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Plant Cell. 1999 Jul; 11(7): 1227–1238.
PMCID: PMC144275

A maize homolog of mammalian CENPC is a constitutive component of the inner kinetochore.


Genes for three maize homologs (CenpcA, CenpcB, and CenpcC) of the conserved kinetochore assembly protein known as centromere protein C (CENPC) have been identified. The C-terminal portion of maize CENPC shares similarity with mammalian CENPC and its yeast homolog Mif2p over a 23-amino acid region known as region I. Immunolocalization experiments combined with three-dimensional light microscopy demonstrated that CENPC is a component of the kinetochore throughout interphase, mitosis, and meiosis. It is shown that sister kinetochore separation occurs in two discrete phases during meiosis. A partial separation of sister kinetochores occurs in prometaphase I, and a complete separation occurs in prometaphase II. CENPC is absent on structures known as neocentromeres that, in maize, demonstrate poleward movement but lack other important features of centromeres/kinetochores. CENPC and a previously identified centromeric DNA sequence interact closely but do not strictly colocalize on meiotic chromosomes. These and other data indicate that CENPC occupies an inner domain of the maize kinetochore.

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Selected References

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  • Alfenito MR, Birchler JA. Molecular characterization of a maize B chromosome centric sequence. Genetics. 1993 Oct;135(2):589–597. [PMC free article] [PubMed]
  • Allshire RC. Centromeres, checkpoints and chromatid cohesion. Curr Opin Genet Dev. 1997 Apr;7(2):264–273. [PubMed]
  • Ananiev EV, Phillips RL, Rines HW. Complex structure of knob DNA on maize chromosome 9. Retrotransposon invasion into heterochromatin. Genetics. 1998 Aug;149(4):2025–2037. [PMC free article] [PubMed]
  • Aragón-Alcaide L, Miller T, Schwarzacher T, Reader S, Moore G. A cereal centromeric sequence. Chromosoma. 1996 Dec;105(5):261–268. [PubMed]
  • Asai DJ, Brokaw CJ, Thompson WC, Wilson L. Two different monoclonal antibodies to alpha-tubulin inhibit the bending of reactivated sea urchin spermatozoa. Cell Motil. 1982;2(6):599–614. [PubMed]
  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Binarova P, Cihalikova J, Dolezel J. Localization of MPM-2 recognized phosphoproteins and tubulin during cell cycle progression in synchronized Vicia faba root meristem cells. Cell Biol Int. 1993 Sep;17(9):847–856. [PubMed]
  • Brown MT. Sequence similarities between the yeast chromosome segregation protein Mif2 and the mammalian centromere protein CENP-C. Gene. 1995 Jul 4;160(1):111–116. [PubMed]
  • Brown MT, Goetsch L, Hartwell LH. MIF2 is required for mitotic spindle integrity during anaphase spindle elongation in Saccharomyces cerevisiae. J Cell Biol. 1993 Oct;123(2):387–403. [PMC free article] [PubMed]
  • Campbell MS, Gorbsky GJ. Microinjection of mitotic cells with the 3F3/2 anti-phosphoepitope antibody delays the onset of anaphase. J Cell Biol. 1995 Jun;129(5):1195–1204. [PMC free article] [PubMed]
  • Choo KH. Centromere DNA dynamics: latent centromeres and neocentromere formation. Am J Hum Genet. 1997 Dec;61(6):1225–1233. [PMC free article] [PubMed]
  • Cooke CA, Schaar B, Yen TJ, Earnshaw WC. Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma. 1997 Dec;106(7):446–455. [PubMed]
  • Dawe R Kelly. MEIOTIC CHROMOSOME ORGANIZATION AND SEGREGATION IN PLANTS. Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49(NaN):371–395. [PubMed]
