Understanding the role of asymmetric cell division in cancer using C. elegans

Developmental Dynamics

Volumn 239, Issue 5, 2010, Pages 1378-1387

  Hyenne, Vincent ^a   Chartier, Nicolas T ^a   Labbé, Jean Claude ^b  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Asymmetric cell division; Caenorhabditis elegans; Cell polarity; Normal and cancer stem cells

Indexed keywords

PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4;

CAENORHABDITIS ELEGANS; CARCINOGENESIS; CELL DIVISION; CELL FATE; CELL FUNCTION; CELL POLARITY; EMBRYO DEVELOPMENT; HOMEOSTASIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SPINDLE CELL;

ANIMALS; CAENORHABDITIS ELEGANS; CELL DIVISION; CELL LINEAGE; DISEASE MODELS, ANIMAL; NEOPLASMS; STEM CELLS;

CAENORHABDITIS ELEGANS;

EID: 77951553280     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22237     Document Type: Review

References (97)

1. Aceto D, Beers M, Kemphues KJ. 2006. Interaction of PAR-6 with CDC-42 is required for maintenance but not establishment of PAR asymmetry in C. elegans. Dev Biol 299:286-397.
2. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. 2003. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983-3988. (Pubitemid 36418143)
3. Albertson DG. 1984. Formation of the first cleavage spindle in nematode embryos. Dev Biol 101:61-72.
4. Betschinger J, Mechtler K, Knoblich JA. 2006. Asymmetric segregation of the tumor suppressor brat regulates selfrenewal in Drosophila neural stem cells. Cell 124:1241-1253.
5. Bonnet D, Dick JE. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3:730-737.
6. Bowman SK, Neumuller RA, Novatchkova M, Du Q, Knoblich JA. 2006. The Drosophila NuMA homolog mud regulates spindle orientation in asymmetric cell division. Dev Cell 10:731-742.
7. Boyd L, Guo S, Levitan D, Stinchcomb DT, Kemphues KJ. 1996. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122:3075-3084.
8. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C, Gharakhani J, Jülicher F, Hyman AA. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729-1732.
9. Bringmann H, Hyman AA. 2005. A cytokinesis furrow is positioned by two consecutive signals. Nature 436:731-734. (Pubitemid 41117278)
10. Bultje RS, Castaneda-Castellanos DR, Jan LY, Jan YN, Kriegstein AR, Shi SH. 2009. Mammalian Par3 regulates progenitor cell asymmetric division via notch signaling in the developing neocortex. Neuron 63:189-202.
11. Byrd DT, Kimble J. 2009. Scratching the niche that controls Caenorhabditis elegans germline stem cells. Semin Cell Dev Biol 20:1107-1113.
12. Caussinus E, Gonzalez C. 2005. Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster. Nat Genet 37:1125-1129. (Pubitemid 41486667)
13. Cheeks RJ, Canman JC, Gabriel WN, Meyer N, Strome S, Goldstein B. 2004. C. elegans PAR proteins function by mobilizing and stabilizing asymmetrically localized protein complexes. Curr Biol 14:851-862. (Pubitemid 38800906)
14. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, Brisken C, Minucci S, Di Fiore PP, Pelicci PG. 2009. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cell 138:1083-1095.
15. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM. 2006. Cancer stem cells--perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res 66:9339-9344. (Pubitemid 44623625)
16. Colombo K, Grill SW, Kimple RJ, Willard FS, Siderovski DP, Gönczy P. 2003. Translation of polarity cues into asymmetric spindle positioning in Caenorhabditis elegans embryos. Science 300:1957-1961. (Pubitemid 36734605)
