From polyploidy to aneuploidy, genome instability and cancer

Nature Reviews Molecular Cell Biology

Volumn 5, Issue 1, 2004, Pages 45-54

  Storchova, Zuzana ^a   Pellman, David ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANEUPLOIDY; CANCER; CARCINOGENESIS; CELL CYCLE; CELL FUSION; CELL MATURATION; CELL SIZE; CENTROSOME; DIPLOIDY; EUKARYOTE; EVOLUTION; POLYPLOIDY; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENTIATION; STRESS;

ANEUPLOIDY; ANIMALS; EVOLUTION; GENOMIC INSTABILITY; HUMANS; MODELS, GENETIC; NEOPLASMS; POLYPLOIDY;

EUKARYOTA;

EID: 0347762556     PISSN: 14710072     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrm1276     Document Type: Review

References (125)

1. Stebbins, G. L. Types of polyploids: their classification and significance. Adv. Genet. 1, 403-429 (1947).
2. Otto, S. P. & Whitton, J. Polyploid incidence and evolution. Annu. Rev. Genet. 34, 401-437 (2000).
3. Taylor, M. V. Muscle differentiation: how two cells become one. Curr. Biol. 12, R224-R228 (2002).
4. Vignery, A. Osteoclasts and giant cells: macrophage-macrophage fusion mechanism. Int. J. Exp. Pathol. 81, 291-304 (2000).
5. Deaven, L. L. & Kreizinger, J. D. Cell fusion as a mechanism for the origin of polyploid cells in vitro. Experientia 27, 311-313 (1971).
6. Secchiero, P. et al. Human herpesvirus 7 infection induces profound cell cycle perturbations coupled to disregulation of cdc2 and cyclin B and polyploidization of CD4(+) T cells. Blood 92, 1685-1696 (1998).
7. Hernandez, L. D., Hoffman, L. R., Wolfsberg, T. G. & White, J. M. Virus-cell and cell-cell fusion. Annu. Rev. Cell Dev. Biol. 12, 627-661 (1996).
8. Blau, H. M., Brazelton, T. R. & Weimann, J. M. The evolving concept of a stem cell: entity or function? Cell 105, 829-841 (2001).
9. Terada, N. et al. Bone marrow cells adopt the phenotype of other cells by spontaneous cell fusion. Nature 416, 542-545 (2002).
10. Vassilopoulos, G., Wang, P. R. & Russell, D. W. Transplanted bone marrow regenerates liver by cell fusion, Nature 422, 901-904 (2003).
11. Wang, X. et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 422, 897-901 (2003). One of several examples of stem-cell plasticity that occurs by cell fusion. Uniquely, it shows that the polyploid fusion product can generate cells of normal ploidy by reduction mitosis.
12. Yang, Y., Geldmacher, D. S. & Herrup, K. DNA replication precedes neuronal cell death in Alzheimer's disease. J. Neurosci. 21, 2661-2668 (2001).
13. Edgar, B. A. & Orr-Weaver, T. L. Endoreplication cell cycles: more for less. Cell 105, 297-306 (2001).
14. Zimmet, J. & Ravid, K. Polyploidy: occurrence in nature, mechanisms, and significance for the megakaryocyte-platelet system. Exp. Hematol. 28, 3-16 (2000).
15. Cebolla, A. et al. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J. 18, 4476-4484 (1999).
16. Kondorosi, E., Roudier, F. & Gendreau, E. Plant cell-size control: growing by ploidy? Curr. Opin. Plant Biol. 3, 488-492 (2000).
17. Ravid, K., Lu, J., Zimmet, J. M. & Jones, M. R. Roads to polyploidy: the megakaryocyte example. J. Cell Physiol. 190, 7-20 (2002).
18. Smith, A. V. & Orr-Weaver, T. L. The regulation of the cell cycle during Drosophila embryogenesis: the transition to polyteny. Development 112, 997-1008 (1991).
19. Nagata, Y., Muro, Y. & Todokoro, K. Thrombopoietin-induced polyploidization of bone marrow megakaryocytes is due to a unique regulatory mechanism in late mitosis. J. Cell Biol. 139, 449-457 (1997).