  • Dawe RK, Cande WZ. Induction of centromeric activity in maize by suppressor of meiotic drive 1. Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8512–8517. [PMC free article] [PubMed]
  • Dawe RK, Sedat JW, Agard DA, Cande WZ. Meiotic chromosome pairing in maize is associated with a novel chromatin organization. Cell. 1994 Mar 11;76(5):901–912. [PubMed]
  • Dennis ES, Peacock WJ. Knob heterochromatin homology in maize and its relatives. J Mol Evol. 1984;20(3-4):341–350. [PubMed]
  • Depinet TW, Zackowski JL, Earnshaw WC, Kaffe S, Sekhon GS, Stallard R, Sullivan BA, Vance GH, Van Dyke DL, Willard HF, et al. Characterization of neo-centromeres in marker chromosomes lacking detectable alpha-satellite DNA. Hum Mol Genet. 1997 Aug;6(8):1195–1204. [PubMed]
  • Dong F, Miller JT, Jackson SA, Wang GL, Ronald PC, Jiang J. Rice (Oryza sativa) centromeric regions consist of complex DNA. Proc Natl Acad Sci U S A. 1998 Jul 7;95(14):8135–8140. [PMC free article] [PubMed]
  • du Sart D, Cancilla MR, Earle E, Mao JI, Saffery R, Tainton KM, Kalitsis P, Martyn J, Barry AE, Choo KH. A functional neo-centromere formed through activation of a latent human centromere and consisting of non-alpha-satellite DNA. Nat Genet. 1997 Jun;16(2):144–153. [PubMed]
  • Fukagawa T, Brown WR. Efficient conditional mutation of the vertebrate CENP-C gene. Hum Mol Genet. 1997 Dec;6(13):2301–2308. [PubMed]
  • Goldstein LS. Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell. 1981 Sep;25(3):591–602. [PubMed]
  • Harrington JJ, Van Bokkelen G, Mays RW, Gustashaw K, Willard HF. Formation of de novo centromeres and construction of first-generation human artificial microchromosomes. Nat Genet. 1997 Apr;15(4):345–355. [PubMed]
  • Houben A, Guttenbach M, Kress W, Pich U, Schubert I, Schmid M. Immunostaining and interphase arrangement of field bean kinetochores. Chromosome Res. 1995 Jan;3(1):27–31. [PubMed]
  • Jiang J, Nasuda S, Dong F, Scherrer CW, Woo SS, Wing RA, Gill BS, Ward DC. A conserved repetitive DNA element located in the centromeres of cereal chromosomes. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):14210–14213. [PMC free article] [PubMed]
  • Kalitsis P, Fowler KJ, Earle E, Hill J, Choo KH. Targeted disruption of mouse centromere protein C gene leads to mitotic disarray and early embryo death. Proc Natl Acad Sci U S A. 1998 Feb 3;95(3):1136–1141. [PMC free article] [PubMed]
  • Karpen GH, Allshire RC. The case for epigenetic effects on centromere identity and function. Trends Genet. 1997 Dec;13(12):489–496. [PubMed]
  • Knehr M, Poppe M, Schroeter D, Eickelbaum W, Finze EM, Kiesewetter UL, Enulescu M, Arand M, Paweletz N. Cellular expression of human centromere protein C demonstrates a cyclic behavior with highest abundance in the G1 phase. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10234–10239. [PMC free article] [PubMed]
  • Meluh PB, Koshland D. Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell. 1995 Jul;6(7):793–807. [PMC free article] [PubMed]
  • Meluh PB, Koshland D. Budding yeast centromere composition and assembly as revealed by in vivo cross-linking. Genes Dev. 1997 Dec 15;11(24):3401–3412. [PMC free article] [PubMed]
  • Moens PB, Spyropoulos B. Immunocytology of chiasmata and chromosomal disjunction at mouse meiosis. Chromosoma. 1995 Nov;104(3):175–182. [PubMed]
  • Mole-Bajer J, Bajer AS, Zinkowski RP, Balczon RD, Brinkley BR. Autoantibodies from a patient with scleroderma CREST recognized kinetochores of the higher plant Haemanthus. Proc Natl Acad Sci U S A. 1990 May;87(9):3599–3603. [PMC free article] [PubMed]
  • Nicklas RB. How cells get the right chromosomes. Science. 1997 Jan 31;275(5300):632–637. [PubMed]
