Road to the crossroads of life and death: Linking sister chromatid cohesion and separation to aneuploidy, apoptosis and cancer

Critical Reviews in Oncology/Hematology

Volumn 72, Issue 3, 2009, Pages 181-193

  Panigrahi, Anil K ^a   Pati, Debananda ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Aneuploidy; Apoptosis; Cohesin; Rad21; Separase

Indexed keywords

COHESIN; PROMOTER OF ANEUPLOIDY PROTEIN; PROTEIN P53; REGULATOR PROTEIN; RETINOBLASTOMA PROTEIN; SEPARASE; UNCLASSIFIED DRUG;

ANEUPLOIDY; APOPTOSIS; CANCER GENETICS; CANCER RISK; CARCINOGENESIS; CELL ADHESION; CELL DEATH; CELL PROLIFERATION; CELL SEPARATION; CHROMOSOME SEGREGATION; GENE MUTATION; GENOMIC INSTABILITY; HUMAN; MITOSIS; NONHUMAN; PROGNOSIS; PROTEIN FUNCTION; REVIEW; SISTER CHROMATID;

ANEUPLOIDY; ANIMALS; APOPTOSIS; HUMANS; MUTATION; NEOPLASMS; SISTER CHROMATID EXCHANGE;

EID: 71549142051     PISSN: 10408428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2008.12.002     Document Type: Review

References (131)

1. Huettenbrenner S., Maier S., Leisser C., et al. The evolution of cell death programs as prerequisites of multicellularity. Mutat Res 543 3 (2003) 235-249
2. Hipfner D.R., and Cohen S.M. Connecting proliferation and apoptosis in development and disease. Nat Rev Mol Cell Biol 5 10 (2004) 805-815
3. Green D.R., and Evan G.I. A matter of life and death. Cancer Cell 1 1 (2002) 19-30
4. Vermeulen K., Van Bockstaele D.R., and Berneman Z.N. Apoptosis: mechanisms and relevance in cancer. Ann Hematol 84 10 (2005) 627-639
5. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 1 (2000) 57-70
6. Vogelstein B., and Kinzler K.W. The multistep nature of cancer. Trends Genet 9 4 (1993) 138-141
7. Weinberg R.A. Oncogenes, antioncogenes, and the molecular bases of multistep carcinogenesis. Cancer Res 49 14 (1989) 3713-3721
8. Nowell P.C. The clonal evolution of tumor cell populations. Science 194 4260 (1976) 23-28
9. Tomlinson I.P., Novelli M.R., and Bodmer W.F. The mutation rate and cancer. Proc Natl Acad Sci USA 93 25 (1996) 14800-14803
10. Jackson A.L., and Loeb L.A. The mutation rate and cancer. Genetics 148 4 (1998) 1483-1490
11. Hahn W.C., and Weinberg R.A. Modelling the molecular circuitry of cancer. Nat Rev Cancer 2 5 (2002) 331-341
12. Prehn R.T. Cancers beget mutations versus mutations beget cancers. Cancer Res 54 20 (1994) 5296-5300
13. Soto A.M., and Sonnenschein C. The somatic mutation theory of cancer: growing problems with the paradigm?. Bioessays 26 10 (2004) 1097-1107
14. Strickland J.E., Ueda M., Hennings H., and Yuspa S.H. A model for initiated mouse skin: suppression of papilloma but not carcinoma formation by normal epidermal cells in grafts on athymic nude mice. Cancer Res 52 6 (1992) 1439-1444
15. Anderson E. The role of oestrogen and progesterone receptors in human mammary development and tumorigenesis. Breast Cancer Res 4 5 (2002) 197-201