20. Waizenegger, I., Gimenez-Abian, J. F., Wernic, D. & Peters, J. M. Regulation of human separase by securin binding and autocleavage. Curr. Biol. 12, 1368-1378 (2002).
21. Minn, A. J., Boise, L. H. & Thompson, C. B. Expression of Bcl-xL and loss of p53 can cooperate to overcome a cell cycle checkpoint induced by mitotic spindle damage. Genes Dev. 10, 2621-2631 (1996).
22. Lanni, J. S. & Jacks, T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18, 1055-1064 (1998).
23. Andreassen, P. R., Lohez, O. D., Lacroix, F. B. & Margolis, R. L. N. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Mol. Biol. Cell 12, 1315-1328 (2001).
24. Elledge, S. J. Cell cycle checkpoints: preventing an identity crisis. Science 274, 1664-1672 (1996).
25. Andreassen, P. R., Martineau, S. N. & Margolis, R. L. N. Chemical induction of mitotic checkpoint override in mammalian cells results in aneuploidy following a transient tetraploid state. Mutat. Res. 372, 181-194 (1996). A new checkpoint that functions in G1 to block the proliferation of tetraploid cells. The checkpoint is p53 dependent and its failure results in aneuploidy.
26. Sauer, K., Knoblich, J. A., Richardson, H. & Lehner, C. F. Distinct modes of cyclin E/cdc2c kinase regulation and S-phase control in mitotic end endoreduplication cycles of Drosophila embryogenesis. Genes Dev. 9, 1327-1339 (1995).
27. Guidotti, J. E. et al. Liver cell polyploidization: a pivotal role for binuclear hepatocytes. J. Biol. Chem. 278, 19095-19101 (2003). Polyploid hepatocytes are formed by mitotic failure. The polyploids proceed through mitosis with a bipolar spindle by clustering extra chromosomes.
28. Goda, G. R., Malhi, H. & Gupta, S. Polyploidy associated with oxidative injury attenuates proliferative potential of cells. J. Cell Sci. 114, 2943-2951 (2001).
29. Gupta, S. Hepatic polyploidy and liver growth control. Semin, Cancer Biol. 10, 161-171 (2000).
30. Vliegen, H. W., Eulderink, F., Bruschke, A. V., van der Laarse, A. & Cornelisse, C. J. Polyploidy of myocyte nuclei in pressure overloaded human hearts: a flow cytometric study in left and right ventricular myocardium. Am. J. Cardiovasc. Pathol. 5, 27-31 (1995).
31. Hixon, M. L. et al. Cks 1 mediates vascular smooth muscle cell polyploidization. J. Biol. Chem. 275, 40434-40442 (2000).
32. Oberringer, M. et al. Centrosome multiplication accompanies a transient clustering of polyploid cells during tissue repair. Mol. Cell Biol. Res. Commun. 2, 190-196 (1999).
33. Kudryavtsev, B. N., Kudryavtseva, M. V., Sakuta, G. A. & Stein, G. I. Human hepatocyte polyploidization kinetics in the course of life cycle. Virchows Arch. B Cell Pathol. Incl. Mol. Pathol. 64, 387-393 (1993).
34. Wagner, M. et al. Replicative senescence of human endothelial cells in vitro involves G1 arrest, polyploidization and senescence-associated apoptosis. Exp. Gerontol. 36, 1327-1347 (2001).
35. Smogorzewska, A. & de Lange, T. Different telomere damage signaling pathways in human and mouse cells. EMBO J. 21, 4338-4348 (2002).
36. Galipeau, P. C. et al. 17p (p53) allelic losses, 4N (G2/tetraploid) populations, and progression to aneuploidy in Barrett's esophagus. Proc. Natl Acad. Sci. USA 93, 7081-7084 (1996). Increased tetraploid populations in Barrett's oesophagus predict progression to aneuploidy, and the development of ploidy abnormalities is interdependent with inactivation of the p53 gene in vivo.
