The Croonian Lecture 2001 hunting the antisocial cancer cell: MCM proteins and their exploitation

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 360, Issue 1458, 2005, Pages 1119-1132

  Laskey, Ronald ^a,b  

^a HUTCHISON MRC RESEARCH CENTRE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cancer diagnosis; Cell proliferation; DNA replication; Minichromosome maintenance proteins; Replication licencing

Indexed keywords

CANCER;

EUKARYOTA;

EID: 31344438919     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2005.1656     Document Type: Conference Paper

References (67)

1. Aparicio, O. J., Weinstein, D. M. & Bell, S. P. 1997 Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 91, 59-69.
2. Aussel, L., Barre, F. X., Aroyo, M., Stasiak, A., Stasiak, A. Z. & Sherratt, D. 2002 FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108, 195-205.
3. Baldwin, P., Laskey, R. & Coleman, N. 2003 Translational approaches to improving cervical screening. Nat. Rev. Cancer 3, 217-226.
4. Bell, S. P. & Dutta, A. 2002 DNA replication in eukaryotic cells. Annu. Rev. Biochem. 71, 333-374.
5. Blow, J. J., Dilworth, S. M., Dingwall, C., Mills, A. D. & Laskey, R. A. 1987 Chromosome replication in cell-free systems from Xenopus eggs. Phil. Trans. R. Soc. B 317, 483-494.
6. Blow, J. J. & Laskey, R. A. 1988 A role for the nuclear envelope in controlling DNA replication within the cell cycle. Nature, 332, 546-548.
7. Brewer, B. J. 1988 When polymerases collide: replication and the transcriptional organisation of the E. coli chromosome. Cell 53, 679-686.
8. Campbell, J. L. & Newlon, C. S. 1991 Chromosomal DNA replication. In The molecular and cellular biology of the yeast Saccharomyces cerevisiae (ed. J. R. Broach & J. R. Pringle), vol. 1, pp. 41-146. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
9. Celniker, S. J., Sweder, K., Srienc, F., Bailey, J. E. & Campbell, J. L. 1984 Deletion mutations affecting autonomously replicating sequence Ars1 of Saccharomyces cerevisiae. Mol. Cell. Biol. 4, 2455-2466.
10. Chong, J. P. J., Mahbubani, H. M., Khoo, C.-Y. & Blow, J. 1995 Purification of an Mcm-containing complex as a component of the DNA replication licensing system. Nature 375, 418-421.
11. Coverley, D., Wilkinson, H., Madine, M. A., Mills, A. & Laskey, R. A. 1998 Protein kinase inhibition in G2 causes mammalian MCM proteins to reassociate with chromatin and restores ability to replicate. Exp. Cell. Res. 238, 63-69.
12. Coverley, D., Laman, H. & Laskey, R. A. 2002 Distinct roles for cyclins E and A during DNA replication. Nat. Cell. Biol. 4, 523-528.
13. Davies, J. R., Freeman, A., Morris, L. S., Bingham, S., Dilworth, S., Scott, I., Laskey, R. A., Miller, R. & Coleman, N. 2002 Analysis of minichromosome maintenance proteins as a novel method for detection of colorectal cancer in stool. Lancet 359, 1917-1919.
14. Dimitrova, D. S., Todorov, I. T., Melendy, T. & Gilbert, D. M. 1999 Mcm2, but not RPA, is a component of the mammalian early G1-phase pre-replication complex. J. Cell. Biol. 146, 709-722.
15. Egelman, E. 2001 Pumping DNA. Nature 409, 573-575.
16. Evan, G. & Littlewood, T. 1998 A matter of life and cell death. Science 281, 1317-1322.
17. Evan, G. I. & Vousden, K. H. 2001 Proliferation, cell cycle and apoptosis in cancer. Nature 411, 342-348.
18. Forsburg, S. L. 2004 Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev. 68, 109-131.
19. Freeman, A., Morris, L. S., Mills, A. D., Stoeber, K., Laskey, R. A., Williams, G. H. & Coleman, N. 1999 Minichromosome maintenance proteins as biological markers of dysplasia and malignancy. Clin. Cancer Res. 5, 2121-2132.
20. Freidberg, E. C. 2003 DNA damage and repair. Nature 421, 436-440.
21. Geng, Y. et al. 2003 Cyclin E ablation in the mouse. Cell 114, 431-443.
