E-cadherin regulates the behavior and fate of epithelial stem cells and their progeny in the mouse incisor

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 357-366

  Li, Chun Ying ^a   Cha, Wanghee ^a   Luder, Hans Ulrich ^b   Charles, Roch Philippe ^c   McMahon, Martin ^c   Mitsiadis, Thimios A ^b   Klein, Ophir D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ameloblasts; Cell migration; Cell proliferation; E cadherin; Epithelial stem cells; Fibroblast growth factors (FGFs); Incisor; Mouse; Sprouty genes

Indexed keywords

CYCLINE; DOXYCYCLINE; FIBROBLAST GROWTH FACTOR; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; TAMOXIFEN; UVOMORULIN;

AMELOBLAST; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INACTIVATION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; INCISOR; MOLECULAR DYNAMICS; MORPHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN DOMAIN; PROTEIN EXPRESSION; TISSUE REGENERATION;

ANIMALIA;

EID: 84861223918     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.012     Document Type: Article

References (55)

1. Ahn S., Joyner A.L. Dynamic changes in the response of cells to positive hedgehog signaling during mouse limb patterning. Cell 2004, 118:505-516.
2. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2001, 2:287-293.
3. Bai C.B., Auerbach W., Lee J.S., Stephen D., Joyner A.L. Gli2, but not Gli1, is required for initial Shh signaling and ectopic activation of the Shh pathway. Development 2002, 129:4753-4761.
4. Bai J., Uehara Y., Montell D.J. Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor coactivator amplified in breast cancer. Cell 2000, 103:1047-1058.
5. Barker N., van Es J.H., Kuipers J., Kujala P., van den Born M., Cozijnsen M., Haegebarth A., Korving J., Begthel H., Peters P.J., Clevers H. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
6. Barrandon Y., Green H. Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:2302-2306.
7. Barron M.J., Brookes S.J., Draper C.E., Garrod D., Kirkham J., Shore R.C., Dixon M.J. The cell adhesion molecule nectin-1 is critical for normal enamel formation in mice. Hum. Mol. Genet. 2008, 17:3509-3520.
8. Bartlett J.D., Dobeck J.M., Tye C.E., Perez-Moreno M., Stokes N., Reynolds A.B., Fuchs E., Skobe Z. Targeted p120-catenin ablation disrupts dental enamel development. PLoS One 2010, 5.
9. Boussadia O., Kutsch S., Hierholzer A., Delmas V., Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech. Dev. 2002, 115:53-62.
10. Chen T., Yuan D., Wei B., Jiang J., Kang J., Ling K., Gu Y., Li J., Xiao L., Pei G. E-cadherin-mediated cell-cell contact is critical for induced pluripotent stem cell generation. Stem Cells 2010, 28:1315-1325.
11. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 2001, 1:37-49.
12. Dailey L., Ambrosetti D., Mansukhani A., Basilico C. Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 2005, 16:233-247.
13. de Rooij D.G., Grootegoed J.A. Spermatogonial stem cells. Curr. Opin. Cell Biol. 1998, 10:694-701.
14. Di Carlo A., De Felici M. A role for E-cadherin in mouse primordial germ cell development. Dev. Biol. 2000, 226:209-219.
15. Diamond I., Owolabi T., Marco M., Lam C., Glick A. Conditional gene expression in the epidermis of transgenic mice using the tetracycline-regulated transactivators tTA and rTA linked to the keratin 5 promoter. J. Invest. Dermatol. 2000, 115:788-794.
16. Franzdottir S.R., Engelen D., Yuva-Aydemir Y., Schmidt I., Aho A., Klambt C. Switch in FGF signalling initiates glial differentiation in the Drosophila eye. Nature 2009, 460:758-761.