37. Margolis, R. L., Lohez, O. D. & Andreassen, P. R. G1 tetraploidy checkpoint and the suppression of tumorigenesis. J. Cell. Biochem. 88, 673-683 (2003).
38. Vinogradov, A. E., Anatskaya, O. V. & Kudryavtsev, B. N. Relationship of hepatocyte ploidy levels with body size and growth rate in mammals. Genome 44, 350-360 (2001). Comparison of hepatocyte ploidy levels and its relationship to body size, postnatal growth rate and postnatal-development type. The study shows the interdependency of liver ploidy and the maximal metabolic rate.
39. Brodsky, V. & Delone, G. V. Functional control of hepatocyte proliferation. Comparison with the temporal control of cardiomyocyte proliferation. Biomed. Sci, 1, 467-470 (1990).
40. Torres, S. et al. Thyroid hormone regulation of rat hepatocyte proliferation and polyploidization. Am. J. Physiol. 276, G155-G163 (1999).
41. Mable, B. K. & Otto, S. P. Masking and purging mutations following EMS treatment in haploid, diploid and tetraploid yeast (Saccharomyces cerevisiae). Genet. Res. 77, 9-26 (2001).
42. Mortimer, R. K. Radiobiological and genetic studies on a polyploid series (haploid to hexaploid) of Saccharomyces cerevisiae. Radiat. Res. 9, 312-326 (1958).
43. Epstein, C. J. Cell size, nuclear content, and the development of polyploidy in the mammalian liver. Proc. Natl Acad. Sci. USA 57, 327-334 (1967).
44. Tyson, C. B., Lord, P. G. & Wheals, A. E. Dependency of size of Saccharomyces cerevisiae cells on growth rate. J. Bacteriol. 138, 92-98 (1979).
45. Nurse, P., Thuriaux, P. & Nasmyth, K. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet. 146, 167-178 (1976).
46. Rupes, I. Checking cell size in yeast. Trends Genet, 18, 479-485 (2002).
47. Hartwell, L. H. & Unger, M. W. Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J. Cell Biol. 75, 422-435 (1977).
48. Brooks, R. F. & Shields, R. Cell growth, cell division and cell size homeostasis in Swiss 3T3 cells. Exp. Cell Res. 156, 1-6 (1985).
49. Conlon, I. J., Dunn, G. A., Mudge, A. W. & Raff, M. C. Extracellular control of cell size. Nature Cell Biol. 3, 918-921 (2001).
50. Conlon, I. & Raff, M. Differences in the way a mammalian cell and yeast cells coordinate cell growth and cell-cycle progression. J. Biol. 2, 7 (2003).
51. Schulz, H. N. & Jorgensen, B. B. Big bacteria. Annu. Rev. Microbiol. 55, 105-137 (2001).
52. Kato, N. & Lam, E. Chromatin of endoreduplicated pavement cells has greater range of movement than that of diploid guard cells in Arabidopsis thaliana. J. Cell Sci. 116, 2195-2201 (2003).
53. Mayer, V. W. & Aguilera, A. High levels of chromosome instability in polyploids of Saccharomyces cerevisae. Mutat. Res. 231, 177-186 (1990).
54. Mayer, V. W., Goin, C. J., Arras, C. A. & Taylor-Mayer, R. E. Comparison of chemically induced chromosome loss in a diploid, triploid, and tetraploid strain of Saccharomyces cerevisiae. Mutat. Res. 279, 41-48 (1992).
55. Molnar, M. & Sipiczki, M. Polyploidy in the haplontic yeast Schizosaccharomyces pombe: construction and analysis of strains. Curr. Genet. 24, 45-52 (1993).
56. Martin, G. M. & Sprague, C. A. Parasexual cycle in cultivated human somatic cells. Science 166, 761-763 (1969).
57. Lengauer, C., Kinzler, K. W. & Vogelstein, B. N. Genetic instability in colorectal cancers. Nature 386, 623-627 (1997).
58. Kondo, Y. Developmental capacity and chromosome number in the offspring of artificially produced autotetraploids of Rana nigromaculata. Zool. Sci. 19, 877-883 (2002).