22. Gonzalez, M. A., Tachibana, K. K., Chin, S.-F., Callagy, G., Madine, M. A., Vowler, S. L., Pinder, S. E., Laskey, R. A. & Coleman, N. 2004 Geminin predicts adverse clinical outcome in breast cancer by reflecting cell cycle progression. J. Pathol. 204, 121-130.
23. Hanahan, D. & Weinberg, R. A. 2000 The hallmarks of cancer. Cell 100, 57-70.
24. Harland, R. M. & Laskey, R. A. 1980 Regulated replication of DNA microinjected into eggs of Xenopus laevis. Cell 21, 761-771.
25. Hiraiwa, A., Fujita, M., Nagasaka, T., Adachi, A., Ohashi, M. & Ishibashi, M. 1997 Immunolocalisation of hCDC47 protein in normal and neoplastic human tissues and its relation to growth. Int. J. Cancer 74, 180-184.
26. Hyrien, O. & Méchali, M. 1993 Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos. EMBO J. 12, 4511-4520.
27. Hyrien, O., Maric, C. & Méchali, M. 1995 Transition in specification of embryonic metazoan DNA replication origins. Science 270, 994-997.
28. Ishimi, Y. 1997 A DNA helicase activity is associated with an MCM4, -6 and -7 protein complex. J. Biol. Chem., 272, 24508-24513.
29. Kaplan, D. L. & O'Donnell, M. 2002 DnaB drives DNA branch migration and dislodges proteins while encircling two DNA strands. Mol. Cell 10, 647-657.
30. Kearsey, S. E. 1983 Analysis of sequences conferring autonomous replication in baker's yeast. EMBO J. 2, 1571-1575.
31. Kearsey, S. E. 1984 Structural requirements for the function of a yeast chromosomal replicator. Cell 37, 299-307.
32. Kearsey, S. E. & Labib, K. 1998 MCM proteins: evolution, properties and role in DNA replication. Biochim. Biophys. Acta 1398, 113-136.
33. Krude, T. 2000 Initiation of human DNA replication in vitro using nuclei from cells arrested at an initiation-competent state. J. Biol. Chem. 275, 13 699-13 707.
34. Krude, T., Musahl, C., Laskey, R. A. & Knippers, R. 1996 Human replication proteins hcdc21, hcdc46 and Plmcm3 bind chromatin uniformly before S-phase and are displaced locally during DNA replication. J. Cell. Sci. 109, 309-318.
35. Krude, T., Jackman, M., Pines, J. & Laskey, R. A. 1997 Cyclin/Cdk-dependent initiation of DNA replication in a human cell-free system. Cell 88, 109-119.
36. Kubota, Y., Mimura, S., Nishimoto, S.-I., Takisawa, H. & Nojima, H. 1995 Identification of the yeast MCM3 related protein as a component of Xenopus DNA replication licensing factor. Cell 81, 601-609.
37. Laskey, R. A. 2003 DNA and cancer. In DNA: Changing Science and Society (ed. T. Krude), pp. 88-106. Cambridge University Press.
38. Laskey, R. A. & Harland, R. M. 1981 Replication origins in the eukaryotic chromosome. Cell 24, 283-284.
39. Laskey, R. A. & Madine, M. A. 2003 A rotary pumping model for helicase function of MCM proteins at a distance from replication forks. EMBO Rep. 4, 26-30.
40. Laskey, R. A., Harland, R. M., Earnshaw, W. C. & Dingwall, C. 1981 Chromatin assembly and the co-ordination of DNA replication in the eukaryotic chromosome. In International cell biology (ed. H. Schweiger), pp. 162-167. Heidelberg: Springer.
41. Madine, M. A., Khoo, C.-Y., Mills, A. D. & Laskey, R. A. 1995a MCM3 complex required for cell cycle regulation of DNA replication in vertebrate cells. Nature 375, 421-424.
42. Madine, M., Khoo, C.-Y., Mills, A. D., Musahl, C. & Laskey, R. A. 1995b The nuclear envelope prevents reinitiation of replication by regulating the binding of MCM3 to chromatin in Xenopus egg extracts. Curr. Biol. 5, 1270-1279.
43. Madine, M. A., Swietlik, M., Pelizon, C., Romanowski, P., Mills, A. D. & Laskey, R. A. 2000 The roles of the MCM, Orc and Cdc6 proteins in determining the replication competence of chromatin in quiescent cells. J. Struct. Biol. 129, 198-210.
44. Méchali, M. & Kearsey, S. E. 1984 Lack of specific sequence requirement for DNA replication in Xenopus eggs compared with high sequence specificity in yeast. Cell 38, 55-64.
45. Mills, A. D., Coleman, N., Morris, L. S. & Laskey, R. A. 2000 Detection of S-phase cells in tissue sections by in situ DNA replication. Nat. Cell. Biol. 2, 244-245.
