Anchors and Signals: The diverse roles of integrins in development

Current Topics in Developmental Biology

Volumn 112, Issue , 2015, Pages 233-272

  Maartens, Aidan P ^a   Brown, Nicholas H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cell migration; Cell signaling; Extracellular matrix; Integrin adhesion; Mechanotransduction

Indexed keywords

INTEGRIN;

ANIMAL; CELL ADHESION; DEVELOPMENTAL BIOLOGY; HUMAN; PHYSIOLOGY;

ANIMALS; CELL ADHESION; DEVELOPMENTAL BIOLOGY; HUMANS; INTEGRINS;

EID: 84926177669     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctdb.2014.11.020     Document Type: Chapter

References (177)

1. Abercrombie M. Croonian lecture, 1978-Crawling movement of metazoan cells. Proceedings of the Royal Society Series B Biological Sciences 1980, 207(1167):129-147. 10.1098/Rspb.1980.0017.
2. Ablooglu A.J., Tkachenko E., Kang J.A., Shattil S.J. Integrin alpha V is necessary for gastrulation movements that regulate vertebrate body asymmetry. Development 2010, 137(20):3449-3458. 10.1242/Dev.045310.
3. Akhtar N., Streuli C.H. An integrin-ILK-microtubule network orients cell polarity and lumen formation in glandular epithelium. Nature Cell Biology 2013, 15(1):17-27. 10.1038/Ncb2646.
4. Akiyama S.K., Yamada S.S., Chen W.T., Yamada K.M. Analysis of fibronectin receptor function with monoclonal-antibodies-Roles in cell-adhesion, migration, matrix assembly, and cytoskeletal organization. Journal of Cell Biology 1989, 109(2):863-875. 10.1083/Jcb.109.2.863.
5. Anderson R., Fassler R., Georges-Labouesse E., Hynes R.O., Bader B.L., Kreidberg J.A., et al. Mouse primordial germ cells lacking beta 1 integrins enter the germline but fail to migrate normally to the gonads. Development 1999, 126(8):1655-1664.
6. Antoniades I., Stylianou P., Skourides P.A. Making the connection: Ciliary adhesion complexes anchor basal bodies to the actin cytoskeleton. Developmental Cell 2014, 28(1):70-80. 10.1016/J.Devcel.2013.12.003.
7. Bard J.B.L., Hay E.D. Behavior of fibroblasts from developing avian cornea-Morphology and movement insitu and invitro. Journal of Cell Biology 1975, 67(2):400-418. 10.1083/Jcb.67.2.400.
8. Baron W., Colognato H., Ffrench-Constant C. Integrin-growth factor interactions as regulators of oligodendroglial development and function. Glia 2005, 51(1):80. (vol. 49, p. 467, 2005). 10.1002/Glia.20238.
9. Bedzhov I., Zernicka-Goetz M. Self-organizing properties of mouse pluripotent cells initiate morphogenesis upon implantation. Cell 2014, 156(5):1032-1044. 10.1016/J.Cell.2014.01.023.
10. Belvindrah R., Hankel S., Walker J., Patton B.L., Muller U. beta 1 integrins control the formation of cell chains in the adult rostral migratory stream. Journal of Neuroscience 2007, 27(10):2704-2717. 10.1523/Jneurosci.2991-06.2007.
11. Bergstralh D.T., Lovegrove H.E., St Johnston D. Discs large links spindle orientation to apical-basal polarity in drosophila epithelia. Current Biology 2013, 23(17):1707-1712. 10.1016/J.Cub.2013.07.017.
12. Bershadsky A.D., Balaban N.Q., Geiger B. Adhesion-dependent cell mechanosensitivity. Annual Review of Cell and Developmental Biology 2003, 19:677-695. 10.1146/Annurev.Cellbio.19.111301.153011.
13. Bhat N., Riley B.B. Integrin-alpha 5 coordinates assembly of posterior cranial placodes in zebrafish and enhances Fgf-dependent regulation of Otic/epibranchial cells. Plos One 2011, 6(12):e27778. 10.1371/journal.pone.0027778.
14. Bilder D., Haigo S.L. Expanding the morphogenetic repertoire: Perspectives from the Drosophila egg. Developmental Cell 2012, 22(1):12-23. 10.1016/J.Devcel.2011.12.003.