59. Diter, A., Guyomard, R. & Chourrout, D. Gene segregation in induced tetraploid rainbow trout: genetic evidence of preferential pairing of homologous chromosomes. Genome 30, 547-553 (1988).
60. Galitski, T., Saldanha, A. J., Styles, C. A., Lander, E. S. & Fink, G. R. Ploidy regulation of gene expression. Science 285, 251-254 (1999). Microarray-based gene expression analysis identified genes showing ploidy-dependent expression in isogenic Saccharomyces cerevisiae strains.
61. Osborn, T. C. et al. Understanding mechanisms of novel gene expression in polyploids. Trends Genet. 19, 141-147 (2003).
62. Lin, H. et al. Polyploids require Bik 1 for kinetochore-microtubule attachment. J. Cell Biol. 155, 1173-1184 (2001).
63. Martinez-Perez, E., Shaw, P. J. & Moore, G. Polyploidy induces centromere association. J. Cell Biol. 148, 233-238 (2000).
64. Doxsey, S. Re-evaluating centrosome function. Nature Rev. Mol. Cell Biol. 2, 688-698 (2001).
65. Hinchcliffe, E. H. & Sluder, G. 'It takes two to tango': understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev. 15, 1167-1181 (2001).
66. Bartek, J. & Lukas, J. Mammalian G1- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell Biol. 13, 738-747 (2001).
67. Borel, F., Lohez, O. D., Lacroix, F. B. & Margolis, R. L. Multiple centrosomes arise from tetraploidy checkpoint failure and mitotic centrosome clusters in p53 and RB pocket protein-compromised cells. Proc. Natl Acad. Sci. USA 99, 9819-9824 (2002). Multiple-centrosome occurrence in p53- and Rb-deficient cells results from failure of the tetraploidy checkpoint rather than from a direct effect of p53 and Rb on centrosome overduplication.
68. -/- cells. EMBO J. 21, 483-492 (2002). Overexpression of Aurora A, Aurora B and Polo-like kinase results in centrosome amplification and an abortive cell cycle.
69. WAF1 induces stable G1 arrest in resulting tetraploid cells. Cancer Res. 61, 7660-7668 (2001).
70. Shackney, S. E. et al. Model for the genetic evolution of human solid tumors. Cancer Res. 49, 3344-3354 (1989).
71. Reid, B. J. et al. Barrett's esophagus: ordering the events that lead to cancer. Eur. J. Cancer Prev. 5 (Suppl. 2), 57-65 (1996).
72. Pera, F. & Rainer, B. Studies of multipolar mitoses in euploid tissue cultures. I. Somatic reduction to exactly haploid and triploid chromosome sets. Chromosoma 42, 71-86 (1973).
73. Bennett, R. J. & Johnson, A. D. Completion of a parasexual cycle in Candida albicans by induced chromosome loss in tetraploid strains. EMBO J. 22, 2505-2515 (2003).
74. Ring, D., Hubble, R. & Kirschner, M. Mitosis in a cell with multiple centrioles. J. Cell Biol. 94, 549-556 (1982).
75. Nigg, E. A. Centrosome aberrations: cause or consequence of cancer progression? Nature Rev. Cancer 2, 815-825 (2002).
76. Martin, G. M. & Sprague, C. A. Vinblastine induces multipolar mitoses in tetraploid human cells. Exp. Cell Res. 63, 466-467 (1970).
77. Mitelman, F., Johansson, B. & Mertens, F., (eds) Mitelman Database of Chromosome Aberrations in Cancer. http://cgap.nci.gov/Chromosomes/Mitelman (2003).
78. Matzke, M. A., Mette, M. F., Kanno, T. & Matzke, A. J. Does the intrinsic instability of aneuploid genomes have a causal role in cancer? Trends Genet. 19, 253-256 (2003).
79. Duesberg, P. & Rasnick, D. N. Aneuploidy, the somatic mutation that makes cancer a species of its own. Cell Motil. Cytoskeleton 47, 81-107 (2000).