16. Manchester K.L. Theodor Boveri and the origin of malignant tumours. Trends Cell Biol 5 10 (1995) 384-387
17. Duesberg P., Li R., Fabarius A., and Hehlmann R. Aneuploidy and cancer: from correlation to causation. Contrib Microbiol 13 (2006) 16-44
18. Marx J. Debate surges over the origins of genomic defects in cancer. Science 297 5581 (2002) 544-546
19. Cahill D.P., Lengauer C., Yu J., et al. Mutations of mitotic checkpoint genes in human cancers. Nature 392 6673 (1998) 300-303
20. Aguilera A., and Gomez-Gonzalez B. Genome instability: a mechanistic view of its causes and consequences. Nat Rev Genet 9 3 (2008) 204-217
21. Ionov Y., Peinado M.A., Malkhosyan S., Shibata D., and Perucho M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature 363 6429 (1993) 558-561
22. Esteller M. Epigenetics in cancer. N Engl J Med 358 11 (2008) 1148-1159
23. Feinberg A.P., Ohlsson R., and Henikoff S. The epigenetic progenitor origin of human cancer. Nat Rev Genet 7 1 (2006) 21-33
24. Teixeira M.R., and Heim S. Multiple numerical chromosome aberrations in cancer: what are their causes and what are their consequences?. Semin Cancer Biol 15 1 (2005) 3-12
25. Gagos S., and Irminger-Finger I. Chromosome instability in neoplasia: chaotic roots to continuous growth. Int J Biochem Cell Biol 37 5 (2005) 1014-1033
26. Rajagopalan H., and Lengauer C. Aneuploidy and cancer. Nature 432 7015 (2004) 338-341
27. Duesberg P., and Li R. Multistep carcinogenesis: a chain reaction of aneuploidizations. Cell Cycle 2 3 (2003) 202-210
28. Tyzzer E.E. Tumor immunity. J Cancer Res 1 (1916) 125-155
29. Whitman R.C. Somatic mutations as a factor in the production of cancer. J Cancer Res 4 (1919) 181-202
30. Muller H.J. Artificial transmutation of the gene. Science 66 1699 (1927) 84-87
31. Fardon J.C. A reconsideration of the somatic mutation theory of cancer in the light of some recent developments. Science 117 3043 (1953) 441-445
32. Fisher J.C. Multiple-mutation theory of carcinogenesis. Nature 181 4609 (1958) 651-652
33. Land H., Parada L.F., and Weinberg R.A. Tumorigenic conversion of primary embryo fibroblasts requires at least two cooperating oncogenes. Nature 304 5927 (1983) 596-602
34. Knudson A.G. Two genetic hits (more or less) to cancer. Nat Rev Cancer 1 2 (2001) 157-162
35. Futreal P.A., Coin L., Marshall M., et al. A census of human cancer genes. Nat Rev Cancer 4 3 (2004) 177-183
36. Steen H.B. The origin of oncogenic mutations: where is the primary damage?. Carcinogenesis 21 10 (2000) 1773-1776
37. Cairns J. Somatic stem cells and the kinetics of mutagenesis and carcinogenesis. Proc Natl Acad Sci USA 99 16 (2002) 10567-10570
38. Sonnenschein C., and Soto A.M. Somatic mutation theory of carcinogenesis: why it should be dropped and replaced. Mol Carcinog 29 4 (2000) 205-211
39. Mitelman F, Johansson B, Mertens FE. Mitelman database of chromosome aberrations in cancer. http://cgap.nci.nih.gov/chromosomes/mitelman; 2006.