15. Bokel C., Brown N.H. Integrins in development: Moving on, responding to, and sticking to the extracellular matrix. Developmental Cell 2002, 3(3):311-321. 10.1016/S1534-5807(02)00265-4.
16. Boube M., Martin-Bermudo M.D., Brown N.H., Casanova J. Specific tracheal migration is mediated by complementary expression of cell surface proteins. Genes & Development 2001, 15(12):1554-1562. 10.1101/Gad.195501.
17. Boudreau N., Sympson C.J., Werb Z., Bissell M.J. Suppression of ice and apoptosis in mammary epithelial-cells by extracellular-matrix. Science 1995, 267(5199):891-893. 10.1126/Science.7531366.
18. Bouvard D., Brakebusch C., Gustafsson E., Aszodi A., Bengtsson T., Berna A., et al. Functional consequences of integrin gene mutations in mice. Circulation Research 2001, 89(3):211-223. 10.1161/Hh1501.094874.
19. Brabant M.C., Fristrom D., Bunch T.A., Brower D.L. Distinct spatial and temporal functions for PS integrins during Drosophila wing morphogenesis. Development 1996, 122(10):3307-3317.
20. Breau M.A., Pietri T., Eder O., Blanche M., Brakebusch C., Fassler R., et al. Lack of beta 1 integrins in enteric neural crest cells leads to a Hirschsprung-like phenotype. Development 2006, 133(9):1725-1734. 10.1242/Dev.02346.
21. Brower D.L. Platelets with wings: The maturation of Drosophila integrin biology. Current Opinion in Cell Biology 2003, 15(5):607-613. 10.1016/S0955-0674(03)00102-9.
22. Brower D.L., Jaffe S.M. Requirement for integrins during Drosophila wing development. Nature 1989, 342(6247):285-287. 10.1038/342285a0.
23. Brown N.H. Cell-cell adhesion via the ECM: Integrin genetics in fly and worm. Matrix Biology 2000, 19(3):191-201. 10.1016/S0945-053x(00)00064-0.
24. Brown N.H. Extracellular matrix in development: Insights from mechanisms conserved between invertebrates and vertebrates. Cold Spring Harbor Perspectives in Biology 2011, 3:a005082. 10.1101/cshperspect.a005082.
25. Brown N.H., Gregory S.L., Rickoll W.L., Fessler L.I., Prout M., White R.A.H., et al. Talin is essential for integrin function in Drosophila. Developmental Cell 2002, 3(4):569-579. 10.1016/S1534-5807(02)00290-3.
26. Brunet T., Bouclet A., Ahmadi P., Mitrossilis D., Driquez B., Brunet A.C., et al. Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria. Nature Communications 2013, 4:2821. 10.1038/Ncomms3821.
27. Bukharova T., Weijer G., Bosgraaf L., Dormann D., van Haastert P.J., Weijer C.J. Paxillin is required for cell-substrate adhesion, cell sorting and slug migration during Dictyostelium development. Journal of Cell Science 2005, 118(20):4913. (vol. 118, p. 4295, 2005).
28. Burridge K., Feramisco J.R. Micro-injection and localization of a 130k-protein in living fibroblasts-Relationship to actin and fibronectin. Cell 1980, 19(3):587-595. 10.1016/S0092-8674(80)80035-3.
29. Cai D.F., Chen S.C., Prasad M., He L., Wang X.B., Choesmel-Cadamuro V., et al. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014, 157(5):1146-1159. 10.1016/J.Cell.2014.03.045.
30. Campbell I.D., Humphries M.J. Integrin structure, activation, and interactions. Cold Spring Harbor Perspectives in Biology 2011, 3:a004994. 10.1101/cshperspect.a004994.
31. Carisey A., Tsang R., Greiner A.M., Nijenhuis N., Heath N., Nazgiewicz A., et al. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Current Biology 2013, 23(4):271-281. 10.1016/J.Cub.2013.01.009.
32. Chen J.C., Krasnow M.A. Integrin beta 1 suppresses multilayering of a simple epithelium. Plos One 2012, 7(12):e52886. 10.1371/journal.pone.0052886.
33. Chen S.Y., Lewallen M., Xie T. Adhesion in the stem cell niche: Biological roles and regulation. Development 2013, 140(2):255-265. 10.1242/Dev.083139.
