The tumor suppressor Apc controls planar cell polarities central to gut homeostasis

Journal of Cell Biology

Volumn 198, Issue 3, 2012, Pages 331-341

  Bellis, Julien ^a,c   Duluc, Isabelle ^b,c   Romagnolo, Béatrice ^b   Perret, Christine ^b   Faux, Maree C ^d   Dujardin, Denis ^a,c   Formstone, Caroline ^e   Lightowler, Sally ^f   Ramsay, Robert G ^f,g   Freund, Jean Noël ^b,c   De Mey, Jan R ^a,c  

^a CNRS   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Australia)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f PETER MACCALLUM CANCER CENTRE   (Australia)

^g UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TUMOR SUPPRESSOR PROTEIN;

ADENOMATOUS POLYP; ANISOTROPY; ARTICLE; CANCER GROWTH; CANCER STAGING; CELL DIVISION; CELL FATE; CELL POLARITY; CELL TYPE; COLORECTAL CANCER; GENE MUTATION; HOMEOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

ACTINS; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; ANISOTROPY; CELL LINE; CHROMATIN; CROSSES, GENETIC; DISEASE PROGRESSION; DOGS; HOMEOSTASIS; INTERPHASE; INTESTINES; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MUTATION; STOCHASTIC PROCESSES; TELOPHASE;

MUS;

EID: 84866450211     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201204086     Document Type: Article

References (53)

