Post-transcriptional homeostasis and regulation of MCM2-7 in mammalian cells

Nucleic Acids Research

Volumn 40, Issue 11, 2012, Pages 4914-4924

  Chuang, Chen Hua ^a   Yang, Dian ^a   Bai, Gongshi ^b   Freeland, Amy ^b   Pruitt, Steven C ^b   Schimenti, John C ^a  

^a Animal Health Diagnostic Center   (United States)

^b ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; MICRORNA; MICRORNA 34; MINICHROMOSOME MAINTENANCE PROTEIN 2; MINICHROMOSOME MAINTENANCE PROTEIN 3; MINICHROMOSOME MAINTENANCE PROTEIN 4; MINICHROMOSOME MAINTENANCE PROTEIN 5; MINICHROMOSOME MAINTENANCE PROTEIN 6; MINICHROMOSOME MAINTENANCE PROTEIN 7; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ARTICLE; CELL GROWTH; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; DICER1 GENE; DNA REPLICATION; DOWN REGULATION; EMBRYO; ENZYME INHIBITION; ENZYME REGULATION; FIBROBLAST; GENE; GENE DISRUPTION; GENE LOSS; IN VIVO STUDY; MAMMAL CELL; MCM4 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STOICHIOMETRY; TRANSCRIPTION REGULATION; UPREGULATION;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMATIN; DNA HELICASES; DNA-BINDING PROTEINS; DOWN-REGULATION; HOMEOSTASIS; LEUCINE; MICE; MICRORNAS; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA INTERFERENCE; RNA, MESSENGER;

EID: 84862183180     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks176     Document Type: Article

References (48)