34. Cheng P., Andersen P., Hassel D., Kaynak B.L., Limphong P., Juergensen L., et al. Fibronectin mediates mesendodermal cell fate decisions. Development 2013, 140(12):2587-2596. 10.1242/Dev.089052.
35. Chiarugi P., Giannoni E. Anoikis: A necessary death program for anchorage-dependent cells. Biochemical Pharmacology 2008, 76(11):1352-1364. 10.1016/J.Bcp.2008.07.023.
36. Ciruna B., Rossant J. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Developmental Cell 2001, 1(1):37-49. 10.1016/S1534-5807(01)00017-X.
37. Comber K., Huelsmann S., Evans I., Sanchez-Sanchez B.J., Chalmers A., Reuter R., et al. A dual role for the beta PS integrin myospheroid in mediating Drosophila embryonic macrophage migration. Journal of Cell Science 2013, 126(15):3475-3484. 10.1242/Jcs.129700.
38. Conti F.J., Monkley S.J., Wood M.R., Critchley D.R., Muller U. Talin 1 and 2 are required for myoblast fusion, sarcomere assembly and the maintenance of myotendinous junctions. Development 2009, 136(21):3597-3606. 10.1242/Dev.035857.
39. Critchley D.R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annual Review of Biophysics 2009, 38:235-254. 10.1146/Annurev.Biophys.050708.133744.
40. Crump J.G., Swartz M.E., Kimmel C.B. An integrin-dependent role of pouch endoderm in hyoid cartilage development. Plos Biology 2004, 2(9):1432-1445. 10.1371/journal.pbio.0020244.
41. Davidson B. Ciona intestinalis as a model for cardiac development. Seminars in Cell & Developmental Biology 2007, 18(1):16-26. 10.1016/J.Semcdb.2006.12.007.
42. Davidson L.A., Dzamba B.D., Keller R., Desimone D.W. Live imaging of cell protrusive activity, and extracellular matrix assembly and remodeling during morphogenesis in the frog, Xenopus laevis. Developmental Dynamics 2008, 237(10):2684-2692. 10.1002/Dvdy.21600.
43. De Arcangelis A., Mark M., Kreidberg J., Sorokin L., Georges-Labouesse E. Synergistic activities of alpha 3 and alpha 6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 1999, 126(17):3957-3968.
44. Deakin N.O., Turner C.E. Paxillin comes of age. Journal of Cell Science 2008, 121(15):2435-2444. 10.1242/Jcs.018044.
45. del Rio A., Perez-Jimenez R., Liu R.C., Roca-Cusachs P., Fernandez J.M., Sheetz M.P. Stretching single talin rod molecules activates vinculin binding. Science 2009, 323(5914):638-641. 10.1126/Science.1162912.
46. Delon I., Brown N.H. The integrin adhesion complex changes its composition and function during morphogenesis of an epithelium. Journal of Cell Science 2009, 122(23):4363-4374. 10.1242/Jcs.055996.
47. Devenport D., Brown N.H. Morphogenesis in the absence of integrins: Mutation of both Drosophila beta subunits prevents midgut migration. Development 2004, 131(21):5405-5415. 10.1242/Dev.01427.
48. Discher D.E., Janmey P., Wang Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 2005, 310(5751):1139-1143. 10.1126/Science.1116995.
49. Dray N., Lawton A., Nandi A., Julich D., Emonet T., Holley S.A. Cell-fibronectin interactions propel vertebrate trunk elongation via tissue mechanics. Current Biology 2013, 23(14):1335-1341. 10.1016/J.Cub.2013.05.052.
50. DuFort C.C., Paszek M.J., Weaver V.M. Balancing forces: Architectural control of mechanotransduction. Nature Reviews Molecular Cell Biology 2011, 12(5):308-319. 10.1038/Nrm3112.
51. Dupuy A.G., Caron E. Integrin-dependent phagocytosis-Spreading from microadhesion to new concepts. Journal of Cell Science 2008, 121(11):1773-1783. 10.1242/Jcs.018036.
52. Ellis S.J., Tanentzapf G. Integrin-mediated adhesion and stem-cell-niche interactions. Cell and Tissue Research 2010, 339(1):121-130. 10.1007/S00441-009-0828-4.