17. Couwenbergs C, Labbé JC, Goulding M, Marty T, Bowerman B, Gotta M. 2007. Heterotrimeric G protein signaling functions with dynein to promote spindle positioning in C. elegans. J Cell Biol 179:15-22. (Pubitemid 47606679)
18. Cowan CR, Hyman AA. 2004. Centrosomes direct cell polarity independently of microtubule assembly in C. elegans embryos. Nature 431:92-96.
19. Cuenca AA, Schetter A, Aceto D, Kemphues K, Seydoux G. 2003. Polarization of the C. elegans zygote proceeds via distinct establishment and maintenance phases. Development 130:1255-1265. (Pubitemid 36410775)
20. Dalerba P, Cho RW, Clarke MF. 2007. Cancer stem cells: models and concepts. Annu Rev Med 58:267-284. (Pubitemid 46706514)
21. Daniels BR, Perkins EM, Dobrowsky TM, Sun SX, D. W. 2009. Asymmetric enrichment of PIE-1 in the Caenorhabditis elegans zygote mediated by binary counterdiffusion. J Cell Biol 184:473-479.
22. DeRenzo C, Reese KJ, Seydoux G. 2003. Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424:685-689. (Pubitemid 36987994)
23. Etemad-Moghadam B, Guo S, Kemphues KJ. 1995. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83:743-752.
24. Goldstein B, Hird SN. 1996. Specification of the anteroposterior axis in Caenorhabditis elegans. Development 122:1467-1474. (Pubitemid 26159636)
25. Gotta M, Ahringer J. 2001. Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos. Nat Cell Biol 3:297-300. (Pubitemid 32201325)
26. Gotta M, Abraham MC, Ahringer J. 2001. CDC-42 controls early cell polarity and spindle orientation in C. elegans. Curr Biol 11:482-488. (Pubitemid 32328926)
27. Gotta M, Dong Y, Peterson YK, Lanier SM, Ahringer J. 2003. Asymmetrically distributed C. elegans homologs of AGS3/PINS control spindle position in the early embryo. Curr Biol 13:1029-1037. (Pubitemid 36726038)
28. Goulding MB, Canman JC, Senning EN, Marcus AH, Bowerman B. 2007. Control of nuclear centration in the C. elegans zygote by receptor-independent Galpha signaling and myosin II. J Cell Biol 178:1177-1191. (Pubitemid 47480225)
29. Grill SW, Gönczy P, Stelzer EH, Hyman AA. 2001. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630-633. (Pubitemid 32154816)
30. Guedes S, Priess JR. 1997. The C. elegans MEX-1 protein is present in germline blastomeres and is a P granule component. Development 124:731-739. (Pubitemid 27092439)
31. Guo S, Kemphues KJ. 1995. par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81:611-620.
32. Gupta PB, Chaffer CL, Weinberg RA. 2009. Cancer stem cells: mirage or reality? Nat Med 15:1010-1012.
33. Hao Y, Boyd L, Seydoux G. 2006. Stabilization of cell polarity by the C. elegans RING protein PAR-2. Dev Cell 10:199-208. (Pubitemid 43174953)
34. Hemminki A, Markie D, Tomlinson I, Avizienyte E, Roth S, Loukola A, Bignell G, Warren W, Aminoff M, Höglund P, Järvinen H, Kristo P, Pelin K, Ridanpää M, Salovaara R, Toro T, Bodmer W, Olschwang S, Olsen AS, Stratton MR, de la Chapelle A, Aaltonen LA. 1998. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391:184-187.
35. Hird SN, White JG. 1993. Cortical and cytoplasmic flow polarity in early embryonic cells of Caenorhabditis elegans. J Cell Biol 121:1343-1355.
36. Hird SN, Paulsen JE, Strome S. 1996. Segregation of germ granules in living Caenorhabditis elegans embryos: cell-typespecific mechanisms for cytoplasmic localisation. Development 122:1303-1312.