1. Truong, L.N. and Wu, X. (2011) Prevention of DNA re-replication in eukaryotic cells. J. Mol. Cell Biol., 3, 13-22.
2. Woodward, A.M., Gö hler, T., Luciani, M.G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D.A. and Blow, J.J. (2006) Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol., 173, 673-683. (Pubitemid 46165576)
3. Ge, X., Jackson, D.A. and Blow, J.J. (2007) Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev., 21, 3331-3341. (Pubitemid 350277759)
4. Ibarra, A., Schwob, E. and Mendez, J. (2008) Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl Acad. Sci. USA, 105, 8956-8961.
5. Bicknell, L.S., Bongers, E.M., Leitch, A., Brown, S., Schoots, J., Harley, M.E., Aftimos, S., Al-Aama, J.Y., Bober, M., Brown, P.A. et al. (2011) Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat. Genet., 43, 356-359.
6. Bicknell, L.S., Walker, S., Klingseisen, A., Stiff, T., Leitch, A., Kerzendorfer, C., Martin, C.A., Yeyati, P., Al Sanna, N., Bober, M. et al. (2011) Mutations in ORC1, encoding the largest subunit of the origin recognition complex, cause microcephalic primordial dwarfism resembling Meier-Gorlin syndrome. Nat. Genet., 43, 350-355.
7. Guernsey, D.L., Matsuoka, M., Jiang, H., Evans, S., Macgillivray, C., Nightingale, M., Perry, S., Ferguson, M., LeBlanc, M., Paquette, J. et al. (2011) Mutations in origin recognition complex gene ORC4 cause Meier-Gorlin syndrome. Nat. Genet., 43, 360-364.
8. Shima, N., Alcaraz, A., Liachko, I., Buske, T.R., Andrews, C.A., Munroe, R.J., Hartford, S.A., Tye, B.K. and Schimenti, J.C. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet., 39, 93-98. (Pubitemid 46026507)
9. Pruitt, S.C., Bailey, K.J. and Freeland, A. (2007) Reduced Mcm2 expression results in severe stem/progenitor cell deficiency and cancer. Stem Cells, 25, 3121-3132. (Pubitemid 350294438)
10. Chuang, C.H., Wallace, M.D., Abratte, C., Southard, T. and Schimenti, J.C. (2010) Incremental genetic perturbations to MCM2-7 expression and subcellular distribution reveal exquisite sensitivity of mice to DNA replication stress. PLoS Genet., 6, e1001110.
11. Kawabata, T., Luebben, S.W., Yamaguchi, S., Ilves, I., Matise, I., Buske, T., Botchan, M.R. and Shima, N. (2011) Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol. Cell, 41, 543-553.
12. Tsao, C.C., Geisen, C. and Abraham, R.T. (2004) Interaction between human MCM7 and RAD17 proteins is required for replication checkpoint signaling. EMBO J., 23, 4660-4669. (Pubitemid 39657865)
13. Cortez, D., Glick, G. and Elledge, S.J. (2004) Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases. Proc. Natl Acad. Sci. USA, 101, 10078-10083. (Pubitemid 38891197)
14. Orr, S.J., Gaymes, T., Ladon, D., Chronis, C., Czepulkowski, B., Wang, R., Mufti, G.J., Marcotte, E.M. and Thomas, N.S. (2010) Reducing MCM levels in human primary T cells during the G(0) ! G(1) transition causes genomic instability during the first cell cycle. Oncogene, 29, 3803-3814.
15. Crevel, G., Hashimoto, R., Vass, S., Sherkow, J., Yamaguchi, M., Heck, M.M. and Cotterill, S. (2007) Differential requirements for MCM proteins in DNA replication in Drosophila S2 cells. PLoS One, 2, e833.
16. Buchsbaum, S., Morris, C., Bochard, V. and Jalinot, P. (2007) Human INT6 interacts with MCM7 and regulates its stability during S phase of the cell cycle. Oncogene, 26, 5132-5144. (Pubitemid 47206946)
17. Bochman, M.L. and Schwacha, A. (2009) The Mcm complex: unwinding the mechanism of a replicative helicase. Microbiol. Mol. Biol. Rev., 73, 652-683.
18. Ishimi, Y. (1997) A DNA helicase activity is associated with an MCM4,-6, and-7 protein complex. J. Biol. Chem., 272, 24508-24513. (Pubitemid 27418662)
19. Lee, J.K. and Hurwitz, J. (2001) Processive DNA helicase activity of the minichromosome maintenance proteins 4, 6, and 7 complex requires forked DNA structures. Proc. Natl Acad. Sci. USA, 98, 54-59. (Pubitemid 32095862)
20. Ishimi, Y., Ichinose, S., Omori, A., Sato, K. and Kimura, H. (1996) Binding of human minichromosome maintenance proteins with histone H3. J. Biol. Chem., 271, 24115-24122. (Pubitemid 26327393)
21. Schwacha, A. and Bell, S.P. (2001) Interactions between two catalytically distinct MCM subgroups are essential for coordinated ATP hydrolysis and DNA replication. Mol. Cell., 8, 1093-1104. (Pubitemid 34031811)
22. Sato, M., Gotow, T., You, Z., Komamura-Kohno, Y., Uchiyama, Y., Yabuta, N., Nojima, H. and Ishimi, Y. (2000) Electron microscopic observation and single-stranded DNA binding activity of the Mcm4, 6, 7 complex. J. Mol. Biol., 300, 421-431.
23. Brambrink, T., Foreman, R., Welstead, G.G., Lengner, C.J., Wernig, M., Suh, H. and Jaenisch, R. (2008) Sequential expression of pluripotency markers during direct reprogramming of mouse somatic cells. Cell Stem Cell, 2, 151-159. (Pubitemid 351168714)
24. Frisa, P.S. and Jacobberger, J.W. (2010) Cytometry of chromatin bound Mcm6 and PCNA identifies two states in G1 that are separated functionally by the G1 restriction point. BMC Cell Biol., 11, 26.
25. Friedrich, T.D., Bedner, E., Darzynkiewicz, Z. and Lehman, J.M. (2005) Distinct patterns of MCM protein binding in nuclei of S phase and rereplicating SV40-infected monkey kidney cells. Cytometry A, 68, 10-18. (Pubitemid 41572057)