40. Frankfurt O.S., Chin J.L., Englander L.S., Greco W.R., Pontes J.E., and Rustum Y.M. Relationship between DNA ploidy, glandular differentiation, and tumor spread in human prostate cancer. Cancer Res 45 3 (1985) 1418-1423
41. Ried T., Heselmeyer-Haddad K., Blegen H., Schrock E., and Auer G. Genomic changes defining the genesis, progression, and malignancy potential in solid human tumors: a phenotype/genotype correlation. Genes Chromosomes Cancer 25 3 (1999) 195-204
42. Pilch H., Gunzel S., Schaffer U., Tanner B., and Heine M. Evaluation of DNA ploidy and degree of DNA abnormality in benign and malignant melanocytic lesions of the skin using video imaging. Cancer 88 6 (2000) 1370-1377
43. Duesberg P., Rausch C., Rasnick D., and Hehlmann R. Genetic instability of cancer cells is proportional to their degree of aneuploidy. Proc Natl Acad Sci USA 95 23 (1998) 13692-13697
44. Choma D., Daures J.P., Quantin X., and Pujol J.L. Aneuploidy and prognosis of non-small-cell lung cancer: a meta-analysis of published data. Br J Cancer 85 1 (2001) 14-22
45. Ikeguchi M., Ohfuji S., Oka A., Tsujitani S., Maeta M., and Kaibara N. Aneuploidy of tumor cells in cases of gastric cancer with esophageal invasion: another indicator of poor prognosis. J Surg Oncol 58 2 (1995) 83-90
46. Sciallero S., Giaretti W., Geido E., et al. DNA aneuploidy is an independent factor of poor prognosis in pancreatic and peripancreatic cancer. Int J Pancreatol 14 1 (1993) 21-28
47. Kearney T.J., Price E.A., Lee S., and Silberman A.W. Tumor aneuploidy in young patients with colorectal cancer. Cancer 72 1 (1993) 42-45
48. Nakopoulou L., Panayotopoulou E.G., Giannopoulou I., et al. Extra copies of chromosomes 16 and X in invasive breast carcinomas are related to aggressive phenotype and poor prognosis. J Clin Pathol 60 7 (2007) 808-815
49. Carter S.L., Eklund A.C., Kohane I.S., Harris L.N., and Szallasi Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet 38 9 (2006) 1043-1048
50. Fabarius A., Hehlmann R., and Duesberg P.H. Instability of chromosome structure in cancer cells increases exponentially with degrees of aneuploidy. Cancer Genet Cytogenet 143 1 (2003) 59-72
51. Willenbucher R.F., Aust D.E., Chang C.G., et al. Genomic instability is an early event during the progression pathway of ulcerative-colitis-related neoplasia. Am J Pathol 154 6 (1999) 1825-1830
52. Shih I.M., Zhou W., Goodman S.N., Lengauer C., Kinzler K.W., and Vogelstein B. Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. Cancer Res 61 3 (2001) 818-822
53. Aardema M.J., Albertini S., Arni P., et al. Aneuploidy: a report of an ECETOC task force. Mutat Res 410 1 (1998) 3-79
54. Ai H., Barrera J.E., Meyers A.D., Shroyer K.R., and Varella-Garcia M. Chromosomal aneuploidy precedes morphological changes and supports multifocality in head and neck lesions. Laryngoscope 111 10 (2001) 1853-1858
55. Medina D. Biological and molecular characteristics of the premalignant mouse mammary gland. Biochim Biophys Acta 1603 1 (2002) 1-9
56. Amiel A., Gronich N., Yukla M., et al. Random aneuploidy in neoplastic and pre-neoplastic diseases, multiple myeloma, and monoclonal gammopathy. Cancer Genet Cytogenet 162 1 (2005) 78-81
57. Duesberg P., and Rasnick D. Aneuploidy, the somatic mutation that makes cancer a species of its own. Cell Motil Cytoskeleton 47 2 (2000) 81-107
