Cancer stem cell division: When the rules of asymmetry are broken

Stem Cells and Development

Volumn 24, Issue 4, 2015, Pages 405-416

  Mukherjee, Subhas ^a   Kong, Jun ^b   Brat, Daniel J ^a,b,c  

^a EMORY UNIVERSITY HOSPITAL   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; AURORA B KINASE; BETA CATENIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 4; CYCLIN E; CYCLIN E1; DISC LARGE 1 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; LETHAL GIANT LARVA 2 PROTEIN; MICRORNA; MICRORNA 146A; MICRORNA 34A; MICRORNA LET7E; NOTCH1 RECEPTOR; NUCLEAR MITOTIC APPARATUS PROTEIN 1; OCTAMER TRANSCRIPTION FACTOR 4; ONCOPROTEIN; PROSPERO HOMEOBOX 1 PROTEIN; PROTEIN; PROTEIN KINASE C; PROTEIN KINASE C IOTA; PROTEIN NUMB; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 6; RGS PROTEIN; RGS1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ADRENAL CORTEX CARCINOMA; ARTICLE; ASYMMETRIC CELL DIVISION; BLADDER CARCINOMA; BRAIN TUMOR; BREAST CANCER; CANCER STEM CELL; CARCINOSARCOMA; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL POPULATION; CELL RENEWAL; CLEAR CELL CARCINOMA; COLORECTAL CARCINOMA; CUTANEOUS MELANOMA; CYSTADENOCARCINOMA; DAUGHTER CELL; ENDOMETRIOID CARCINOMA; ENDOMETRIUM CARCINOMA; ENDOSOME; EPITHELIAL MESENCHYMAL TRANSITION; GENE DELETION; GENE MUTATION; GLIOBLASTOMA; GLIOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; KIDNEY CARCINOMA; LUNG ADENOCARCINOMA; LUNG METASTASIS; MICROTUBULE; NEURAL STEM CELL; NONHUMAN; PANCREAS ADENOCARCINOMA; PANCREAS CARCINOMA; PRIORITY JOURNAL; PROTEIN DEGRADATION; SARCOMA; SMALL CELL LUNG CANCER; SQUAMOUS CELL CARCINOMA; SQUAMOUS CELL LUNG CARCINOMA; TRANSITIONAL CELL CARCINOMA; ANIMAL; CYTOLOGY; GENE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR GENE;

ANIMALS; ASYMMETRIC CELL DIVISION; GENES, CDC; GENES, NEOPLASM; HUMANS; NEOPLASTIC STEM CELLS; SIGNAL TRANSDUCTION;

EID: 84923071310     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2014.0442     Document Type: Article

References (79)