26. Reinholdt, L., Ashley, T., Schimenti, J. and Shima, N. (2004) Forward genetic screens for meiotic and mitotic recombination-defective mutants in mice. Methods Mol. Biol., 262, 87-107.
27. Elferink, C.J. and Reiners, J.J. Jr (1996) Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques, 20, 470-477. (Pubitemid 26080883)
28. Sugimoto, K., Mori, K., Uchida, K., Kobayashi, D. and Itoi, K. (2007) Quantitative analysis of thyroid-stimulating hormone messenger RNA and heterogeneous nuclear RNA in hypothyroid rats. Brain Res. Bull., 74, 142-146. (Pubitemid 47187922)
29. Kuehbacher, A., Urbich, C., Zeiher, A.M. and Dimmeler, S. (2007) Role of Dicer and Drosha for endothelial microRNA expression and angiogenesis. Circ. Res., 101, 59-68. (Pubitemid 47094624)
30. Kaller, M., Liffers, S.T., Oeljeklaus, S., Kuhlmann, K., Rö h, S., Hoffmann, R., Warscheid, B. and Hermeking, H. (2011) Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol. Cell. Proteomics, 10, M111.010462.
31. Lal, A., Thomas, M.P., Altschuler, G., Navarro, F., O'Day, E., Li, X.L., Concepcion, C., Han, Y.C., Thiery, J., Rajani, D.K. et al. (2011) Capture of MicroRNA-Bound mRNAs Identifies the Tumor Suppressor miR-34a as a Regulator of Growth Factor Signaling. PLoS Genet., 7, e1002363.
32. He, L., He, X., Lim, L.P., de Stanchina, S.E., Xuan, Z., Liang, Y., Xue, W., Zender, L., Magnus, J., Ridzon, D. et al. (2007) A microRNA component of the p53 tumour suppressor network. Nature, 447, 1130-1134. (Pubitemid 47014436)
33. Yamakuchi, M., Lotterman, C.D., Bao, C., Hruban, R.H., Karim, B., Mendell, J.T., Huso, D. and Lowenstein, C.J. (2010) P53-induced microRNA-107 inhibits HIF-1 and tumor angiogenesis. Proc. Natl Acad. Sci. USA, 107, 6334-6339.
34. Li, X., Schimenti, J. and Tye, B. (2009) Aneuploidy and improved growth are coincident but not causal in a yeast cancer model. PLoS Biol., 7, e1000161.
35. Remus, D., Beuron, F., Tolun, G., Griffith, J.D., Morris, E.P. and Diffley, J.F. (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell, 139, 719-730.
36. Kunnev, D., Rusiniak, M.E., Kudla, A., Freeland, A., Cady, G.K. and Pruitt, S.C. (2010) DNA damage response and tumorigenesis in Mcm2-deficient mice. Oncogene, 29, 3630-3638.
37. Liku, M.E., Nguyen, V.Q., Rosales, A.W., Irie, K. and Li, J.J. (2005) CDK phosphorylation of a novel NLS-NES module distributed between two subunits of the Mcm2-7 complex prevents chromosomal rereplication. Mol. Biol. Cell, 16, 5026-5039. (Pubitemid 41416479)
38. Madine, M.A., Khoo, C.Y., Mills, A.D., Musahl, C. and Laskey, R.A. (1995) The nuclear envelope prevents reinitiation of replication by regulating the binding of MCM3 to chromatin in Xenopus egg extracts. Curr. Biol., 5, 1270-1279. (Pubitemid 3000036)
39. Gillespie, P.J., Khoudoli, G.A., Stewart, G., Swedlow, J.R. and Blow, J.J. (2007) ELYS/MEL-28 chromatin association coordinates nuclear pore complex assembly and replication licensing. Curr. Biol., 17, 1657-1662. (Pubitemid 47503804)
40. Ishimi, Y., Okayasu, I., Kato, C., Kwon, H.J., Kimura, H., Yamada, K. and Song, S.Y. (2003) Enhanced expression of Mcm proteins in cancer cells derived from uterine cervix. Eur. J. Biochem., 270, 1089-1101. (Pubitemid 36384443)
41. Lin, D.I., Aggarwal, P. and Diehl, J.A. (2008) Phosphorylation of MCM3 on Ser-112 regulates its incorporation into the MCM2-7 complex. Proc. Natl Acad. Sci. USA, 105, 8079-8084. (Pubitemid 351904711)
42. Burkhart, R., Schulte, D., Hu, D., Musahl, C., Gö hring, F. and Knippers, R. (1995) Interactions of human nuclear proteins P1Mcm3 and P1Cdc46. Eur. J. Biochem., 228, 431-438.
43. Kawabata, T., Yamaguchi, S., Buske, T., Luebben, S.W., Wallace, M., Matise, I., Schimenti, J.C. and Shima, N. (2011) A reduction of licensed origins reveals strain-specific replication dynamics in mice. Mamm. Genome, 22, 506-517.
44. Scian, M.J., Carchman, E.H., Mohanraj, L., Stagliano, K.E., Anderson, M.A., Deb, D., Crane, B.M., Kiyono, T., Windle, B., Deb, S.P. et al. (2008) Wild-type p53 and p73 negatively regulate expression of proliferation related genes. Oncogene, 27, 2583-2593. (Pubitemid 351550876)
45. Kuipers, M., Stasevich, T., Sasaki, T., Wilson, K., Hazelwood, K., McNally, J., Davidson, M. and Gilbert, D. (2011) Highly stable loading of Mcm proteins onto chromatin in living cells requires replication to unload. J. Cell Biol., 192, 29-41.
46. Wong, P.G., Winter, S.L., Zaika, E., Cao, T.V., Oguz, U., Koomen, J.M., Hamlin, J.L. and Alexandrow, M.G. (2011) Cdc45 limits replicon usage from a low density of preRCs in mammalian cells. PLoS One, 6, e17533.
47. Schulte, D., Burkhart, R., Musahl, C., Hu, B., Schlatterer, C., Hameister, H. and Knippers, R. (1995) Expression, phosphorylation and nuclear localization of the human P1 protein, a homologue of the yeast Mcm 3 replication protein. J. Cell Sci., 108(Pt 4), 1381-1389.
48. Gao, N., Davuluri, G., Gong, W., Seiler, C., Lorent, K., Furth, E.E., Kaestner, K.H. and Pack, M. (2011) The nuclear pore complex protein Elys is required for genome stability in mouse intestinal epithelial progenitor cells. Gastroenterology, 140, 1547-1555.