58. Weaver B.A., and Cleveland D.W. Aneuploidy: instigator and inhibitor of tumorigenesis. Cancer Res 67 21 (2007) 10103-10105
59. Dutrillaux B., Gerbault-Seureau M., Remvikos Y., Zafrani B., and Prieur M. Breast cancer genetic evolution: I. Data from cytogenetics and DNA content. Breast Cancer Res Treat 19 3 (1991) 245-255
60. Kops G.J., Weaver B.A., and Cleveland D.W. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5 10 (2005) 773-785
61. Duesberg P., Fabarius A., and Hehlmann R. Aneuploidy, the primary cause of the multilateral genomic instability of neoplastic and preneoplastic cells. IUBMB Life 56 2 (2004) 65-81
62. Lofberg R., Lindquist K., Veress B., and Tribukait B. Highly malignant carcinoma in chronic ulcerative colitis without preceding dysplasia or DNA aneuploidy. Report of a case. Dis Colon Rectum 35 1 (1992) 82-86
63. Dohner K., and Dohner H. Molecular characterization of acute myeloid leukemia. Haematologica 93 7 (2008) 976-982
64. Lengauer C., Kinzler K.W., and Vogelstein B. Genetic instabilities in human cancers. Nature 396 6712 (1998) 643-649
65. Muleris M., Chalastanis A., Meyer N., et al. Chromosomal instability in near-diploid colorectal cancer: a link between numbers and structure. PLoS ONE 3 2 (2008) e1632
66. Baer C.F., Miyamoto M.M., and Denver D.R. Mutation rate variation in multicellular eukaryotes: causes and consequences. Nat Rev Genet 8 8 (2007) 619-631
67. Filee J., Forterre P., Sen-Lin T., and Laurent J. Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J Mol Evol 54 6 (2002) 763-773
68. Lindahl T. Instability and decay of the primary structure of DNA. Nature 362 6422 (1993) 709-715
69. Ruley H.E. Adenovirus early region 1A enables viral and cellular transforming genes to transform primary cells in culture. Nature 304 5927 (1983) 602-606
70. Kiyono T., Foster S.A., Koop J.I., McDougall J.K., Galloway D.A., and Klingelhutz A.J. Both Rb/p16INK4a inactivation and telomerase activity are required to immortalize human epithelial cells. Nature 396 6706 (1998) 84-88
71. Hahn W.C., Counter C.M., Lundberg A.S., Beijersbergen R.L., Brooks M.W., and Weinberg R.A. Creation of human tumour cells with defined genetic elements. Nature 400 6743 (1999) 464-468
72. Li R., Sonik A., Stindl R., Rasnick D., and Duesberg P. Aneuploidy vs. gene mutation hypothesis of cancer: recent study claims mutation but is found to support aneuploidy. Proc Natl Acad Sci USA 97 7 (2000) 3236-3241
73. Sussan T.E., Yang A., Li F., Ostrowski M.C., and Reeves R.H. Trisomy represses Apc(Min)-mediated tumours in mouse models of Down's syndrome. Nature 451 7174 (2008) 73-75
74. Baker D.J., Jeganathan K.B., Cameron J.D., et al. BubR1 insufficiency causes early onset of aging-associated phenotypes and infertility in mice. Nat Genet 36 7 (2004) 744-749
75. Williams B.R., Prabhu V.R., Hunter K.E., et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 322 5902 (2008) 703-709
76. Weinberg R.A. The retinoblastoma protein and cell cycle control. Cell 81 3 (1995) 323-330
77. Sellers W.R., and Kaelin Jr. W.G. Role of the retinoblastoma protein in the pathogenesis of human cancer. J Clin Oncol 15 11 (1997) 3301-3312
78. Riley T., Sontag E., Chen P., and Levine A. Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9 5 (2008) 402-412
79. Phillips J.L., Hayward S.W., Wang Y., et al. The consequences of chromosomal aneuploidy on gene expression profiles in a cell line model for prostate carcinogenesis. Cancer Res 61 22 (2001) 8143-8149