53. Engler A.J., Sen S., Sweeney H.L., Discher D.E. Matrix elasticity directs stem cell lineage specification. Cell 2006, 126(4):677-689. 10.1016/J.Cell.2006.06.044.
54. Fairclough S.R., Dayel M.J., King N. Multicellular development in a choanoflagellate. Current Biology 2010, 20(20):R875-R876. 10.1016/J.Cub.2010.09.014.
55. Farge E. Mechanical induction of twist in the Drosophila foregut/stomodeal primordium. Current Biology 2003, 13(16):1365-1377. 10.1016/S0960-9822(03)00576-1.
56. Fassler R., Meyer M. Consequences of lack of beta-1 integrin gene-expression in mice. Genes & Development 1995, 9(15):1896-1908. 10.1101/Gad.9.15.1896.
57. Fernandez-Minan A., Martin-Bermudo M.D., Gonzalez-Reyes A. Integrin signaling regulates spindle orientation in Drosophila to preserve the follicular-epithelium monolayer. Current Biology 2007, 17(8):683-688. 10.1016/J.Cub.2007.02.052.
58. Fogerty F.J., Fessler L.I., Bunch T.A., Yaron Y., Parker C.G., Nelson R.E., et al. Tiggrin, a novel Drosophila extracellular-matrix protein that functions as a ligand for Drosophila alpha(Ps2)beta(Ps) integrins. Development 1994, 120(7):1747-1758.
59. Freeman M., Gurdon J.B. Regulatory principles of developmental signaling. Annual Review of Cell and Developmental Biology 2002, 18:515-539. 10.1146/Annurev.Cellbio.18.012502.083458.
60. Frick A., Grammel D., Schmidt F., Poschl J., Priller M., Pagella P., et al. Proper cerebellar development requires expression of beta 1-integrin in Bergmann glia, but not in granule neurons. Glia 2012, 60(5):820-832. 10.1002/Glia.22314.
61. Friedl P., Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nature Reviews Molecular Cell Biology 2009, 10(7):445-457. 10.1038/Nrm2720.
62. Friedl P., Sahai E., Weiss S., Yamada K.M. New dimensions in cell migration. Nature Reviews Molecular Cell Biology 2012, 13(11):743-747. 10.1038/Nrm3459.
63. Friedland J.C., Lee M.H., Boettiger D. Mechanically activated integrin switch controls alpha(5)beta(1) function. Science 2009, 323(5914):642-644. 10.1126/Science.1168441.
64. Frisch S.M., Francis H. Disruption of epithelial cell-matrix interactions induces apoptosis. Journal of Cell Biology 1994, 124(4):619-626. 10.1083/Jcb.124.4.619.
65. Fuchs Y., Steller H. Programmed cell death in animal development and disease. Cell 2011, 147(4):742-758. 10.1016/J.Cell.2011.10.033.
66. Garcia-Bellido A. Genetic control of wing disc development in Drosophila. Ciba Foundation Symposium 1975, 29:161-182.
67. Geiger B. 130k protein from chicken gizzard-Its localization at the termini of microfilament bundles in cultured chicken-cells. Cell 1979, 18(1):193-205. 10.1016/0092-8674(79)90368-4.
68. Geiger B., Yamada K.M. Molecular architecture and function of matrix adhesions. Cold Spring Harbor Perspectives in Biology 2011, 3:a005033. 10.1101/cshperspect.a005033.
69. Georges-Labouesse E., Mark M., Messaddeq N., Gansmuller A. Essential role of alpha 6 integrins in cortical and retinal lamination. Current Biology 1998, 8(17):983-986. 10.1016/S0960-9822(98)70402-6.
70. Gilbert S.F. Conceptual breakthroughs in developmental biology. Journal of Biosciences 1998, 23(3):169-176. 10.1007/Bf02720017.
71. Gillies T.E., Cabernard C. Cell division orientation in animals. Current Biology 2011, 21(15):R599-R609. 10.1016/J.Cub.2011.06.055.
72. Goh K.L., Yang J.T., Hynes R.O. Mesodermal defects and cranial neural crest apoptosis in alpha 5 integrin-null embryos. Development 1997, 124(21):4309-4319.