1. Aguado, R., N. Martin-Blanco, M. Caraballo, and M. Canelles. 2010. The endocytic adaptor Numb regulates thymus size by modulating pre-TCR signaling during asymmetric division. Blood. 116:1705-1714. http://dx.doi.org/10.1182/blood-2009-10-246777
2. Altmann, G.G. 1990. Renewal of the intestinal epithelium: new aspects as indicated by recent ultrastructural observations. J. Electron Microsc. Tech. 16:2-14. http://dx.doi.org/10.1002/jemt.1060160103
3. Andreu, P., S. Colnot, C. Godard, S. Gad, P. Chafey, M. Niwa-Kawakita, P. Laurent-Puig, A. Kahn, S. Robine, C. Perret, and B. Romagnolo. 2005. Crypt-restricted proliferation and commitment to the Paneth cell lineage following Apc loss in the mouse intestine. Development. 132:1443-1451. http://dx.doi.org/10.1242/dev.01700
4. Barker, N., J.H. van Es, J. Kuipers, P. Kujala, M. van den Born, M. Cozijnsen, A. Haegebarth, J. Korving, H. Begthel, P.J. Peters, and H. Clevers. 2007. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature. 449:1003-1007. http://dx.doi.org/10.1038/nature06196
5. Barker, N., R.A. Ridgway, J.H. van Es, M. van de Wetering, H. Begthel, M. van den Born, E. Danenberg, A.R. Clarke, O.J. Sansom, and H. Clevers. 2009. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature. 457:608-611. http://dx.doi.org/10.1038/nature07602
6. Bjerknes, M., and H. Cheng. 1981. The stem-cell zone of the small intestinal epithelium. III. Evidence from columnar, enteroendocrine, and mucous cells in the adult mouse. Am. J. Anat. 160:77-91. http://dx.doi.org/10.1002/aja.1001600107
7. Bjerknes, M., and H. Cheng. 1999. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology. 116:7-14. http://dx.doi.org/10.1016/S0016-5085(99)70222-2
8. Booth, C., and C.S. Potten. 2000. Gut instincts: thoughts on intestinal epithelial stem cells. J. Clin. Invest. 105:1493-1499. http://dx.doi.org/10.1172/JCI10229
9. Buske, P., J. Galle, N. Barker, G. Aust, H. Clevers, and M. Loeffler. 2011. A comprehensive model of the spatio-temporal stem cell and tissue organisation in the intestinal crypt. PLOS Comput. Biol. 7:e1001045. http://dx.doi.org/10.1371/journal.pcbi.1001045
10. Caldwell, C.M., R.A. Green, and K.B. Kaplan. 2007. APC mutations lead to cytokinetic failures in vitro and tetraploid genotypes in Min mice. J. Cell Biol. 178:1109-1120. http://dx.doi.org/10.1083/jcb.200703186
11. Chang, W.W.L., and C.P. Leblond. 1971. Renewal of the epithelium in the descending colon of the mouse. I. Presence of three cell populations: vacuolatedcolumnar, mucous and argentaffin. Am. J. Anat. 131:73-99. http://dx.doi.org/10.1002/aja.1001310105
12. Chang, W.W.L., and N.J. Nadler. 1975. Renewal of the epithelium in the descending colon of the mouse. IV. Cell population kinetics of vacuolated-columnar and mucous cells. Am. J. Anat. 144:39-56. http://dx.doi.org/10.1002/aja.1001440104
13. Cheng, H., and C.P. Leblond. 1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. I. Columnar cell. Am. J. Anat. 141:461-479. http://dx.doi.org/10.1002/aja.1001410403
14. Clayton, E., D.P. Doupé, A.M. Klein, D.J. Winton, B.D. Simons, and P.H. Jones. 2007. A single type of progenitor cell maintains normal epidermis. Nature. 446:185-189. http://dx.doi.org/10.1038/nature05574
15. Colaluca, I.N., D. Tosoni, P. Nuciforo, F. Senic-Matuglia, V. Galimberti, G. Viale, S. Pece, and P.P. Di Fiore. 2008. NUMB controls p53 tumour suppressor activity. Nature. 451:76-80. http://dx.doi.org/10.1038/nature06412
16. Colnot, S., M. Niwa-Kawakita, G. Hamard, C. Godard, S. Le Plenier, C. Houbron, B. Romagnolo, D. Berrebi, M. Giovannini, and C. Perret. 2004. Colorectal cancers in a new mouse model of familial adenomatous polyposis: influence of genetic and environmental modifiers. Lab. Invest. 84:1619-1630. http://dx.doi.org/10.1038/labinvest.3700180
17. Dho, S.E., M.B. French, S.A. Woods, and C.J. McGlade. 1999. Characterization of four mammalian numb protein isoforms. Identification of cytoplasmic and membrane-associated variants of the phosphotyrosine binding domain. J. Biol. Chem. 274:33097-33104. http://dx.doi.org/10.1074/jbc.274.46.33097