80. Upender M.B., Habermann J.K., McShane L.M., et al. Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells. Cancer Res 64 19 (2004) 6941-6949
81. Hyman E., Kauraniemi P., Hautaniemi S., et al. Impact of DNA amplification on gene expression patterns in breast cancer. Cancer Res 62 21 (2002) 6240-6245
82. Pollack J.R., Sorlie T., Perou C.M., et al. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proc Natl Acad Sci USA 99 20 (2002) 12963-12968
83. Virtaneva K., Wright F.A., Tanner S.M., et al. Expression profiling reveals fundamental biological differences in acute myeloid leukemia with isolated trisomy 8 and normal cytogenetics. Proc Natl Acad Sci USA 98 3 (2001) 1124-1129
84. Bohlander S.K. Fusion genes in leukemia: an emerging network. Cytogenet Cell Genet 91 1-4 (2000) 52-56
85. Redner R.L., and Liu J.M. Leukemia fusion proteins and co-repressor complexes: changing paradigms. J Cell Biochem 94 5 (2005) 864-869
86. Schmitt C.A. Senescence, apoptosis and therapy-cutting the lifelines of cancer. Nat Rev Cancer 3 4 (2003) 286-295
87. Vicencio J.M., et al. Senescence, apoptosis or autophagy? When a damaged cell must decide its path-a mini-review. Gerontology 54 2 (2008) 92-99
88. Zhivotovsky B., and Kroemer G. Apoptosis and genomic instability. Nat Rev Mol Cell Biol 5 9 (2004) 752-762
89. Baixeras E., Bosca L., Stauber C., et al. From apoptosis to autoimmunity: insights from the signaling pathways leading to proliferation or to programmed cell death. Immunol Rev 142 (1994) 53-91
90. Evan G.I., and Vousden K.H. Proliferation, cell cycle and apoptosis in cancer. Nature 411 6835 (2001) 342-348
91. Blagosklonny M.V. Apoptosis, proliferation, differentiation: in search of the order. Semin Cancer Biol 13 2 (2003) 97-105
92. Smith M.L., and Fornace Jr. A.J. Genomic instability and the role of p53 mutations in cancer cells. Curr Opin Oncol 7 1 (1995) 69-75
93. Lanni J.S., and Jacks T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol Cell Biol 18 2 (1998) 1055-1064
94. Pihan G.A., and Doxsey S.J. The mitotic machinery as a source of genetic instability in cancer. Semin Cancer Biol 9 4 (1999) 289-302
95. Lengauer C., Kinzler K.W., and Vogelstein B. Genetic instability in colorectal cancers. Nature 386 6625 (1997) 623-627
96. Goepfert T.M., McCarthy M., Kittrell F.S., et al. Progesterone facilitates chromosome instability (aneuploidy) in p53 null normal mammary epithelial cells. FASEB J 14 14 (2000) 2221-2229
97. Medina D., Kittrell F.S., Shepard A., et al. Biological and genetic properties of the p53 null preneoplastic mammary epithelium. FASEB J 16 8 (2002) 881-883
98. Medina D., Kittrell F.S., Shepard A., Contreras A., Rosen J.M., and Lydon J. Hormone dependence in premalignant mammary progression. Cancer Res 63 5 (2003) 1067-1072
99. Pati D., Haddad B.R., Haegele A., et al. Hormone-induced chromosomal instability in p53-null mammary epithelium. Cancer Res 64 16 (2004) 5608-5616
100. Zhang N., Ge G., Meyer R., et al. Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci USA 105 35 (2008) 13033-13038
101. Nasmyth K. Segregating sister genomes: the molecular biology of chromosome separation. Science 297 5581 (2002) 559-565
102. Meyer R, Fofanov V, Panigrahi A, Merchant F, Zhang N, Pati D. Overexpression and mislocalization of the chromosomal segregation protein separase in multiple human cancers. Clin Cancer Res 2009, in press.
