Picking up the threads: Extracellular matrix signals in epithelial morphogenesis

Current Opinion in Cell Biology

Volumn 30, Issue 1, 2014, Pages 83-90

  Rodriguez Fraticelli, Alejo E ^a   Martin Belmonte, Fernando ^a  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BASEMENT MEMBRANE; CELL ADHESION; CELL DIFFERENTIATION; CELL MIGRATION; CELL POLARITY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION; CELL MOTION; CELL SHAPE; CYTOLOGY; HUMAN; METABOLISM; STEM CELL; APOPTOSIS; CANCER CELL; CELL FUNCTION; CELL SPREADING; CYTOSKELETON; MECHANOTRANSDUCTION;

CELL MOVEMENT; CELL SHAPE; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84903994544     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.06.008     Document Type: Review

References (71)

1. Datta A., Bryant D.M., Mostov K.E. Molecular regulation of lumen morphogenesis. Curr Biol 2011, 21:R126-R136.
2. Wozniak M.A., Chen C.S. Mechanotransduction in development: a growing role for contractility. Nat Rev Mol Cell Biol 2009, 10:34-43.
3. Lu P., Takai K., Weaver V.M., Werb Z. Extracellular matrix degradation and remodeling in development and disease. Cold Spring Harb Perspect Biol 2011, 3:a005058. 10.1101/cshperspect.a005058.
4. Paszek M.J., Zahir N., Johnson K.R., Lakins J.N., Rozenberg G.I., Gefen A., Reinhart-King C.A., Margulies S.S., Dembo M., Boettiger D., Hammer D.A., Weaver V.M. Tensional homeostasis and the malignant phenotype. Cancer Cell 2005, 8:241-254.
5. Daley W.P., Yamada K.M. ECM-modulated cellular dynamics as a driving force for tissue morphogenesis. Curr Opin Genet Dev 2013, 23:408-414.
6. Spenle C., Simon-Assmann P., Orend G., Miner J.H. Laminin alpha5 guides tissue patterning and organogenesis. Cell Adhes Migr 2013, 7:90-100.
7. O'Brien L.E., Jou T.S., Pollack A.L., Zhang Q., Hansen S.H., Yurchenco P., Mostov K.E. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat Cell Biol 2001, 3:831-838.
8. Debnath J., Mills K.R., Collins N.L., Reginato M.J., Muthuswamy S.K., Brugge J.S. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell 2002, 111:29-40.
9. Muschler J., Lochter A., Roskelley C.D., Yurchenco P., Bissell M.J. Division of labor among the alpha6beta4 integrin, beta1 integrins, and an E3 laminin receptor to signal morphogenesis and beta-casein expression in mammary epithelial cells. Mol Biol Cell 1999, 10:2817-2828.
10. Rasmussen J.P., Reddy S.S., Priess J.R. Laminin is required to orient epithelial polarity in the C. elegans pharynx. Development 2012, 139:2050-2060.
11. Ochoa-Espinosa A., Affolter M. Branching morphogenesis: from cells to organs and back. Cold Spring Harb Perspect Biol 2012, 4:a008243. 10.1101/cshperspect.a008243.
12. Martin-Belmonte F., Yu W., Rodriguez-Fraticelli A.E., Ewald A.J., Werb Z., Alonso M.A., Mostov K. Cell-polarity dynamics controls the mechanism of lumen formation in epithelial morphogenesis. Curr Biol 2008, 18:507-513.
13. Nguyen-Ngoc K.V., Cheung K.J., Brenot A., Shamir E.R., Gray R.S., Hines W.C., Yaswen P., Werb Z., Ewald A.J. ECM microenvironment regulates collective migration and local dissemination in normal and malignant mammary epithelium. Proc Natl Acad Sci USA 2012, 109:E2595-E2604.
14. Rodriguez-Fraticelli A.E., Martin-Belmonte F. Mechanical control of epithelial lumen formation. Small GTPases 2013, 4:136-140.
15. Leight J.L., Wozniak M.A., Chen S., Lynch M.L., Chen C.S. Matrix rigidity regulates a switch between TGF-beta1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 2012, 23:781-791.
16. Alcaraz J., Xu R., Mori H., Nelson C.M., Mroue R., Spencer V.A., Brownfield D., Radisky D.C., Bustamante C., Bissell M.J. Laminin and biomimetic extracellular elasticity enhance functional differentiation in mammary epithelia. EMBO J 2008, 27:2829-2838.