73. Gotwals P.J., Fessler L.I., Wehrli M., Hynes R.O. Drosophila Ps1 integrin is a laminin receptor and differs in ligand specificity from Ps2. Proceedings of the National Academy of Sciences of the United States of America 1994, 91(24):11447-11451. 10.1073/Pnas.91.24.11447.
74. Goulas S., Conder R., Knoblich J.A. The par complex and integrins direct asymmetric cell division in adult intestinal stem cells. Cell Stem Cell 2012, 11(4):529-540. 10.1016/J.Stem.2012.06.017.
75. Hagedorn E.J., Yashiro H., Ziel J.W., Ihara S., Wang Z., Sherwood D.R. Integrin acts upstream of netrin signaling to regulate formation of the anchor cell's invasive membrane in C. elegans. Developmental Cell 2009, 17(2):187-198. 10.1016/J.Devcel.2009.06.006.
76. Haigo S.L., Bilder D. Global tissue revolutions in a morphogenetic movement controlling elongation. Science 2011, 331(6020):1071-1074. 10.1126/Science.1199424.
77. Halbleib J.M., Nelson W.J. Cadherins in development: Cell adhesion, sorting, and tissue morphogenesis. Genes & Development 2006, 20(23):3199-3214. 10.1101/Gad.1486806.
78. Haubst N., Georges-Labouesse E., De Arcangelis A., Mayer U., Gotz M. Basement membrane attachment is dispensable for radial glial cell fate and for proliferation, but affects positioning of neuronal subtypes. Development 2006, 133(16):3245-3254. 10.1242/Dev.02486.
79. Heller E., Kumar K.V., Grill S.W., Fuchs E. Forces generated by cell intercalation tow epidermal sheets in mammalian tissue morphogenesis. Developmental Cell 2014, 28(6):617-632. 10.1016/J.Devcel.2014.02.011.
80. Hresko M.C., Williams B.D., Waterston R.H. Assembly of body-wall muscle and muscle-cell attachment structures in Caenorhabditis elegans. Journal of Cell Biology 1994, 124(4):491-506. 10.1083/Jcb.124.4.491.
81. Hsieh H.H., Hsu T.Y., Jiang H.S., Wu Y.C. Integrin alpha PAT-2/CDC-42 signaling is required for muscle-mediated clearance of apoptotic cells in Caenorhabditis elegans. Plos Genetics 2012, 8(5):e1002663. 10.1371/Journal.Pgen.1002663.
82. Hsu T.Y., Wu Y.C. Engulfment of apoptotic cells in C. elegans is mediated by integrin alpha/SRC signaling. Current Biology 2010, 20(6):477-486. 10.1016/J.Cub.2010.01.062.
83. Humphries J.D., Byron A., Humphries M.J. Integrin ligands at a glance. Journal of Cell Science 2006, 119(19):3901-3903. 10.1242/Jcs.03098.
84. Huttenlocher A., Horwitz A.R. Integrins in cell migration. Cold Spring Harbor Perspectives in Biology 2011, 3:a005074. 10.1101/cshperspect.a005074.
85. Huveneers S., Danen E.H.J. Adhesion signaling-Crosstalk between integrins, Src and Rho. Journal of Cell Science 2009, 122(8):1059-1069. 10.1242/Jcs.039446.
86. Hynes R.O. Integrins-A family of cell-surface receptors. Cell 1987, 48(4):549-554. 10.1016/0092-8674(87)90233-9.
87. Hynes R.O., Zhao Q. The evolution of cell adhesion. Journal of Cell Biology 2000, 150(2):F89-F95. 10.1083/Jcb.150.2.F89.
88. Ihara S., Hagedorn E.J., Morrissey M.A., Chi Q.Y., Motegi F., Kramer J.M., et al. Basement membrane sliding and targeted adhesion remodels tissue boundaries during uterine-vulval attachment in Caenorhabditis elegans. Nature Cell Biology 2011, 13(6):641-651. 10.1038/Ncb2233.
89. Julich D., Geisler R., Holley S.A., Tübingen 2000 Screen Consortium Integrin alpha 5 and delta/notch signaling have complementary spatiotemporal requirements during zebrafish somitogenesis. Developmental Cell 2005, 8(4):575-586. 10.1016/J.Devcel.2005.01.016.