17. Fuchs E., Segre J.A. Stem cells: a new lease on life. Cell 2000, 100:143-155.
18. Harada H., Kettunen P., Jung H.S., Mustonen T., Wang Y.A., Thesleff I. Localization of putative stem cells in dental epithelium and their association with Notch and FGF signaling. J. Cell Biol. 1999, 147:105-120.
19. Harada H., Toyono T., Toyoshima K., Yamasaki M., Itoh N., Kato S., Sekine K., Ohuchi H. FGF10 maintains stem cell compartment in developing mouse incisors. Development 2002, 129:1533-1541.
20. Hashimoto K. Regulation of keratinocyte function by growth factors. J. Dermatol. Sci. 2000, 24(Suppl. 1):S46-S50.
21. Hwang W.S., Tonna E.A. Autoradiographic analysis of labeling indices and migration rates of cellular component of mouse incisors using tritiated thymidine (H3tdr). J. Dent. Res. 1965, 44:42-53.
22. Jheon A.H., Mostowfi P., Snead M.L., Ihrie R.A., Sone E., Pramparo T., Attardi L.D., Klein O.D. PERP regulates enamel formation via effects on cell-cell adhesion and gene expression. J. Cell Sci. 2011, 124:745-754.
23. Kai T., Spradling A. An empty Drosophila stem cell niche reactivates the proliferation of ectopic cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:4633-4638.
24. Karpowicz P., Willaime-Morawek S., Balenci L., DeVeale B., Inoue T., van der Kooy D. E-cadherin regulates neural stem cell self-renewal. J. Neurosci. 2009, 29:3885-3896.
25. Kieffer-Combeau S., Meyer J.M., Lesot H. Cell-matrix interactions and cell-cell junctions during epithelial histo-morphogenesis in the developing mouse incisor. Int. J. Dev. Biol. 2001, 45:733-742.
26. Klein O.D., Lyons D.B., Balooch G., Marshall G.W., Basson M.A., Peterka M., Boran T., Peterkova R., Martin G.R. An FGF signaling loop sustains the generation of differentiated progeny from stem cells in mouse incisors. Development 2008, 135:377-385.
27. Klein O.D., Minowada G., Peterkova R., Kangas A., Yu B.D., Lesot H., Peterka M., Jernvall J., Martin G.R. Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial-mesenchymal FGF signaling. Dev. Cell 2006, 11:181-190.
28. Larue L., Ohsugi M., Hirchenhain J., Kemler R. E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:8263-8267.
29. Mason J.M., Morrison D.J., Basson M.A., Licht J.D. Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 2006, 16:45-54.
30. Min H., Danilenko D.M., Scully S.A., Bolon B., Ring B.D., Tarpley J.E., DeRose M., Simonet W.S. Fgf-10 is required for both limb and lung development and exhibits striking functional similarity to Drosophila branchless. Genes Dev. 1998, 12:3156-3161.
31. Mitsiadis T.A., Barrandon O., Rochat A., Barrandon Y., De Bari C. Stem cell niches in mammals. Exp. Cell Res. 2007, 313:3377-3385.
32. Montell D.J. Command and control: regulatory pathways controlling invasive behavior of the border cells. Mech. Dev. 2001, 105:19-25.
33. Morrison S.J., Shah N.M., Anderson D.J. Regulatory mechanisms in stem cell biology. Cell 1997, 88:287-298.
34. Ngan E.S., Ma Z.Q., Chua S.S., DeMayo F.J., Tsai S.Y. Inducible expression of FGF-3 in mouse mammary gland. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:11187-11192.
35. Niewiadomska P., Godt D., Tepass U. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 1999, 144:533-547.
36. Oakberg E.F. A new concept of spermatogonial stem-cell renewal in the mouse and its relationship to genetic effects. Mutat. Res. 1971, 11:1-7.