103. Hamid T., and Kakar S.S. PTTG/securin activates expression of p53 and modulates its function. Mol Cancer 3 (2004) 18
104. Hernando E., Nahle Z., Juan G., et al. Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control. Nature 430 7001 (2004) 797-802
105. Hanks S., Coleman K., Reid S., et al. Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat Genet 36 11 (2004) 1159-1161
106. Zhang N., Kuznetsov S., Sharan S.K., Li K., Rao P.H., and Pati D. A handcuff model for the cohesin complex. J Cell Biol 183 6 (2008) 1019-1031
107. Orr-Weaver T.L. The ties that bind: localization of the sister-chromatid cohesin complex on yeast chromosomes. Cell 99 1 (1999) 1-4
108. Nasmyth K. Separating sister chromatids. Trends Biochem Sci 24 3 (1999) 98-104
109. Koshland D.E., and Guacci V. Sister chromatid cohesion: the beginning of a long and beautiful relationship. Curr Opin Cell Biol 12 3 (2000) 297-301
110. Nasmyth K., Peters J.M., and Uhlmann F. Splitting the chromosome: cutting the ties that bind sister chromatids. Science 288 5470 (2000) 1379-1385
111. Yanagida M. Cell cycle mechanisms of sister chromatid separation; roles of Cut1/separin and Cut2/securin. Genes Cells 5 1 (2000) 1-8
112. Warren W.D., Steffensen S., Lin E., et al. The Drosophila RAD21 cohesin persists at the centromere region in mitosis. Curr Biol 10 22 (2000) 1463-1466
113. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 35 (2001) 673-745
114. Amon A. Together until separin do us part. Nat Cell Biol 3 1 (2001) E12-E14
115. Onn I., Heidinger-Pauli J.M., Guacci V., Unal E., and Koshland D.E. Sister chromatid cohesion: a simple concept with a complex reality. Annu Rev Cell Dev Biol 24 (2008) 105-129
116. Hagstrom K.A., and Meyer B.J. Condensin and cohesin: more than chromosome compactor and glue. Nat Rev Genet 4 7 (2003) 520-534
117. Uhlmann F., Lottspeich F., and Nasmyth K. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1. Nature 400 6739 (1999) 37-42
118. Uhlmann F., Wernic D., Poupart M.A., Koonin E.V., and Nasmyth K. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast. Cell 103 3 (2000) 375-386
119. Waizenegger I.C., Hauf S., Meinke A., and Peters J.M. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase. Cell 103 3 (2000) 399-410
120. Tomonaga T., Nagao K., Kawasaki Y., et al. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. Genes Dev 14 21 (2000) 2757-2770
121. Hauf S., Waizenegger I.C., and Peters J.M. Cohesin cleavage by separase required for anaphase and cytokinesis in human cells. Science 293 5533 (2001) 1320-1323
122. Ciosk R., Zachariae W., Michaelis C., Shevchenko A., Mann M., and Nasmyth K. An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast. Cell 93 6 (1998) 1067-1076
123. Zou H., McGarry T.J., Bernal T., and Kirschner M.W. Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis. Science 285 5426 (1999) 418-422
124. Leismann O., Herzig A., Heidmann S., and Lehner C.F. Degradation of Drosophila PIM regulates sister chromatid separation during mitosis. Genes Dev 14 17 (2000) 2192-2205
125. Cohen-Fix O., Peters J.M., Kirschner M.W., and Koshland D. Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p. Genes Dev 10 24 (1996) 3081-3093
126. Funabiki H., Yamano H., Kumada K., Nagao K., Hunt T., and Yanagida M. Cut2 proteolysis required for sister-chromatid seperation in fission yeast. Nature 381 6581 (1996) 438-441
127. Jallepalli P.V., and Lengauer C. Chromosome segregation and cancer: cutting through the mystery. Nat Rev Cancer 1 2 (2001) 109-117
128. Zhan Q., Fan S., Bae I., et al. Induction of bax by genotoxic stress in human cells correlates with normal p53 status and apoptosis. Oncogene 9 12 (1994) 3743-3751
129. Pati D., Zhang N., and Plon S.E. Linking sister chromatid cohesion and apoptosis: role of Rad21. Mol Cell Biol 22 23 (2002) 8267-8277
130. Chen F., Kamradt M., Mulcahy M., et al. Caspase proteolysis of the cohesin component RAD21 promotes apoptosis. J Biol Chem 277 19 (2002) 16775-16781
131. Kurokawa H., Nishio K., Fukumoto H., Tomonari A., Suzuki T., and Saijo N. Alteration of caspase-3 (CPP32/Yama/apopain) in wild-type MCF-7, breast cancer cells. Oncol Rep 6 1 (1999) 33-37