1. Knoblich JA. (2010). Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849-860.
2. Yong KJ and B Yan. (2011). The relevance of symmetric and asymmetric cell divisions to human central nervous system diseases. J Clin Neurosci 18:458-463.
3. Conklin EG. (1905). The mutation theory from the standpoint of cytology. Science 21:525-529.
4. Yamashita YM, AP Mahowald, JR Perlin and MT Fuller. (2007). Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518-521.
5. Bultje RS, DR Castaneda-Castellanos, LY Jan, YN Jan, AR Kriegstein and SH Shi. (2009). Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189-202.
6. Troy A, AB Cadwallader, Y Fedorov, K Tyner, KK Tanaka and BB Olwin. (2012). Coordination of satellite cell activation and self-renewal by Par-complex-dependent asymmetric activation of p38alpha/beta MAPK. Cell Stem Cell 11:541-553.
7. Chia W, WG Somers and H Wang. (2008). Drosophila neuroblast asymmetric divisions: cell cycle regulators, asymmetric protein localization, and tumorigenesis. J Cell Biol 180:267-272.
8. Gomez-Lopez S, RG Lerner and C Petritsch. (2014). Asymmetric cell division of stem and progenitor cells during homeostasis and cancer. Cell Mol Life Sci 71:575-597.
9. Liu J, C Sato, M Cerletti and A Wagers. (2010). Notch signaling in the regulation of stem cell self-renewal and differentiation. Curr Top Dev Biol 92:367-409.
10. Agrawal N, M Kango, A Mishra and P Sinha. (1995). Neoplastic transformation and aberrant cell-cell interactions in genetic mosaics of lethal(2)giant larvae (lgl), a tumor suppressor gene of Drosophila. Dev Biol 172:218-229.
11. Gaiano N, JS Nye and G Fishell. (2000). Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395-404.
12. Viloria-Petit AM, L David, JY Jia, T Erdemir, AL Bane, D Pinnaduwage, L Roncari, M Narimatsu, R Bose, et al. (2009). A role for the TGFbeta-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci U S A 106:14028-14033.
13. Hou C, L Ding, J Zhang, Y Jin, C Sun, Z Li, X Sun, T Zhang, A Zhang, H Li and J Gao. (2014). Abnormal cerebellar development and Purkinje cell defects in Lgl1- Pax2 conditional knockout mice. Dev Biol 395:167-181.
14. Kunnev D, I Ivanov and Y Ionov. (2009). Par-3 partitioning defective 3 homolog (C. elegans) and androgen-induced prostate proliferative shutoff associated protein genes are mutationally inactivated in prostate cancer cells. BMC Cancer 9:318.
15. Rothenberg SM, G Mohapatra, MN Rivera, D Winokur, P Greninger, M Nitta, PM Sadow, G Sooriyakumar, BW Brannigan, et al. (2010). A genome-wide screen for microdeletions reveals disruption of polarity complex genes in diverse human cancers. Cancer Res 70:2158-2164.
16. Chen G, J Kong, C Tucker-Burden, M Anand, Y Rong, F Rahman, CS Moreno, EG Van Meir, CG Hadjipanayis and DJ Brat. (2014). Human Brat ortholog TRIM3 is a tumor suppressor that regulates asymmetric cell division in glioblastoma. Cancer Res 74:4536-4548.
17. Komori H, Q Xiao, BM McCartney and CY Lee. (2014). Brain tumor specifies intermediate progenitor cell identity by attenuating beta-catenin/Armadillo activity. Development 141:51-62.
18. Arama E, D Dickman, Z Kimchie, A Shearn and Z Lev. (2000). Mutations in the beta-propeller domain of the Drosophila brain tumor (brat) protein induce neoplasm in the larval brain. Oncogene 19:3706-3716.
19. Sonoda J and RP Wharton. (2001). Drosophila brain tumor is a translational repressor. Genes Dev 15:762-773.
20. Vessey JP, G Amadei, SE Burns, MA Kiebler, DR Kaplan and FD Miller. (2012). An asymmetrically localized Staufen2- dependent RNA complex regulates maintenance of mammalian neural stem cells. Cell Stem Cell 11:517-528.
21. Heitzler P and P Simpson. (1991). The choice of cell fate in the epidermis of Drosophila. Cell 64:1083-1092.
22. Caussinus E and C Gonzalez. (2005). Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat Genet 37:1125-1129.
23. Beaucher M, E Hersperger, A Page-McCaw and A Shearn. (2007). Metastatic ability of Drosophila tumors depends on MMP activity. Dev Biol 303:625-634.
24. Janic A, L Mendizabal, S Llamazares, D Rossell and C Gonzalez. (2010). Ectopic expression of germline genes drives malignant brain tumor growth in Drosophila. Science 330:1824-1827.
25. Takahashi M, T Yoshimoto, M Shimoda, T Kono, M Koizumi, S Yazumi, Y Shimada, R Doi, T Chiba and H Kubo. (2006). Loss of function of the candidate tumor suppressor prox1 by RNA mutation in human cancer cells. Neoplasia 8:1003-1010.
26. Nagai H, Y Li, S Hatano, O Toshihito, M Yuge, E Ito, M Utsumi, H Saito and T Kinoshita. (2003). Mutations and aberrant DNA methylation of the PROX1 gene in hematologic malignancies. Genes Chromosomes Cancer 38:13-21.