80. Nowell, P. C. Genetic instability and tumor development. Basic Life Sci. 57, 221-231 (1991).
81. Cahill, D. P., Kinzler, K. W., Vogelstein, B. & Lengauer, C. Genetic instability and darwinian selection in tumours. Trends Cell Biol. 9, M57-M60 (1999).
82. Nowak, M. A. et al. The role of chromosomal instability in tumor initiation. Proc. Natl Acad. Sci. USA 99, 16226-16231 (2002).
83. Kinzler, K. W. & Vogelstein, B. Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 386, 761-763 (1997).
84. Albertson, D. G., Collins, C., McCormick, F. & Gray, J. W. Chromosome aberrations in solid tumors. Nature Genet. 34, 369-376 (2003).
85. Waldman, F. M. et al. Chromosomal alterations in ductal carcinomas in situ and their in situ recurrences. J. Natl Cancer Inst. 92, 313-320 (2000).
86. Kuukasjarvi, T. et al. Genetic heterogeneity and clonal evolution underlying development of asynchronous metastasis in human breast cancer. Cancer Res. 57, 1597-1604 (1997).
87. Kuukasjarvi, T. et al. Genetic changes in intraductal breast cancer detected by comparative genomic hybridization. Am. J. Pathol. 150, 1465-1471 (1997).
88. Lingle, W. L. et al. Centrosome amplification drives chromosomal instability in breast tumor development. Proc. Natl Acad. Sci. USA 99, 1978-1983 (2002). About 60-80% of breast cancers are aneuploid and 80% have centrosome amplification. This is independent of p53 status and positively correlates with tumour development and progression.
89. McEachern, M. J., Krauskopf, A. & Blackburn, E. H. Telomeres and their control. Annu. Rev. Genet. 34, 331-358 (2000).
90. Masutomi, K. & Hahn, W. C. Telomerase and tumorigenesis. Cancer Lett. 194, 163-172 (2003).
91. DePinho, R. A. & Wong, K. K. The age of cancer: telomeres, checkpoints, and longevity. J. Clin. Invest. 111, S9-S14 (2003).
92. Blasco, M. A. & Hahn, W. C. Evolving views of telomerase and cancer. Trends Cell Biol. 13, 289-294 (2003).
93. Kim, N. W. et al. Specific association of human telomerase activity with immortal cells and cancer. Science 266, 2011-2015 (1994).
94. Bryan, T. M., Englezou, A., Dalla-Pozza, L., Dunham, M. A. & Reddel, R. R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nature Med 3, 1271-1274 (1997).
95. Artandi, S. E. et al. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406, 641-645 (2000). Telomere attrition in ageing telomerase-deficient p53-mutant mice promotes the development of epithelial cancers by a process of fusion-bridge-breakage that leads to the formation of complex non-reciprocal translocations.
96. Boveri, T. Zur Frage der Entstehung maligner Tumoren. (Gustav Fisher Verlag, Jena, Germany, 1914).
97. D'Assoro, A. B., Lingle, W. L. & Salisbury, J. L. Centrosome amplification and the development of cancer. Oncogene 21, 6146-6153 (2002).
98. Pihan, G. A., Wallace, J., Zhou, Y. & Doxsey, S. J. Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas. Cancer Res. 63, 1398-1404 (2003). Some of the most common human cancers have centrosome defects together with mitotic spindle defects and chromosome instability even before invasion. The development of centrosome defects does not require the abrogation of p53 function.
99. Duensing, S. & Munger, K. Centrosomes, genomic instability, and cervical carcinogenesis. Crit. Rev Eukaryot. Gene Expr. 13, 9-23 (2003).
100. Fukasawa, K., Choi, T., Kuriyama, R., Rulong, S. & Vande Woude, G. F. Abnormal centrosome amplification in the absence of p53. Science 271, 1744-1747 (1996).
101. Duensing, S. & Munger, K. Centrosome abnormalities, genomic instability and carcinogenic progression. Biochim. Biophys. Acta 1471, M81-M88 (2001).
