Numb/Numbl-Opo Antagonism Controls Retinal Epithelium Morphogenesis by Regulating Integrin Endocytosis

Developmental Cell

Volumn 23, Issue 4, 2012, Pages 782-795

  Bogdanović, Ozren ^a   Delfino Machín, Mariana ^a   Nicolás Pérez, María ^a   Gavilán, María P ^b   Gago Rodrigues, Inês ^a   Fernández Miñán, Ana ^a   Lillo, Concepción ^c   Ríos, Rosa M ^b   Wittbrodt, Joachim ^d   Martínez Morales, Juan R ^a  

^a Departamento de Biología Molecular e Ingeniería Bioquímica   (Spain)

^b CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

^c UNIVERSITY OF SALAMANCA   (Spain)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLATHRIN; INTEGRIN; MEMBRANE PROTEIN; PROTEIN NUMB; PROTEIN NUMBL; PROTEIN OPO; UNCLASSIFIED DRUG;

ARTICLE; ENDOCYTOSIS; GENE; GENE MUTATION; HUMAN; HUMAN CELL; MORPHOGENESIS; NUMB GENE; NUMBL GENE; OPO GENE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; CELLS, CULTURED; ENDOCYTOSIS; FISH PROTEINS; HELA CELLS; HUMANS; INTEGRINS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; ORYZIAS; RETINAL PIGMENT EPITHELIUM;

TELEOSTEI; VERTEBRATA;

EID: 84867728445     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.09.004     Document Type: Article

References (57)