27. Dudas J, T Mansuroglu, F Moriconi, F Haller, J Wilting, T Lorf, L Fuzesi and G Ramadori. (2008). Altered regulation of Prox1-gene-expression in liver tumors. BMC Cancer 8:92.
28. Versmold B, J Felsberg, T Mikeska, D Ehrentraut, J Kohler, JA Hampl, G Rohn, D Niederacher, B Betz, et al. (2007). Epigenetic silencing of the candidate tumor suppressor gene PROX1 in sporadic breast cancer. Int J Cancer 121:547-554.
29. Boulay JL, U Stiefel, E Taylor, B Dolder, A Merlo and F Hirth. (2009). Loss of heterozygosity of TRIM3 in malignant gliomas. BMC Cancer 9:71.
30. Liu Y, R Raheja, N Yeh, D Ciznadija, AM Pedraza, T Ozawa, E Hukkelhoven, H Erdjument-Bromage, P Tempst, et al. (2014). TRIM3, a tumor suppressor linked to regulation of p21(Waf1/Cip1). Oncogene 33:308-315.
31. Betschinger J, K Mechtler and JA Knoblich. (2006). Asymmetric segregation of the tumor suppressor brat regulates self-renewal in Drosophila neural stem cells. Cell 124:1241-1253.
32. Wodarz A, A Ramrath, U Kuchinke and E Knust. (1999). Bazooka provides an apical cue for Inscuteable localization in Drosophila neuroblasts. Nature 402:544-547.
33. Du Q and IG Macara. (2004). Mammalian Pins is a conformational switch that links NuMA to heterotrimeric G proteins. Cell 119:503-516.
34. Woods DF, C Hough, D Peel, G Callaini and PJ Bryant. (1996). Dlg protein is required for junction structure, cell polarity, and proliferation control in Drosophila epithelia. J Cell Biol 134:1469-1482.
35. Wodarz A and I Nathke. (2007). Cell polarity in development and cancer. Nat Cell Biol 9:1016-1024.
36. Ota J, Y Yamashita, K Okawa, H Kisanuki, S Fujiwara, M Ishikawa, Y Lim Choi, S Ueno, R Ohki, et al. (2003). Proteomic analysis of hematopoietic stem cell-like fractions in leukemic disorders. Oncogene 22:5720-5728.
37. Vang R, M Shih Ie and RJ Kurman. (2009). Ovarian lowgrade and high-grade serous carcinoma: pathogenesis, clinicopathologic and molecular biologic features, and diagnostic problems. Adv Anat Pathol 16:267-282.
38. Fukukawa C, K Ueda, T Nishidate, T Katagiri and Y Nakamura. (2010). Critical roles of LGN/GPSM2 phosphorylation by PBK/TOPK in cell division of breast cancer cells. Genes Chromosomes Cancer 49:861-872.
39. Matsumine A, A Ogai, T Senda, N Okumura, K Satoh, GH Baeg, T Kawahara, S Kobayashi, M Okada, K Toyoshima and T Akiyama. (1996). Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science 272:1020-1023.
40. Kawahara K, T Morishita, T Nakamura, F Hamada, K Toyoshima and T Akiyama. (2000). Down-regulation of beta-catenin by the colorectal tumor suppressor APC requires association with Axin and beta-catenin. J Biol Chem 275:8369-8374.
41. Yang J, W Zhang, PM Evans, X Chen, X He and C Liu. (2006). Adenomatous polyposis coli (APC) differentially regulates beta-catenin phosphorylation and ubiquitination in colon cancer cells. J Biol Chem 281:17751-17757.
42. Roeder I and R Lorenz. (2006). Asymmetry of stem cell fate and the potential impact of the niche: observations, simulations, and interpretations. Stem Cell Rev 2:171-180.
43. Habib SJ, BC Chen, FC Tsai, K Anastassiadis, T Meyer, E Betzig and R Nusse. (2013). A localized Wnt signal orients asymmetric stem cell division in vitro. Science 339:1445-1448.
44. Knoblich JA. (2008). Mechanisms of asymmetric stem cell division. Cell 132:583-597.
45. Doetsch F. (2003). A niche for adult neural stem cells. Curr Opin Genet Dev 13:543-550.
46. Espinoza I, R Pochampally, F Xing, K Watabe and L Miele. (2013). Notch signaling: targeting cancer stem cells and epithelial-to-mesenchymal transition. Onco Targets Ther 6:1249-1259.
47. Shackleton M, F Vaillant, KJ Simpson, J Stingl, GK Smyth, ML Asselin-Labat, L Wu, GJ Lindeman and JE Visvader. (2006). Generation of a functional mammary gland from a single stem cell. Nature 439:84-88.
48. Malanchi I, A Santamaria-Martinez, E Susanto, H Peng, HA Lehr, JF Delaloye and J Huelsken. (2012). Interactions between cancer stem cells and their niche govern metastatic colonization. Nature 481:85-89.
49. Zheng H, H Ying, H Yan, AC Kimmelman, DJ Hiller, AJ Chen, SR Perry, G Tonon, GC Chu, et al. (2008). Pten and p53 converge on c-Myc to control differentiation, self-renewal, and transformation of normal and neoplastic stem cells in glioblastoma. Cold Spring Harb Symp Quant Biol 73:427-437.
50. Quinn LM, J Secombe and GR Hime. (2013). Myc in stem cell behaviour: insights from Drosophila. Adv Exp Med Biol 786:269-285.
51. Harris RE, M Pargett, C Sutcliffe, D Umulis and HL Ashe. (2011). Brat promotes stem cell differentiation via control of a bistable switch that restricts BMP signaling. Dev Cell 20:72-83.