18. Dho, S.E., J. Trejo, D.P. Siderovski, and C.J. McGlade. 2006. Dynamic regulation of mammalian numb by G protein-coupled receptors and protein kinase C activation: Structural determinants of numb association with the cortical membrane. Mol. Biol. Cell. 17:4142-4155. http://dx.doi.org/10.1091/mbc.E06-02-0097
19. Dikovskaya, D., D. Schiffmann, I.P. Newton, A. Oakley, K. Kroboth, O. Sansom, T.J. Jamieson, V. Meniel, A. Clarke, and I.S. Näthke. 2007. Loss of APC induces polyploidy as a result of a combination of defects in mitosis and apoptosis. J. Cell Biol. 176:183-195. http://dx.doi.org/10.1083/jcb.200610099
20. Draviam, V.M., I. Shapiro, B. Aldridge, and P.K. Sorger. 2006. Misorientation and reduced stretching of aligned sister kinetochores promote chromosome missegregation in EB1- or APC-depleted cells. EMBO J. 25:2814-2827. http://dx.doi.org/10.1038/sj.emboj.7601168
21. Fischer, E., E. Legue, A. Doyen, F. Nato, J.F. Nicolas, V. Torres, M. Yaniv, and M. Pontoglio. 2006. Defective planar cell polarity in polycystic kidney disease. Nat. Genet. 38:21-23. http://dx.doi.org/10.1038/ng1701
22. Fleming, E.S., M. Zajac, D.M. Moschenross, D.C. Montrose, D.W. Rosenberg, A.E. Cowan, and J.S. Tirnauer. 2007. Planar spindle orientation and asymmetric cytokinesis in the mouse small intestine. J. Histochem. Cytochem. 55:1173-1180. http://dx.doi.org/10.1369/jhc.7A7234.2007
23. Fleming, E.S., M. Temchin, Q. Wu, L. Maggio-Price, and J.S. Tirnauer. 2009. Spindle misorientation in tumors from APC(min/+) mice. Mol. Carcinog. 48:592-598. http://dx.doi.org/10.1002/mc.20506
24. Fodde, R., R. Smits, N. Hofland, M. Kielman, and P. Meera Khan. 1999. Mechanisms of APC-driven tumorigenesis: lessons from mouse models. Cytogenet. Cell Genet. 86:105-111. http://dx.doi.org/10.1159/000015361
25. Formstone, C.J., C. Moxon, J. Murdoch, P. Little, and I. Mason. 2010. Basal enrichment within neuroepithelia suggests novel function(s) for Celsr1 protein. Mol. Cell. Neurosci. 44:210-222. http://dx.doi.org/10.1016/j.mcn.2010.03.008
26. Fre, S., A. Bardin, S. Robine, and D. Louvard. 2011. Notch signaling in intestinal homeostasis across species: the cases of Drosophila, Zebrafish and the mouse. Exp. Cell Res. 317:2740-2747. http://dx.doi.org/10.1016/j.yexcr.2011.06.012
27. Gong, Y., C. Mo, and S.E. Fraser. 2004. Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature. 430:689-693. http://dx.doi.org/10.1038/nature02796
28. Green, R.A., R. Wollman, and K.B. Kaplan. 2005. APC and EB1 function together in mitosis to regulate spindle dynamics and chromosome alignment. Mol. Biol. Cell. 16:4609-4622. http://dx.doi.org/10.1091/mbc.E05-03-0259
29. Gulino, A., L. Di Marcotullio, and I. Screpanti. 2010. The multiple functions of Numb. Exp. Cell Res. 316:900-906. http://dx.doi.org/10.1016/j.yexcr.2009.11.017
30. Helms, A.W., and J.E. Johnson. 1998. Progenitors of dorsal commissural interneurons are defined by MATH1 expression. Development. 125:919-928.
31. Jory, A., I. Le Roux, B. Gayraud-Morel, P. Rocheteau, M. Cohen-Tannoudji, A. Cumano, and S. Tajbakhsh. 2009. Numb promotes an increase in skeletal muscle progenitor cells in the embryonic somite. Stem Cells. 27:2769-2780. http://dx.doi.org/10.1002/stem.220
32. Klein, A.M., and B.D. Simons. 2011. Universal patterns of stem cell fate in cycling adult tissues. Development. 138:3103-3111. http://dx.doi.org/10.1242/dev.060103
33. Lopez-Garcia, C., A.M. Klein, B.D. Simons, and D.J. Winton. 2010. Intestinal stem cell replacement follows a pattern of neutral drift. Science. 330:822-825. http://dx.doi.org/10.1126/science.1196236
34. Mahmoud, N.N., S.K. Boolbol, R.T. Bilinski, C. Martucci, A. Chadburn, and M.M. Bertagnolli. 1997. Apc gene mutation is associated with a dominantnegative effect upon intestinal cell migration. Cancer Res. 57:5045-5050.
35. Montcouquiol, M., J.M. Jones, and N. Sans. 2008. Detection of planar polarity proteins in mammalian cochlea. Methods Mol. Biol. 468:207-219. http://dx.doi.org/10.1007/978-1-59745-249-6_16
