e. [DOI] [PubMed] [Google Scholar]
  34. Mori S., Akiyama T., Yamada Y., Morishita Y., Sugawara I., Toyoshima K., Yamamoto T. C-erbB-2 gene product, a membrane protein commonly expressed on human fetal epithelial cells. Lab Invest. 1989 Jul;61(1):93–97. [PubMed] [Google Scholar]
  35. Murphy T. D., Karpen G. H. Interactions between the nod+ kinesin-like gene and extracentromeric sequences are required for transmission of a Drosophila minichromosome. Cell. 1995 Apr 7;81(1):139–148. doi: 10.1016/0092-8674(95)90378-x. [DOI] [PubMed] [Google Scholar]
  36. Nangaku M., Sato-Yoshitake R., Okada Y., Noda Y., Takemura R., Yamazaki H., Hirokawa N. KIF1B, a novel microtubule plus end-directed monomeric motor protein for transport of mitochondria. Cell. 1994 Dec 30;79(7):1209–1220. doi: 10.1016/0092-8674(94)90012-4. [DOI] [PubMed] [Google Scholar]
  37. Nislow C., Lombillo V. A., Kuriyama R., McIntosh J. R. A plus-end-directed motor enzyme that moves antiparallel microtubules in vitro localizes to the interzone of mitotic spindles. Nature. 1992 Oct 8;359(6395):543–547. doi: 10.1038/359543a0. [DOI] [PubMed] [Google Scholar]
  38. Roof D. M., Meluh P. B., Rose M. D. Kinesin-related proteins required for assembly of the mitotic spindle. J Cell Biol. 1992 Jul;118(1):95–108. doi: 10.1083/jcb.118.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Saunders W. S., Hoyt M. A. Kinesin-related proteins required for structural integrity of the mitotic spindle. Cell. 1992 Aug 7;70(3):451–458. doi: 10.1016/0092-8674(92)90169-d. [DOI] [PubMed] [Google Scholar]
  40. Sawin K. E., LeGuellec K., Philippe M., Mitchison T. J. Mitotic spindle organization by a plus-end-directed microtubule motor. Nature. 1992 Oct 8;359(6395):540–543. doi: 10.1038/359540a0. [DOI] [PubMed] [Google Scholar]
  41. Saxton W. M., Porter M. E., Cohn S. A., Scholey J. M., Raff E. C., McIntosh J. R. Drosophila kinesin: characterization of microtubule motility and ATPase. Proc Natl Acad Sci U S A. 1988 Feb;85(4):1109–1113. doi: 10.1073/pnas.85.4.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Scholey J. M., Heuser J., Yang J. T., Goldstein L. S. Identification of globular mechanochemical heads of kinesin. Nature. 1989 Mar 23;338(6213):355–357. doi: 10.1038/338355a0. [DOI] [PubMed] [Google Scholar]
  43. Scholey J. M., Porter M. E., Grissom P. M., McIntosh J. R. Identification of kinesin in sea urchin eggs, and evidence for its localization in the mitotic spindle. Nature. 1985 Dec 5;318(6045):483–486. doi: 10.1038/318483a0. [DOI] [PubMed] [Google Scholar]
  44. Selden R. F., Howie K. B., Rowe M. E., Goodman H. M., Moore D. D. Human growth hormone as a reporter gene in regulation studies employing transient gene expression. Mol Cell Biol. 1986 Sep;6(9):3173–3179. doi: 10.1128/mcb.6.9.3173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Shiio Y., Yamamoto T., Yamaguchi N. Negative regulation of Rb expression by the p53 gene product. Proc Natl Acad Sci U S A. 1992 Jun 15;89(12):5206–5210. doi: 10.1073/pnas.89.12.5206. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Smith D. B., Johnson K. S. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene. 1988 Jul 15;67(1):31–40. doi: 10.1016/0378-1119(88)90005-4. [DOI] [PubMed] [Google Scholar]
  47. Vale R. D., Reese T. S., Sheetz M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 1985 Aug;42(1):39–50. doi: 10.1016/s0092-8674(85)80099-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Vernos I., Raats J., Hirano T., Heasman J., Karsenti E., Wylie C. Xklp1, a chromosomal Xenopus kinesin-like protein essential for spindle organization and chromosome positioning. Cell. 1995 Apr 7;81(1):117–127. doi: 10.1016/0092-8674(95)90376-3. [DOI] [PubMed] [Google Scholar]
  49. Walker J. E., Saraste M., Runswick M. J., Gay N. J. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1982;1(8):945–951. doi: 10.1002/j.1460-2075.1982.tb01276.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Walker R. A., Sheetz M. P. Cytoplasmic microtubule-associated motors. Annu Rev Biochem. 1993;62:429–451. doi: 10.1146/annurev.bi.62.070193.002241. [DOI] [PubMed] [Google Scholar]
  51. Wang S. Z., Adler R. Chromokinesin: a DNA-binding, kinesin-like nuclear protein. J Cell Biol. 1995 Mar;128(5):761–768. doi: 10.1083/jcb.128.5.761. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wordeman L., Mitchison T. J. Identification and partial characterization of mitotic centromere-associated kinesin, a kinesin-related protein that associates with centromeres during mitosis. J Cell Biol. 1995 Jan;128(1-2):95–104. doi: 10.1083/jcb.128.1.95. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Yamamoto T., Ikawa S., Akiyama T., Semba K., Nomura N., Miyajima N., Saito T., Toyoshima K. Similarity of protein encoded by the human c-erb-B-2 gene to epidermal growth factor receptor. Nature. 1986 Jan 16;319(6050):230–234. doi: 10.1038/319230a0. [DOI] [PubMed] [Google Scholar]
  54. Yen T. J., Li G., Schaar B. T., Szilak I., Cleveland D. W. CENP-E is a putative kinetochore motor that accumulates just before mitosis. Nature. 1992 Oct 8;359(6395):536–539. doi: 10.1038/359536a0. [DOI] [PubMed] [Google Scholar]
  55. Zhang P., Hawley R. S. The genetic analysis of distributive segregation in Drosophila melanogaster. II. Further genetic analysis of the nod locus. Genetics. 1990 May;125(1):115–127. doi: 10.1093/genetics/125.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Zhang P., Knowles B. A., Goldstein L. S., Hawley R. S. A kinesin-like protein required for distributive chromosome segregation in Drosophila. Cell. 1990 Sep 21;62(6):1053–1062. doi: 10.1016/0092-8674(90)90383-p. [DOI] [PubMed] [Google Scholar]