37. Okamura D., Kimura T., Nakano T., Matsui Y. Cadherin-mediated cell interaction regulates germ cell determination in mice. Development 2003, 130:6423-6430.
38. Parsa S., Kuremoto K., Seidel K., Tabatabai R., Mackenzie B., Yamaza T., Akiyama K., Branch J., Koh C.J., Al Alam D., Klein O.D., Bellusci S. Signaling by FGFR2b controls the regenerative capacity of adult mouse incisors. Development 2010, 137:3743-3752.
39. Potten C.S. Epidermal cell production rates. J. Invest. Dermatol. 1975, 65:488-500.
40. Potten C.S., Schofield R., Lajtha L.G. A comparison of cell replacement in bone marrow, testis and three regions of surface epithelium. Biochim. Biophys. Acta 1979, 560:281-299.
41. Robinson M.L. An essential role for FGF receptor signaling in lens development. Semin. Cell Dev. Biol. 2006, 17:726-740.
42. Seidel K., Ahn C.P., Lyons D., Nee A., Ting K., Brownell I., Cao T., Carano R.A., Curran T., Schober M., Fuchs E., Joyner A., Martin G.R., de Sauvage F.J., Klein O.D. Hedgehog signaling regulates the generation of ameloblast progenitors in the continuously growing mouse incisor. Development 2010, 137:3753-3761.
43. Shim K., Minowada G., Coling D.E., Martin G.R. Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev. Cell 2005, 8:553-564.
44. Smith C.E., Warshawsky H. Cellular renewal in the enamel organ and the odontoblast layer of the rat incisor as followed by radioautography using 3H-thymidine. Anat. Rec. 1975, 183:523-561.
45. Solit D.B., Garraway L.A., Pratilas C.A., Sawai A., Getz G., Basso A., Ye Q., Lobo J.M., She Y., Osman I., Golub T.R., Sebolt-Leopold J., Sellers W.R., Rosen N. BRAF mutation predicts sensitivity to MEK inhibition. Nature 2006, 439:358-362.
46. Song X., Zhu C.H., Doan C., Xie T. Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 2002, 296:1855-1857.
47. Terling C., Heymann R., Rozell B., Obrink B., Wroblewski J. Dynamic expression of E-cadherin in ameloblasts and cementoblasts in mice. Eur. J. Oral Sci. 1998, 106(Suppl. 1):137-142.
48. Thompson R.C., Deo M., Turner D.L. Analysis of microRNA expression by in situ hybridization with RNA oligonucleotide probes. Methods 2007, 43:153-161.
49. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W.E., Rendl M., Fuchs E. Defining the epithelial stem cell niche in skin. Science 2004, 303:359-363.
50. Vaudry D., Stork P.J., Lazarovici P., Eiden L.E. Signaling pathways for PC12 cell differentiation: making the right connections. Science 2002, 296:1648-1649.
51. Wang X.P., Suomalainen M., Felszeghy S., Zelarayan L.C., Alonso M.T., Plikus M.V., Maas R.L., Chuong C.M., Schimmang T., Thesleff I. An integrated gene regulatory network controls stem cell proliferation in teeth. PLoS Biol. 2007, 5:e159.
52. Yoshida T., Miyoshi J., Takai Y., Thesleff I. Cooperation of nectin-1 and nectin-3 is required for normal ameloblast function and crown shape development in mouse teeth. Dev. Dyn. 2010, 239:2558-2569.
53. Zelenka P.S., Arpitha P. Coordinating cell proliferation and migration in the lens and cornea. Semin. Cell Dev. Biol. 2008, 19:113-124.
54. Zhao H., Yang T., Madakashira B.P., Thiels C.A., Bechtle C.A., Garcia C.M., Zhang H., Yu K., Ornitz D.M., Beebe D.C., Robinson M.L. Fibroblast growth factor receptor signaling is essential for lens fiber cell differentiation. Dev. Biol. 2008, 318:276-288.
55. Zohn I.E., Li Y., Skolnik E.Y., Anderson K.V., Han J., Niswander L. p38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 2006, 125:957-969.