17. Thery M. Micropatterning as a tool to decipher cell morphogenesis and functions. J Cell Sci 2010, 123:4201-4213.
18. Tseng Q., Duchemin-Pelletier E., Deshiere A., Balland M., Guillou H., Filhol O., Thery M. Spatial organization of the extracellular matrix regulates cell-cell junction positioning. Proc Natl Acad Sci USA 2012, 109:1506-1511.
19. Pitaval A., Tseng Q., Bornens M., Thery M. Cell shape and contractility regulate ciliogenesis in cell cycle-arrested cells. J Cell Biol 2010, 191:303-312.
20. Rodriguez-Fraticelli A.E., Auzan M., Alonso M.A., Bornens M., Martin-Belmonte F. Cell confinement controls centrosome positioning and lumen initiation during epithelial morphogenesis. J Cell Biol 2012, 198:1011-1023.
21. Dupont S., Morsut L., Aragona M., Enzo E., Giulitti S., Cordenonsi M., Zanconato F., Le Digabel J., Forcato M., Bicciato S., Elvassore N., Piccolo S. Role of YAP/TAZ in mechanotransduction. Nature 2011, 474:179-183.
22. Connelly J.T., Gautrot J.E., Trappmann B., Tan D.W., Donati G., Huck W.T., Watt F.M. Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat Cell Biol 2010, 12:711-718.
23. Brunet T., Bouclet A., Ahmadi P., Mitrossilis D., Driquez B., Brunet A.C., Henry L., Serman F., Bealle G., Menager C., Dumas-Bouchiat F., Givord D., Yanicostas C., Le-Roy D., Dempsey N.M., Plessis A., Farge E. Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nat Commun 2013, 4:2821.
24. Wang X., Ha T. Defining single molecular forces required to activate integrin and notch signaling. Science 2013, 340:991-994.
25. Halder G., Dupont S., Piccolo S. Transduction of mechanical and cytoskeletal cues by YAP and TAZ. Nat Rev Mol Cell Biol 2012, 13:591-600.
26. Calvo F., Ege N., Grande-Garcia A., Hooper S., Jenkins R.P., Chaudhry S.I., Harrington K., Williamson P., Moeendarbary E., Charras G., Sahai E. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat Cell Biol 2013, 15:637-646.
27. Wang N., Butler J.P., Ingber D.E. Mechanotransduction across the cell surface and through the cytoskeleton. Science 1993, 260:1124-1127.
28. Gregor M., Osmanagic-Myers S., Burgstaller G., Wolfram M., Fischer I., Walko G., Resch G.P., Jorgl A., Herrmann H., Wiche G. Mechanosensing through focal adhesion-anchored intermediate filaments. FASEB J 2014, 28:715-729.
29. Zhang H., Landmann F., Zahreddine H., Rodriguez D., Koch M., Labouesse M. A tension-induced mechanotransduction pathway promotes epithelial morphogenesis. Nature 2011, 471:99-103.
30. Weber G.F., Bjerke M.A., DeSimone D.W. A mechanoresponsive cadherin-keratin complex directs polarized protrusive behavior and collective cell migration. Dev Cell 2012, 22:104-115.
31. Bordeleau F., Myrand Lapierre M.E., Sheng Y., Marceau N. Keratin 8/18 regulation of cell stiffness-extracellular matrix interplay through modulation of Rho-mediated actin cytoskeleton dynamics. PLoS ONE 2012, 7:e38780.
32. Seltmann K., Fritsch A.W., Kas J.A., Magin T.M. Keratins significantly contribute to cell stiffness and impact invasive behavior. Proc Natl Acad Sci USA 2013, 110:18507-18512.
33. Wang N., Tytell J.D., Ingber D.E. Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 2009, 10:75-82.
34. Pozzi A., Zent R. Extracellular matrix receptors in branched organs. Curr Opin Cell Biol 2011, 23:547-553.
35. Klinowska T.C., Soriano J.V., Edwards G.M., Oliver J.M., Valentijn A.J., Montesano R., Streuli C.H. Laminin and beta1 integrins are crucial for normal mammary gland development in the mouse. Dev Biol 1999, 215:13-32.
36. Klinowska T.C., Alexander C.M., Georges-Labouesse E., Van der Neut R., Kreidberg J.A., Jones C.J., Sonnenberg A., Streuli C.H. Epithelial development and differentiation in the mammary gland is not dependent on alpha 3 or alpha 6 integrin subunits. Dev Biol 2001, 233:449-467.