102. Zhou, H. et al. Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nature Genet. 20, 189-193 (1998).
103. Kaneko, Y. & Knudson, A. G. Mechanism and relevance of ploidy in neuroblastoma. Genes Chromosom. Cancer 29, 89-95 (2000).
104. Levine, D. S., Sanchez, C. A., Rabinovitch, P. S. & Reid, B. J. Formation of the tetraploid intermediate is associated with the development of cells with more than four centrioles in the elastase-simian virus 40 tumor antigen transgenic mouse model of pancreatic cancer. Proc. Natl Acad. Sci. USA 88, 6427-6431 (1991).
105. Hartwell, L. H., Szankasi, P., Roberts, C. J., Murray, A. W. & Friend, S. H. Integrating genetic approaches into the discovery of anticancer drugs. Science 278, 1064-1068 (1997).
106. Kamb, A. Consequences of nonadaptive alterations in cancer. Mol. Biol. Cell 14, 2201-2205 (2003).
107. Wendel, J. F. Genome evolution in polyploids. Plant Mol. Biol. 42, 225-249 (2000).
108. Soltis, D. E. & Soltis, P. S. Polyploidy: recurrent formation and genome evolution. Trends Ecol. Evol. 14, 348-352 (1999).
109. Wolfe, K. H. Yesterday's polyploids and the mystery of diploidization. Nature Rev. Genet. 2, 333-341 (2001).
110. Beaton, M. J. & Hebert, P. N. Geographical parthenogenesis and polyploidy in Daphnia pulex. Am. Nat. 132, 837-845 (1988).
111. Becak, M. L. & Becak, W. Evolution by polyploidy in Amphibia: new insights. Cytogenet. Cell Genet 80, 28-33 (1998).
112. Bogart, J. P. & Licht, L. E. Reproduction and the origin of polyploids in hybrid salamanders of the genus Ambystoma. Can. J. Genet. Cytol. 28, 605-617 (1986).
113. Ohno, S., Wolf, U. & Atkin, N. B. Evolution from fish to mammals by gene duplication. Hereditas 59, 169-187 (1968).
114. Makalowski, W. Are we polyploids? A brief history of one hypothesis. Genome Res. 11, 667-670 (2001).
115. Bailey, J. A. et al. Recent segmental duplications in the human genome. Science 297, 1003-1007 (2002).
116. Comai, L. Genetic and epigenetic interactions in allopolyploid plants. Plant Mol. Biol. 43, 387-399 (2000).
117. Polymenis, M. & Schmidt, E. V. Coupling of cell division to cell growth by translational control of the G1 cyclin CLN3 in yeast. Genes Dev. 11, 2522-2531 (1997).
118. Berset, C., Trachsel, H. & Altmann, M. The TOR (target of rapamycin) signal transduction pathway regulates the stability of translation initiation factor elF4G in the yeast Saccharomyces cerevisae. Proc. Natl Acad. Sci. USA 95, 4264-4269 (1998).
119. Jorgensen, P., Nishikawa, J. L., Breitkreutz, B. J. & Tyers, M. Systematic identification of pathways that couple cell grcwth and division in yeast. Science 297, 395-400 (2002).
120. Zhang, J. et al. Genomic scale mutant hunt identifies cell size homeostasis genes in S. cerevisiae. Curr. Biol. 12, 1992-2001 (2002).
121. Coelho, C. M. & Leevers, S. J. Do growth and cell division rates determine cell size in multicellular organisms? J. Cell Sci. 113, 2927-2934 (2000).
122. Montagne, J. et al. Drosophila S6 kinase: a regulator of cell size. Science 285, 2126-2129 (1999).
123. Chung, J., Kuo, C. J., Crabtree, G. R. & Blenis, J. Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell 69, 1227-1236 (1992).
124. Nelsen, C. J., Rickheim, D. G., Tucker, M. M., Hansen, L. K. & Albrecht, J. H. Evidence that cyclin D1 mediates both growth and proliferation downstream of TOR in hepatocytes. J. Biol. Chem. 278, 3656-3663 (2003).
125. Mitchison, J. M. Growth during the cell. Int. Rev. Cytol. 226, 165-258 (2003).