  • Peacock WJ, Dennis ES, Rhoades MM, Pryor AJ. Highly repeated DNA sequence limited to knob heterochromatin in maize. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4490–4494. [PMC free article] [PubMed]
  • Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC. The centromere: hub of chromosomal activities. Science. 1995 Dec 8;270(5242):1591–1594. [PubMed]
  • Richards EJ, Dawe RK. Plant centromeres: structure and control. Curr Opin Plant Biol. 1998 Apr;1(2):130–135. [PubMed]
  • Rieder CL. The formation, structure, and composition of the mammalian kinetochore and kinetochore fiber. Int Rev Cytol. 1982;79:1–58. [PubMed]
  • Saitoh H, Tomkiel J, Cooke CA, Ratrie H, 3rd, Maurer M, Rothfield NF, Earnshaw WC. CENP-C, an autoantigen in scleroderma, is a component of the human inner kinetochore plate. Cell. 1992 Jul 10;70(1):115–125. [PubMed]
  • Shah DM, Hightower RC, Meagher RB. Genes encoding actin in higher plants: intron positions are highly conserved but the coding sequences are not. J Mol Appl Genet. 1983;2(1):111–126. [PubMed]
  • Staiger CJ, Cande WZ. Microtubule distribution in dv, a maize meiotic mutant defective in the prophase to metaphase transition. Dev Biol. 1990 Mar;138(1):231–242. [PubMed]
  • Starr DA, Williams BC, Li Z, Etemad-Moghadam B, Dawe RK, Goldberg ML. Conservation of the centromere/kinetochore protein ZW10. J Cell Biol. 1997 Sep 22;138(6):1289–1301. [PMC free article] [PubMed]
  • Sugimoto K, Yata H, Muro Y, Himeno M. Human centromere protein C (CENP-C) is a DNA-binding protein which possesses a novel DNA-binding motif. J Biochem. 1994 Oct;116(4):877–881. [PubMed]
  • Sugimoto K, Kuriyama K, Shibata A, Himeno M. Characterization of internal DNA-binding and C-terminal dimerization domains of human centromere/kinetochore autoantigen CENP-C in vitro: role of DNA-binding and self-associating activities in kinetochore organization. Chromosome Res. 1997 Apr;5(2):132–141. [PubMed]
  • Sullivan BA, Schwartz S. Identification of centromeric antigens in dicentric Robertsonian translocations: CENP-C and CENP-E are necessary components of functional centromeres. Hum Mol Genet. 1995 Dec;4(12):2189–2197. [PubMed]
  • Suzuki T, Ide N, Tanaka I. Immunocytochemical visualization of the centromeres during male and female meiosis in Lilium longiflorum. Chromosoma. 1997 Dec;106(7):435–445. [PubMed]
  • Tomkiel J, Cooke CA, Saitoh H, Bernat RL, Earnshaw WC. CENP-C is required for maintaining proper kinetochore size and for a timely transition to anaphase. J Cell Biol. 1994 May;125(3):531–545. [PMC free article] [PubMed]
  • Warburton PE, Cooke CA, Bourassa S, Vafa O, Sullivan BA, Stetten G, Gimelli G, Warburton D, Tyler-Smith C, Sullivan KF, et al. Immunolocalization of CENP-A suggests a distinct nucleosome structure at the inner kinetochore plate of active centromeres. Curr Biol. 1997 Nov 1;7(11):901–904. [PubMed]
  • Yang CH, Tomkiel J, Saitoh H, Johnson DH, Earnshaw WC. Identification of overlapping DNA-binding and centromere-targeting domains in the human kinetochore protein CENP-C. Mol Cell Biol. 1996 Jul;16(7):3576–3586. [PMC free article] [PubMed]
  • Yu HG, Hiatt EN, Chan A, Sweeney M, Dawe RK. Neocentromere-mediated chromosome movement in maize. J Cell Biol. 1997 Nov 17;139(4):831–840. [PMC free article] [PubMed]
  • Yu HG, Muszynski MG, Kelly Dawe R. The maize homologue of the cell cycle checkpoint protein MAD2 reveals kinetochore substructure and contrasting mitotic and meiotic localization patterns. J Cell Biol. 1999 May 3;145(3):425–435. [PMC free article] [PubMed]

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