37. Myllymaki S.M., Teravainen T.P., Manninen A. Two distinct integrin-mediated mechanisms contribute to apical lumen formation in epithelial cells. PLoS ONE 2011, 6:e19453.
38. Teravainen T.P., Myllymaki S.M., Friedrichs J., Strohmeyer N., Moyano J.V., Wu C., Matlin K.S., Muller D.J., Manninen A. alphaV-integrins are required for mechanotransduction in MDCK epithelial cells. PLoS ONE 2013, 8:e71485.
39. Dinkins M.B., Fratto V.M., Lemosy E.K. Integrin alpha chains exhibit distinct temporal and spatial localization patterns in epithelial cells of the Drosophila ovary. Dev Dyn 2008, 237:3927-3939.
40. Zovein A.C., Luque A., Turlo K.A., Hofmann J.J., Yee K.M., Becker M.S., Fassler R., Mellman I., Lane T.F., Iruela-Arispe M.L. Beta1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell 2010, 18:39-51.
41. Wickstrom S.A., Lange A., Montanez E., Fassler R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase!. EMBO J 2010, 29:281-291.
42. Sakai T., Li S., Docheva D., Grashoff C., Sakai K., Kostka G., Braun A., Pfeifer A., Yurchenco P.D., Fassler R. Integrin-linked kinase (ILK) is required for polarizing the epiblast, cell adhesion, and controlling actin accumulation. Genes Dev 2003, 17:926-940.
43. Akhtar N., Streuli C.H. An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nat Cell Biol 2013, 15:17-27.
44. Lange A., Wickstrom S.A., Jakobson M., Zent R., Sainio K., Fassler R. Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature 2009, 461:1002-1006.
45. Shibue T., Brooks M.W., Weinberg R.A. An integrin-linked machinery of cytoskeletal regulation that enables experimental tumor initiation and metastatic colonization. Cancer Cell 2013, 24:481-498.
46. Bogdanovic O., Delfino-Machin M., Nicolas-Perez M., Gavilan M.P., Gago-Rodrigues I., Fernandez-Minan A., Lillo C., Rios R.M., Wittbrodt J., Martinez-Morales J.R. Numb/Numbl-Opo antagonism controls retinal epithelium morphogenesis by regulating integrin endocytosis. Dev Cell 2012, 23:782-795.
47. 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.
48. Bello V., Sirour C., Moreau N., Denker E., Darribere T. A function for dystroglycan in pronephros development in Xenopus laevis. Dev Biol 2008, 317:106-120.
49. Scheele S., Falk M., Franzen A., Ellin F., Ferletta M., Lonai P., Andersson B., Timpl R., Forsberg E., Ekblom P. Laminin alpha1 globular domains 4-5 induce fetal development but are not vital for embryonic basement membrane assembly. Proc Natl Acad Sci USA 2005, 102:1502-1506.
50. Durbeej M., Larsson E., Ibraghimov-Beskrovnaya O., Roberds S.L., Campbell K.P., Ekblom P. Non-muscle alpha-dystroglycan is involved in epithelial development. J Cell Biol 1995, 130:79-91.
51. Weir M.L., Oppizzi M.L., Henry M.D., Onishi A., Campbell K.P., Bissell M.J., Muschler J.L. Dystroglycan loss disrupts polarity and beta-casein induction in mammary epithelial cells by perturbing laminin anchoring. J Cell Sci 2006, 119:4047-4058.
52. Esser A.K., Cohen M.B., Henry M.D. Dystroglycan is not required for maintenance of the luminal epithelial basement membrane or cell polarity in the mouse prostate. Prostate 2010, 70:777-787.
53. Mirouse V., Christoforou C.P., Fritsch C., St Johnston D., Ray R.P. Dystroglycan and perlecan provide a basal cue required for epithelial polarity during energetic stress. Dev Cell 2009, 16:83-92.
54. Haack T., Bergstralh D.T., St Johnston D. Damage to the Drosophila follicle cell epithelium produces "false clones" with apparent polarity phenotypes. Biol Open 2013, 2:1313-1320.
55. Tanner K., Mori H., Mroue R., Bruni-Cardoso A., Bissell M.J. Coherent angular motion in the establishment of multicellular architecture of glandular tissues. Proc Natl Acad Sci USA 2012, 109:1973-1978.