36. Morin, X., and Y. Bellaïche. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell. 21:102-119. http://dx.doi.org/10.1016/j.devcel.2011.06.012
37. Neumüller, R.A., and J.A. Knoblich. 2009. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 23:2675-2699. http://dx.doi.org/10.1101/gad.1850809
38. Pease, J.C., and J.S. Tirnauer. 2011. Mitotic spindle misorientation in cancer-out of alignment and into the fire. J. Cell Sci. 124:1007-1016. http://dx.doi.org/10.1242/jcs.081406
39. Quyn, A.J., P.L. Appleton, F.A. Carey, R.J. Steele, N. Barker, H. Clevers, R.A. Ridgway, O.J. Sansom, and I.S. Näthke. 2010. Spindle orientation bias in gut epithelial stem cell compartments is lost in precancerous tissue. Cell Stem Cell. 6:175-181. http://dx.doi.org/10.1016/j.stem.2009.12.007
40. Rasin, M.R., V.R. Gazula, J.J. Breunig, K.Y. Kwan, M.B. Johnson, S. Liu-Chen, H.S. Li, L.Y. Jan, Y.N. Jan, P. Rakic, and N. Sestan. 2007. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10:819-827. http://dx.doi.org/10.1038/nn1924
41. Reinsch, S., and E. Karsenti. 1994. Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J. Cell Biol. 126:1509-1526. http://dx.doi.org/10.1083/jcb.126.6.1509
42. Rothenberg, M.E., Y. Nusse, T. Kalisky, J.J. Lee, P. Dalerba, F. Scheeren, N. Lobo, S. Kulkarni, S. Sim, D. Qian, et al. 2012. Identification of a cKit(+) colonic crypt base secretory cell that supports Lgr5(+) stem cells in mice. Gastroenterology. 142:1195-1205. http://dx.doi.org/10.1053/j.gastro.2012.02.006
43. Sato, T., J.H. van Es, H.J. Snippert, D.E. Stange, R.G. Vries, M. van den Born, N. Barker, N.F. Shroyer, M. van de Wetering, and H. Clevers. 2011. Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts. Nature. 469:415-418. http://dx.doi.org/10.1038/nature09637
44. Shroyer, N.F., M.A. Helmrath, V.Y.C. Wang, B. Antalffy, S.J. Henning, and H.Y. Zoghbi. 2007. Intestine-specific ablation of mouse atonal homolog 1 (Math1) reveals a role in cellular homeostasis. Gastroenterology. 132:2478-2488. http://dx.doi.org/10.1053/j.gastro.2007.03.047
45. Simons, B.D., and H. Clevers. 2011. Strategies for homeostatic stem cell self-renewal in adult tissues. Cell. 145:851-862. http://dx.doi.org/10.1016/j.cell.2011.05.033
46. Simons, M., and G. Walz. 2006. Polycystic kidney disease: cell division without a c(l)ue? Kidney Int. 70:854-864. http://dx.doi.org/10.1038/sj.ki.5001534
47. Snippert, H.J., L.G. van der Flier, T. Sato, J.H. van Es, M. van den Born, C. Kroon-Veenboer, N. Barker, A.M. Klein, J. van Rheenen, B.D. Simons, and H. Clevers. 2010. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell. 143:134-144. http://dx.doi.org/10.1016/j.cell.2010.09.016
48. Strutt, D. 2005. Organ shape: controlling oriented cell division. Curr. Biol. 15:R758-R759. http://dx.doi.org/10.1016/j.cub.2005.08.053
49. Su, L.K., K.W. Kinzler, B. Vogelstein, A.C. Preisinger, A.R. Moser, C. Luongo, K.A. Gould, and W.F. Dove. 1992. Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science. 256:668-670. http://dx.doi.org/10.1126/science.1350108
50. van Es, J.H., P. Jay, A. Gregorieff, M.E. van Gijn, S. Jonkheer, P. Hatzis, A. Thiele, M. van den Born, H. Begthel, T. Brabletz, et al. 2005. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat. Cell Biol. 7:381-386. http://dx.doi.org/10.1038/ncb1240
51. Wasan, H.S., H.S. Park, K.C. Liu, N.K. Mandir, A. Winnett, P. Sasieni, W.F. Bodmer, R.A. Goodlad, and N.A. Wright. 1998. APC in the regulation of intestinal crypt fission. J. Pathol. 185:246-255. http://dx.doi.org/10.1002/(SICI)1096-9896(199807)185:3<246::AID-PATH90>3.0.CO;2-8
52. Yang, Q., N.A. Bermingham, M.J. Finegold, and H.Y. Zoghbi. 2001. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science. 294:2155-2158. http://dx.doi.org/10.1126/science.1065718
53. Zhong, W., J.N. Feder, M.M. Jiang, L.Y. Jan, and Y.N. Jan. 1996. Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron. 17:43-53. http://dx.doi.org/10.1016/S0896-6273(00)80279-2