1. Bateman J., Reddy R.S., Saito H., Van Vactor D. The receptor tyrosine phosphatase Dlar and integrins organize actin filaments in the Drosophila follicular epithelium. Curr. Biol. 2001, 11:1317-1327.
2. Bryant D.M., Mostov K.E. From cells to organs: building polarized tissue. Nat. Rev. Mol. Cell Biol. 2008, 9:887-901.
3. Calderwood D.A., Fujioka Y., de Pereda J.M., García-Alvarez B., Nakamoto T., Margolis B., McGlade C.J., Liddington R.C., Ginsberg M.H. Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 2003, 100:2272-2277.
4. Caswell P.T., Vadrevu S., Norman J.C. Integrins: masters and slaves of endocytic transport. Nat. Rev. Mol. Cell Biol. 2009, 10:843-853.
5. Chang H.C., Newmyer S.L., Hull M.J., Ebersold M., Schmid S.L., Mellman I. Hsc70 is required for endocytosis and clathrin function in Drosophila. J. Cell Biol. 2002, 159:477-487.
6. Chen H., Zou Z., Sarratt K.L., Zhou D., Zhang M., Sebzda E., Hammer D.A., Kahn M.L. In vivo beta1 integrin function requires phosphorylation-independent regulation by cytoplasmic tyrosines. Genes Dev. 2006, 20:927-932.
7. Collaco A., Jakab R., Hegan P., Mooseker M., Ameen N. Alpha-AP-2 directs myosin VI-dependent endocytosis of cystic fibrosis transmembrane conductance regulator chloride channels in the intestine. J. Biol. Chem. 2010, 285:17177-17187.
8. Czuchra A., Meyer H., Legate K.R., Brakebusch C., Fässler R. Genetic analysis of beta1 integrin " activation motifs" in mice. J. Cell Biol. 2006, 174:889-899.
9. Dho S.E., Trejo J., Siderovski D.P., McGlade C.J. 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 2006, 17:4142-4155.
10. Dong B., Deng W., Jiang D. Distinct cytoskeleton populations and extensive crosstalk control Ciona notochord tubulogenesis. Development 2011, 138:1631-1641.
11. Ezratty E.J., Bertaux C., Marcantonio E.E., Gundersen G.G. Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J. Cell Biol. 2009, 187:733-747.
12. Filardo E.J., Brooks P.C., Deming S.L., Damsky C., Cheresh D.A. Requirement of the NPXY motif in the integrin beta 3 subunit cytoplasmic tail for melanoma cell migration in vitro and in vivo. J. Cell Biol. 1995, 130:441-450.
13. Formstecher E., Aresta S., Collura V., Hamburger A., Meil A., Trehin A., Reverdy C., Betin V., Maire S., Brun C., et al. Protein interaction mapping: a Drosophila case study. Genome Res. 2005, 15:376-384.
14. Furutani-Seiki M., Wittbrodt J. Medaka and zebrafish, an evolutionary twin study. Mech. Dev. 2004, 121:629-637.
15. Gutzman J.H., Graeden E.G., Lowery L.A., Holley H.S., Sive H. Formation of the zebrafish midbrain-hindbrain boundary constriction requires laminin-dependent basal constriction. Mech. Dev. 2008, 125:974-983.
16. He L., Wang X., Tang H.L., Montell D.J. Tissue elongation requires oscillating contractions of a basal actomyosin network. Nat. Cell Biol. 2010, 12:1133-1142.
17. Huang E.J., Li H., Tang A.A., Wiggins A.K., Neve R.L., Zhong W., Jan L.Y., Jan Y.N. Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev. 2005, 19:138-151.
18. Hurtado L., Caballero C., Gavilan M.P., Cardenas J., Bornens M., Rios R.M. Disconnecting the Golgi ribbon from the centrosome prevents directional cell migration and ciliogenesis. J. Cell Biol. 2011, 193:917-933.
19. Kawakami K. Tol2: a versatile gene transfer vector in vertebrates. Genome Biol. 2007, 8(Suppl 1):S7.
20. Knoblich J.A., Jan L.Y., Jan Y.N. Asymmetric segregation of Numb and Prospero during cell division. Nature 1995, 377:624-627.
21. Kölsch V., Seher T., Fernandez-Ballester G.J., Serrano L., Leptin M. Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 2007, 315:384-386.
22. Kuo J.C., Han X., Hsiao C.T., Yates J.R., Waterman C.M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for β-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 2011, 13:383-393.
23. Kwan K.M., Fujimoto E., Grabher C., Mangum B.D., Hardy M.E., Campbell D.S., Parant J.M., Yost H.J., Kanki J.P., Chien C.B. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev. Dyn. 2007, 236:3088-3099.
24. Lecuit T., Lenne P.F. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8:633-644.
25. Letizia A., Sotillos S., Campuzano S., Llimargas M. Regulated Crb accumulation controls apical constriction and invagination in Drosophila tracheal cells. J. Cell Sci. 2011, 124:240-251.
26. Levayer R., Pelissier-Monier A., Lecuit T. Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 2011, 13:529-540.
27. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457:495-499.
28. Martinez-Morales J.R., Wittbrodt J. Shaping the vertebrate eye. Curr. Opin. Genet. Dev. 2009, 19:511-517.
29. Martinez-Morales J.R., Rembold M., Greger K., Simpson J.C., Brown K.E., Quiring R., Pepperkok R., Martin-Bermudo M.D., Himmelbauer H., Wittbrodt J. ojoplano-mediated basal constriction is essential for optic cup morphogenesis. Development 2009, 136:2165-2175.