56. Wang H., Lacoche S., Huang L., Xue B., Muthuswamy S.K. Rotational motion during three-dimensional morphogenesis of mammary epithelial acini relates to laminin matrix assembly. Proc Natl Acad Sci USA 2013, 110:163-168.
57. Zeng D., Ferrari A., Ulmer J., Veligodskiy A., Fischer P., Spatz J., Ventikos Y., Poulikakos D., Kroschewski R. Three-dimensional modeling of mechanical forces in the extracellular matrix during epithelial lumen formation. Biophys J 2006, 90:4380-4391.
58. Guo Q., Xia B., Moshiach S., Xu C., Jiang Y., Chen Y., Sun Y., Lahti J.M., Zhang X.A. The microenvironmental determinants for kidney epithelial cyst morphogenesis. Eur J Cell Biol 2008, 87:251-266.
59. Haigo S.L., Bilder D. Global tissue revolutions in a morphogenetic movement controlling elongation. Science 2011, 331:1071-1074.
60. Lerner D.W., McCoy D., Isabella A.J., Mahowald A.P., Gerlach G.F., Chaudhry T.A., Horne-Badovinac S. A Rab10-dependent mechanism for polarized basement membrane secretion during organ morphogenesis. Dev Cell 2013, 24:159-168.
61. Bilder D., Haigo S.L. Expanding the morphogenetic repertoire: perspectives from the Drosophila egg. Dev Cell 2012, 22:12-23.
62. Lu P., Weaver V.M., Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012, 196:395-406.
63. Moreno-Bueno G., Salvador F., Martin A., Floristan A., Cuevas E.P., Santos V., Montes A., Morales S., Castilla M.A., Rojo-Sebastian A., Martinez A., Hardisson D., Csiszar K., Portillo F., Peinado H., Palacios J., Cano A. Lysyl oxidase-like 2 (LOXL2), a new regulator of cell polarity required for metastatic dissemination of basal-like breast carcinomas. EMBO Mol Med 2011, 3:528-544.
64. Koshikawa N., Schenk S., Moeckel G., Sharabi A., Miyazaki K., Gardner H., Zent R., Quaranta V. Proteolytic processing of laminin-5 by MT1-MMP in tissues and its effects on epithelial cell morphology. FASEB J 2004, 18:364-366.
65. Gilles C., Polette M., Coraux C., Tournier J.M., Meneguzzi G., Munaut C., Volders L., Rousselle P., Birembaut P., Foidart J.M. Contribution of MT1-MMP and of human laminin-5 gamma2 chain degradation to mammary epithelial cell migration. J Cell Sci 2001, 114:2967-2976.
66. Stratman A.N., Saunders W.B., Sacharidou A., Koh W., Fisher K.E., Zawieja D.C., Davis M.J., Davis G.E. Endothelial cell lumen and vascular guidance tunnel formation requires MT1-MMP-dependent proteolysis in 3-dimensional collagen matrices. Blood 2009, 114:237-247.
67. Sacharidou A., Koh W., Stratman A.N., Mayo A.M., Fisher K.E., Davis G.E. Endothelial lumen signaling complexes control 3D matrix-specific tubulogenesis through interdependent Cdc42- and MT1-MMP-mediated events. Blood 2010, 115:5259-5269.
68. Kheradmand F., Rishi K., Werb Z. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMP-mediated activation of gelatinase A/MMP2. J Cell Sci 2002, 115:839-848.
69. Weaver S.A., Wolters B., Ito N., Woskowicz A.M., Kaneko K., Shitomi Y., Seiki M., Itoh Y. Basal localization of MT1-MMP is essential for epithelial cell morphogenesis in 3D collagen matrix. J Cell Sci 2014, 127:1203-1213.
70. Mori H., Lo A.T., Inman J.L., Alcaraz J., Ghajar C.M., Mott J.D., Nelson C.M., Chen C.S., Zhang H., Bascom J.L., Seiki M., Bissell M.J. Transmembrane/cytoplasmic, rather than catalytic, domains of Mmp14 signal to MAPK activation and mammary branching morphogenesis via binding to integrin beta1. Development 2013, 140:343-352.
71. Williams B.B., Cantrell V.A., Mundell N.A., Bennett A.C., Quick R.E., Jessen J.R. VANGL2 regulates membrane trafficking of MMP14 to control cell polarity and migration. J Cell Sci 2012, 125:2141-2147.