52. Kapinas K, R Grandy, P Ghule, R Medina, K Becker, A Pardee, SK Zaidi, J Lian, J Stein, A van Wijnen and G Stein. (2013). The abbreviated pluripotent cell cycle. J Cell Physiol 228:9-20.
53. Nesbit CE, JM Tersak and EV Prochownik. (1999). MYC oncogenes and human neoplastic disease. Oncogene 18:3004-3016.
54. Perez-Losada J and A Balmain. (2003). Stem-cell hierarchy in skin cancer. Nat Rev Cancer 3:434-443.
55. Besson A, RK Assoian and JM Roberts. (2004). Regulation of the cytoskeleton: an oncogenic function for CDK inhibitors? Nat Rev Cancer 4:948-955.
56. Lange C, WB Huttner and F Calegari. (2009). Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5:320-331.
57. Kondo T, S Ezzat and SL Asa. (2006). Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 6:292-306.
58. Kapinas K and AM Delany. (2011). MicroRNA biogenesis and regulation of bone remodeling. Arthritis Res Ther 13:220.
59. Page SL, KS McKim, B Deneen, TL Van Hook and RS Hawley. (2000). Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics 155:1757-1772.
60. Lerner RG and C Petritsch. (2014). A microRNA-operated switch of asymmetric-to-symmetric cancer stem cell divisions. Nat Cell Biol 16:212-214.
61. Esquela-Kerscher A and FJ Slack. (2006). Oncomirs- microRNAs with a role in cancer. Nat Rev Cancer 6:259-269.
62. Zhang D, Y Wang and S Zhang. (2014). Asymmetric cell division in polyploid giant cancer cells and low eukaryotic cells. Biomed Res Int 2014:432652.
63. Neumuller RA and JA Knoblich. (2009). Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 23:2675-2699.
64. Zhang S, I Mercado-Uribe, Z Xing, B Sun, J Kuang and J Liu. (2014). Generation of cancer stem-like cells through the formation of polyploid giant cancer cells. Oncogene 33:116-128.
65. Beroukhim R, G Getz, L Nghiemphu, J Barretina, T Hsueh, D Linhart, I Vivanco, JC Lee, JH Huang, et al. (2007). Assessing the significance of chromosomal aberrations in cancer: methodology and application to glioma. Proc Natl Acad Sci U S A 104:20007-20012.
66. Peifer M, L Fernandez-Cuesta, ML Sos, J George, D Seidel, LH Kasper, D Plenker, F Leenders, R Sun, et al. (2012). Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet 44:1104-1110.
67. Baca SC, D Prandi, MS Lawrence, JM Mosquera, A Romanel, Y Drier, K Park, N Kitabayashi, TY MacDonald, et al. (2013). Punctuated evolution of prostate cancer genomes. Cell 153:666-677.
68. Cancer Genome Atlas Research Network, C Kandoth, N Schultz, AD Cherniack, R Akbani, Y Liu, H Shen, AG Robertson, I Pashtan, et al. (2013). Integrated genomic characterization of endometrial carcinoma. Nature 497:67-73.
69. Cancer Genome Atlas Research Network. (2011). Integrated genomic analyses of ovarian carcinoma. Nature 474:609-615.
70. Seshagiri S, EW Stawiski, S Durinck, Z Modrusan, EE Storm, CB Conboy, S Chaudhuri, Y Guan, V Janakiraman, et al. (2012). Recurrent R-spondin fusions in colon cancer. Nature 488:660-664.
71. Reinhold WC, M Sunshine, H Liu, S Varma, KW Kohn, J Morris, J Doroshow and Y Pommier. (2012). CellMiner: a web-based suite of genomic and pharmacologic tools to explore transcript and drug patterns in the NCI-60 cell line set. Cancer Res 72:3499-3511.
72. Hodis E, IRWatson, GV Kryukov, ST Arold, MImielinski, JP Theurillat, E Nickerson, D Auclair, L Li, et al. (2012). A landscape of drivermutations in melanoma. Cell 150:251-263.
73. Cancer Genome Atlas Research Network. (2014). Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 507:315-322.
74. Cancer Genome Atlas Research Network. (2012). Comprehensive genomic characterization of squamous cell lung cancers. Nature 489:519-525.
75. Krauthammer M, Y Kong, BH Ha, P Evans, A Bacchiocchi, JP McCusker, E Cheng, MJ Davis, G Goh, et al. (2012). Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 44:1006-1014.
76. Ding L, G Getz, DA Wheeler, ER Mardis, MD McLellan, K Cibulskis, C Sougnez, H Greulich, DM Muzny, et al. (2008). Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455:1069-1075.
77. Barretina J, G Caponigro, N Stransky, K Venkatesan, AA Margolin, S Kim, CJ Wilson, J Lehar, GV Kryukov, et al. (2012). The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 483:603-607.
78. Ho AS, K Kannan, DM Roy, LG Morris, I Ganly, N Katabi, D Ramaswami, LA Walsh, S Eng, et al. (2013). The mutational landscape of adenoid cystic carcinoma. Nat Genet 45:791-798.
79. Jin Y, SA Birlea, PR Fain, TM Ferrara, S Ben, SL Riccardi, JB Cole, K Gowan, PJ Holland, et al. (2012). Genome-wide association analyses identify 13 new susceptibility loci for generalized vitiligo. Nat Genet 44:676-680.