30. Mertes F., Martinez-Morales J.R., Nolden T., Spörle R., Wittbrodt J., Lehrach H., Himmelbauer H. Cloning of mouse ojoplano, a reticular cytoplasmic protein expressed during embryonic development. Gene Expr. Patterns 2009, 9:562-567.
31. Montell D.J. Morphogenetic cell movements: diversity from modular mechanical properties. Science 2008, 322:1502-1505.
32. Nelson W.J. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity. Cold Spring Harb. Perspect. Biol. 2009, 1:a000513.
33. Niikura Y., Tabata Y., Tajima A., Inoue I., Arai K., Watanabe S. Zebrafish Numb homologue: phylogenetic evolution and involvement in regulation of left-right asymmetry. Mech. Dev. 2006, 123:407-414.
34. Nishimura T., Kaibuchi K. Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 2007, 13:15-28.
35. O'Connor-Giles K.M., Skeath J.B. Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 2003, 5:231-243.
36. Papusheva E., Heisenberg C.P. Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis. EMBO J. 2010, 29:2753-2768.
37. Rasin M.R., Gazula V.R., Breunig J.J., Kwan K.Y., Johnson M.B., Liu-Chen S., Li H.S., Jan L.Y., Jan Y.N., Rakic P., Sestan N. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 2007, 10:819-827.
38. Reugels A.M., Boggetti B., Scheer N., Campos-Ortega J.A. Asymmetric localization of Numb:EGFP in dividing neuroepithelial cells during neurulation in Danio rerio. Dev. Dyn. 2006, 235:934-948.
39. Santolini E., Puri C., Salcini A.E., Gagliani M.C., Pelicci P.G., Tacchetti C., Di Fiore P.P. Numb is an endocytic protein. J. Cell Biol. 2000, 151:1345-1352.
40. Sawyer J.M., Harrell J.R., Shemer G., Sullivan-Brown J., Roh-Johnson M., Goldstein B. Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 2010, 341:5-19.
41. Schoenenberger C.A., Zuk A., Zinkl G.M., Kendall D., Matlin K.S. Integrin expression and localization in normal MDCK cells and transformed MDCK cells lacking apical polarity. J. Cell Sci. 1994, 107:527-541.
42. Schotman H., Karhinen L., Rabouille C. dGRASP-mediated noncanonical integrin secretion is required for Drosophila epithelial remodeling. Dev. Cell 2008, 14:171-182.
43. Shaye D.D., Casanova J., Llimargas M. Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat. Cell Biol. 2008, 10:964-970.
44. Smith C.A., Lau K.M., Rahmani Z., Dho S.E., Brothers G., She Y.M., Berry D.M., Bonneil E., Thibault P., Schweisguth F., et al. aPKC-mediated phosphorylation regulates asymmetric membrane localization of the cell fate determinant Numb. EMBO J. 2007, 26:468-480.
45. Solon J., Kaya-Copur A., Colombelli J., Brunner D. Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 2009, 137:1331-1342.
46. Sousa R., Lafer E.M. Keep the traffic moving: mechanism of the Hsp70 motor. Traffic 2006, 7:1596-1603.
47. Teckchandani A., Toida N., Goodchild J., Henderson C., Watts J., Wollscheid B., Cooper J.A. Quantitative proteomics identifies a Dab2/integrin module regulating cell migration. J. Cell Biol. 2009, 186:99-111.
48. Thermes V., Grabher C., Ristoratore F., Bourrat F., Choulika A., Wittbrodt J., Joly J.S. I-SceI meganuclease mediates highly efficient transgenesis in fish. Mech. Dev. 2002, 118:91-98.
49. Tong X., Zitserman D., Serebriiskii I., Andrake M., Dunbrack R., Roegiers F. Numb independently antagonizes Sanpodo membrane targeting and Notch signaling in Drosophila sensory organ precursor cells. Mol. Biol. Cell 2010, 21:802-810.
50. Ulrich F., Heisenberg C.P. Trafficking and cell migration. Traffic 2009, 10:811-818.
51. Ungewickell E.J., Hinrichsen L. Endocytosis: clathrin-mediated membrane budding. Curr. Opin. Cell Biol. 2007, 19:417-425.
52. Wakamatsu Y., Maynard T.M., Jones S.U., Weston J.A. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 1999, 23:71-81.
53. Wang Z., Sandiford S., Wu C., Li S.S. Numb regulates cell-cell adhesion and polarity in response to tyrosine kinase signalling. EMBO J. 2009, 28:2360-2373.
54. Wu M., Smith C.L., Hall J.A., Lee I., Luby-Phelps K., Tallquist M.D. Epicardial spindle orientation controls cell entry into the myocardium. Dev. Cell 2010, 19:114-125.
55. Zhong W., Jiang M.M., Weinmaster G., Jan L.Y., Jan Y.N. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 1997, 124:1887-1897.
56. Zhong W., Jiang M.M., Schonemann M.D., Meneses J.J., Pedersen R.A., Jan L.Y., Jan Y.N. Mouse numb is an essential gene involved in cortical neurogenesis. Proc. Natl. Acad. Sci. USA 2000, 97:6844-6849.
57. Zhou P., Alfaro J., Chang E.H., Zhao X., Porcionatto M., Segal R.A. Numb links extracellular cues to intracellular polarity machinery to promote chemotaxis. Dev. Cell 2011, 20:610-622.