37. Horvitz HR, Herskowitz I. 1992. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68:237-255.
38. Hung TJ, Kemphues KJ. 1999. PAR-6 is a conserved PDZ domain-containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126:127-135.
39. Hyenne V, Desrosiers M, Labbé JC. 2008. C. elegans Brat homologs regulate PAR protein-dependent polarity and asymmetric cell division. Dev Biol 321:368-378.
40. Hyman AA, White JG. 1987. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans. J Cell Biol 105:2123-2135.
41. Jamieson CH, Ailles LE, Dylla SJ, Muijtjens M, Jones C, Zehnder JL, Gotlib J, Li K, Manz MG, Keating A, Sawyers CL, Weissman IL. 2004. Granulocytemacrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med 351:657-667.
42. Jenkins N, Saam JR, Mango SE. 2006. CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 313:1298-1301.
43. Jenne DE, Reimann H, Nezu J, Friedel W, Loff S, Jeschke R, Müller O, Back W, Zimmer M. 1998. Peutz-Jeghers syndrome is caused by mutations in a novel serine threonine kinase. Nat Genet 18:38-43.
44. Kay AJ, Hunter CP. 2001. CDC-42 regulates PAR protein localization and function to control cellular and embryonic polarity in C. elegans. Curr Biol 11:474-481.
45. Kelly PN, Dakic A, Adams JM, Nutt SL, Strasser A. 2007. Tumor growth need not be driven by rare cancer stem cells. Science 317:337.
46. Kemphues KJ, Priess JR, Morton DG, Cheng NS. 1988. Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell 52:311-320.
47. Kennedy JA, Barabe F, Poeppl AG, Wang JC, Dick JE. 2007. Comment on "tumor growth need not be driven by rare cancer stem cells". Science 318:1722; author reply, 1722.
48. Kimura A, Onami S. 2007. Local cortical pulling-force repression switches centrosomal centration and posterior displacement in C. elegans. J Cell Biol 179:1347-1354.
49. Knoblich JA. 2008. Mechanisms of asymmetric stem cell division. Cell 132:583-597.
50. Kunnev D, Ivanov I, Ionov Y. 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.
51. Labbé JC, McCarthy EK, Goldstein B. 2004. The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J Cell Biol 167:245-256.
52. Labbé JC, Pacquelet A, Marty T, Gotta M. 2006. A genomewide screen for suppressors of par-2 uncovers potential regulators of PAR protein-dependent cell polarity in Caenorhabditis elegans. Genetics 174:285-295.
53. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres-Cortes J, Minden M, Paterson B, Caligiuri MA, Dick JE. 1994. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367:645-648.
54. Lechler T, Fuchs E. 2005. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437:275-280.
55. Lee CY, Robinson KJ, Doe CQ. 2006a. Lgl, Pins and aPKC regulate neuroblast self-renewal versus differentiation. Nature 439:594-598.
56. Lee CY, Wilkinson BD, Siegrist SE, Wharton RP, Doe CQ. 2006b. Brat is a Miranda cargo protein that promotes neuronal differentiation and inhibits neuroblast selfrenewal. Dev Cell 10:441-449.
57. Levitan DJ, Boyd L, Mello CC, Kemphues KJ, Stinchcomb DT. 1994. par-2, a gene required for blastomere asymmetry in Caenorhabditis elegans, encodes zinc-finger and ATP-binding motifs. Proc Natl Acad Sci USA 91:6108-6112.
58. Maddox AS, Habermann B, Desai A, Oegema K. 2005. Distinct roles for two C. elegans anillins in the gonad and early embryo. Development 132:2837-2848.
59. McCarthy Campbell EK, Werts AD, Goldstein B. 2009. A cell cycle timer for asymmetric spindle positioning. PLoS Biol 7:e1000088.