46. Musahl, C., Holthoff, H. P., Lesch, R. & Knippers, R. 1998 Stability of the replicative Mcm3 protein in proliferating and differentiating human cells. Exp. Cell. Res. 241, 260-264.
47. Newport, J. & Kirschner, M. 1982 A major developmental transition in early Xenopus embryos. I. Characterization and timing of cellular changes at the midblastula stage. Cell 30, 675-686.
48. Nurse, P. M. 2002 Cyclin dependent kinases and cell cycle control. Chembiochem 3, 596-603.
49. Romanowski, P., Madine, M. A., Rowles, A., Blow, J. J. & Laskey, R. A. 1996 The Xenopus origin recognition complex is essential for DNA replication and MCM binding to chromatin. Curr. Biol. 6, 1416-1425.
50. Sato, M., Gotow, R., You, Z., Komamura-Kohno, Y., Uchiyama, Y., Yabuta, N., Nojima, H. & Ishimi, Y. 2000 Electron microscopic observation and single-stranded DNA binding activity of the Mcm4, 6, 7 complex. J. Mol. Biol. 300, 421-431.
51. Scholzen, T. & Gerdes, J. 2000 Ki-67 protein from the known and the unknown. J. Cell. Physiol. 182, 311-322.
52. Schwacha, A. & Bell, S. P. 2001 Interactions between two catalytically distinct MCM sub-groups are essential for coordinated ATP hydrolysis and DNA replication. Mol. Cell 8, 1093-1104.
53. Shreeram, S. & Blow, J. J. 2003 The role of the replication licensing system in cell proliferation and cancer. Prog. Cell Cycle Res. 5, 287-293.
54. Simpson, A. A. et al. 2000 Structure of the bacteriophage Φ29 DNA packaging motor. Nature 408, 745-750.
55. Sirieix, P. A., O'Donovan, M., Brown, J., Save, V., Coleman, N. & Fitzgerald, R. C. 2003 Surface expression of mini-chromosome maintenance proteins provides a novel method for detecting patients at risk for developing adenocarcinoma in Barrett's esophagus. Clin. Cancer Res. 9, 2560-2566.
56. Stoeber, K., Mills, A. D., Kubota, Y., Krude, T., Romanowski, P., Marheineke, K., Laskey, R. A. & Williams, G. H. 1998 Cdc6 protein causes premature entry into S phase in a mammalian cell-free system. EMBO J. 17, 7219-7229.
57. Stoeber, K. et al. 1999 Immunoassay for urothelial cancers that detects DNA-replication protein Mcm5 in urine. Lancet 354, 1524-1525.
58. Tachibana, K. K., Gonzalez, M. A. & Coleman, N. 2005 Cell-cycle-dependent regulation of DNA replication and its relevance to cancer pathology. J. Pathol. 205, 123-129.
59. Tada, S., Li, A., Maiorano, D., Méchali, M. & Blow, J. J. 2001 Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat. Cell. Biol. 3, 107-113.
60. Takei, Y., Swietlik, M., Tanoue, A., Tsujimoto, J., Kouzarides, T. & Laskey, R. 2001 MCM3AP, a novel acetyltransferase that acetylates replication protein MCM3. EMBO Rep. 2, 119-123.
61. Takei, Y., Assenberg, M., Tsujimoto, G. & Laskey, R. 2002 The MCM3 acetylase MCM3AP inhibits initiation, but not elongation of DNA replication via interaction with MCM3. J. Biol. Chem. 277, 43 121-43 125.
62. Todorov, I. T., Attaran, A. & Kearsey, S. E. 1995 BM28, a human member of the Mcm2-3-5 family is displaced from chromatin during DNA replication. J. Cell. Biol. 129, 1433-1445.
63. Todorov, I. T., Werness, B. A., Wang, H. Q., Buddharajul, N., Todorova, P. D., Slocum, H. K., Brooks, J. S. & Huberman, J. A. 1998 HsMcm2/BM28: a novel proliferation marker for human tumours and normal tissues. Lab. Invest. 78, 73-78.
64. Tye, B. K. 1999 MCM proteins in DNA replication. Annu. Rev. Biochem. 68, 649-686.
65. Williams, G. H., Romanowski, P., Mills, A. D., Morris, L., Stoeber, K., Marr, J., Laskey, R. A. & Coleman, N. C. 1998 Improved cervical smear assessment using antibodies against proteins that regulate DNA replication. Proc. Natl Acad. Sci. USA 95, 14 932-14 937.
66. Wohlschlegel, J. A., Dwyer, B. T., Dhar, S. K., Cvetic, C., Walter, J. C. & Dutta, A. 2000 Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290, 2309-2312.
67. Zhou, B. S. & Elledge, S. J. 2000 The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439.