60. Mello CC, Schubert C, Draper B, Zhang W, Lobel R, Priess JR. 1996. The PIE-1 protein and germline specification in C. elegans embryos. Nature 382:710-712.
61. Miyamoto T, Weissman IL, Akashi K. 2000. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci USA 97:7521-7526.
62. Morrison SJ, Kimble J. 2006. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068-1074.
63. Morton DG, Shakes DC, Nugent S, Dichoso D, Wang W, Golden A, Kemphues KJ. 2002. The Caenorhabditis elegans par-5 gene encodes a 14-3-3 protein required for cellular asymmetry in the early embryo. Dev Biol 241:47-58.
64. Motegi F, Sugimoto A. 2006. Sequential functioning of the ECT-2 RhoGEF, RHO-1 and CDC-42 establishes cell polarity in Caenorhabditis elegans embryos. Nat Cell Biol 8:978-985.
65. Munro E, Nance J, Priess JR. 2004. Cortical flows powered by asymmetrical contraction transport PAR proteins to establish and maintain anterior-posterior polarity in the early C. elegans embryo. Dev Cell 7:413-424.
66. Nguyen-Ngoc T, Afshar K, Gönczy P. 2007. Coupling of cortical dynein and G alpha proteins mediates spindle positioning in Caenorhabditis elegans. Nat Cell Biol 9:1294-1302.
67. Nolan ME, Aranda V, Lee S, Lakshmi B, Basu S, Allred DC, Muthuswamy SK. 2008. The polarity protein Par6 induces cell proliferation and is overexpressed in breast cancer. Cancer Res 68:8201-8209.
68. Pacquelet A, Zanin E, Ashiono C, Gotta M. 2008. PAR-6 levels are regulated by NOS-3 in a CUL-2 dependent manner in Caenorhabditis elegans. Dev Biol 319:267-272.
69. Quintana E, Shackleton M, Sabel MS, Fullen DR, Johnson TM, Morrison SJ. 2008. Efficient tumour formation by single human melanoma cells. Nature 456:593-598.
70. Rappaport R. 1961. Experiments concerning the cleavage stimulus in sand dollar eggs. J Exp Zool 148:81-89.
71. Reese KJ, Dunn MA, Waddle JA, Seydoux G. 2000. Asymmetric segregation of PIE-1 in C. elegans is mediated by two complementary mechanisms that act through separate PIE-1 protein domains. Mol Cell 6:445-455.
72. Rose LS, Lamb ML, Hird SN, Kemphues KJ. 1995. Pseudocleavage is dispensable for polarity and development in C. elegans embryos. Dev Biol 168:479-489.
73. Rosen JM, Jordan CT. 2009. The increasing complexity of the cancer stem cell paradigm. Science 324:1670-1673.
74. Sanchez-Cespedes M, Parrella P, Esteller M, Nomoto S, Trink B, Engles JM, Westra WH, Herman JG, Sidransky D. 2002. Inactivation of LKB1/STK11 is a common event in adenocarcinomas of the lung. Cancer Res 62:3659-3662.
75. Schonegg S, Hyman AA. 2006. CDC-42 and RHO-1 coordinate acto-myosin contractility and PAR protein localization during polarity establishment in C. elegans embryos. Development 133:3507-3516.
76. Schubert CM, Lin R, de Vries CJ, Plasterk RH, Priess JR. 2000. MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol Cell 5:671-682.
77. Schwamborn JC, Berezikov E, Knoblich JA. 2009. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136:913-925.
78. Seydoux G, Mello CC, Pettitt J, Wood WB, Priess JR, Fire A. 1996. Repression of gene expression in the embryonic germ lineage of C. elegans. Nature 382:713-716.
79. Shen Z, Wen XF, Lan F, Shen ZZ, Shao ZM. 2002. The tumor suppressor gene LKB1 is associated with prognosis in human breast carcinoma. Clin Cancer Res 8:2085-2090. (Pubitemid 34753577)
80. Shinin V, Gayraud-Morel B, Gomes D, Tajbakhsh S. 2006. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 8:677-687.
81. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-5828. (Pubitemid 37187480)
82. Spilker AC, Rabilotta A, Zbinden C, Labbé J-C, Gotta M. 2009. MAP Kinase signaling antagonizes PAR-1 function during polarization of the early Caenorhabditis elegans embryo. Genetics 183:965-977.
83. Srinivasan DG, Fisk RM, Xu H, van den Heuvel S. 2003. A complex of LIN-5 and GPR proteins regulates G protein signaling and spindle function in C elegans. Genes Dev 17:1225-1239. (Pubitemid 36583166)
84. Strome S, Wood WB. 1983. Generation of asymmetry and segregation of germline granules in early C. elegans embryos. Cell 35:15-25. (Pubitemid 14240214)
85. Sulston JE, Schierenberg E, White JG, Thomson JN. 1983. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol 100:64-119.
86. Tabara H, Hill RJ, Mello CC, Priess JR, Kohara Y. 1999. pos-1 encodes a cytoplasmic zinc-finger protein essential for germline specification in C. elegans. Development 126:1-11. (Pubitemid 29045895)
87. Tabuse Y, Izumi Y, Piano F, Kemphues KJ, Miwa J, Ohno S. 1998. Atypical protein kinase C cooperates with PAR-3 to establish embryonic polarity in Caenorhabditis elegans. Development 125:3607-3614. (Pubitemid 28469961)
88. Tenlen JR, Molk JN, London N, Page BD, Priess JR. 2008. MEX-5 asymmetry in one-cell C. elegans embryos requires PAR-4- and PAR-1-dependent phosphorylation. Development 135:3665-3675.
89. Tsai MC, Ahringer J. 2007. Microtubules are involved in anterior-posterior axis formation in C. elegans embryos. J Cell Biol 179:397-402. (Pubitemid 350074785)
90. Viloria-Petit AM, David L, Jia JY, Erdemir T, Bane AL, Pinnaduwage D, Roncari L, Narimatsu M, Bose R, Moffat J, Wong JW, Kerbel RS, O'Malley FP, Andrulis IL, Wrana JL. 2009. A role for the TGFbeta-Par6 polarity pathway in breast cancer progression. Proc Natl Acad Sci USA 106:14028-14033.
91. Wallenfang MR, Seydoux G. 2000. Polarization of the anterior-posterior axis of C. elegans is a microtubule-directed process. Nature 408:89-92.
92. Watts JL, Etemad-Moghadam B, Guo S, Boyd L, Draper BW, Mello CC, Priess JR, Kemphues KJ. 1996. par-6, a gene involved in the establishment of asymmetry in early C. elegans embryos, mediates the asymmetric localization of PAR-3. Development 122:3133-3140. (Pubitemid 26371978)
93. Watts JL, Morton DG, Bestman J, Kemphues KJ. 2000. The C. elegans par-4 gene encodes a putative serine-threonine kinase required for establishing embryonic asymmetry. Development 127:1467-1475. (Pubitemid 30232597)
94. Werner M, Munro E, Glotzer M. 2007. Astral signals spatially bias cortical myosin recruitment to break symmetry and promote cytokinesis. Curr Biol 17:1286-1297. (Pubitemid 47176895)
95. Wu M, Kwon HY, Rattis F, Blum J, Zhao C, Ashkenazi R, Jackson TL, Gaiano N, Oliver T, Reya T. 2007. Imaging hematopoietic precursor division in real time. Cell Stem Cell 1:541-554. (Pubitemid 350056405)
96. Zen K, Yasui K, Gen Y, Dohi O, Wakabayashi N, Mitsufuji S, Itoh Y, Zen Y, Nakanuma Y, Taniwaki M, Okanoue T, Yoshikawa T. 2009. Defective expression of polarity protein PAR-3 gene (PARD3) in esophageal squamous cell carcinoma. Oncogene 28:2910-2918.
97. Zwaal RR, Ahringer J, van Luenen HG, Rushforth A, Anderson P, Plasterk RH. 1996. G proteins are required for spatial orientation of early cell cleavages in C. elegans embryos. Cell 86:619-629. (Pubitemid 26299493)