90. Julich D., Mould A.P., Koper E., Holley S.A. Control of extracellular matrix assembly along tissue boundaries via Integrin and Eph/Ephrin signaling. Development 2009, 136(17):2913-2921. 10.1242/Dev.038935.
91. Kardash E., Reichman-Fried M., Maitre J.L., Boldajipour B., Papusheva E., Messerschmidt E.M., et al. A role for Rho GTPases and cell-cell adhesion in single-cell motility in vivo. Nature Cell Biology 2010, 12(1):47-53. 10.1038/Ncb2003.
92. Kelley L.C., Lohmer L.L., Hagedorn E.J., Sherwood D.R. Traversing the basement membrane in vivo: A diversity of strategies. Journal of Cell Biology 2014, 204(3):291-302. 10.1083/Jcb.201311112.
93. Koshida S., Kishimoto Y.K., Ustumi H., Shimizu T., Furutani-Seiki M., Kondoh H., et al. Integrin alpha 5-dependent fibronectin accumulation for maintenance of somite boundaries in zebrafish embryos. Developmental Cell 2005, 8(4):587-598. 10.1016/J.Devcel.2005.03.006.
94. Kragtorp K.A., Miller J.R. Integrin alpha 5 is required for somite rotation and boundary formation in Xenopus. Developmental Dynamics 2007, 236(9):2713-2720. 10.1002/Dvdy.21280.
95. Kreitmeier M., Gerisch G., Heizer C., Mullertaubenberger A. A talin homolog of dictyostelium rapidly assembles at the leading-edge of cells in response to chemoattractant. Journal of Cell Biology 1995, 129(1):179-188. 10.1083/Jcb.129.1.179.
96. Kubow K.E., Horwitz A.R. Reducing background fluorescence reveals adhesions in 3D matrices. Nature Cell Biology 2011, 13(1):3-5.
97. Lallier T.E., Desimone D.W. Separation of neural induction and neurulation in Xenopus. Developmental Biology 2000, 225(1):135-150. 10.1006/Dbio.2000.9833.
98. Lammermann T., Bader B.L., Monkley S.J., Worbs T., Wedlich-Soldner R., Hirsch K., et al. Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 2008, 453(7191):51-55. 10.1038/Nature06887.
99. Larsen E., Mclaughlin H.M.G. The morphogenetic alphabet-lessons for simple-minded genes. Bioessays 1987, 7(3):130-132. 10.1002/Bies.950070309.
100. le Duc Q., Shi Q.M., Blonk I., Sonnenberg A., Wang N., Leckband D., et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. Journal of Cell Biology 2010, 191(4):891. (vol. 189, p. 1107, 2010). 10.1083/Jcb.20100114920101020c.
101. Lechler T., Fuchs E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005, 437(7056):275-280. 10.1038/Nature03922.
102. Lecuit T., Lenne P.F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annual Review of Cell and Developmental Biology 2011, 27(27):157-184. 10.1146/Annurev-Cellbio-100109-104027.
103. Lee J.L., Streuli C.H. Integrins and epithelial cell polarity. Journal of Cell Science 2014, 127(15):3217-3225. 10.1242/Jcs.146142.
104. Lee S., Zhou L.L., Kim J., Kalbfleisch S., Schock F. Lasp anchors the Drosophila male stem cell niche and mediates spermatid individualization. Mechanisms of Development 2008, 125(9-10):768-776. 10.1016/J.Mod.2008.06.012.
105. Leu S.T., Jacques S.A.L., Wingerd K.L., Hikita S.T., Tolhurst E.C., Pring J.L., et al. Integrin alpha-4 beta 1 function is required for cell survival in developing retina. Developmental Biology 2004, 276(2):416-430. 10.1016/J.Ydbio.2004.09.003.
106. Lewellyn L., Cetera M., Horne-Badovinac S. Misshapen decreases integrin levels to promote epithelial motility and planar polarity in Drosophila. Journal of Cell Biology 2013, 200(6):721-729. 10.1083/Jcb.201209129.
107. Lin Y.H., Park Z.Y., Lin D., Brahmbhatt A.A., Rio M.C., Yates J.R., et al. Regulation of cell migration and survival by focal adhesion targeting of Lasp-1. Journal of Cell Biology 2004, 165(3):421-432. 10.1083/Jcb.200311045.
108. Lin G.N., Zhang X., Ren J., Pang Z.M., Wang C.H., Xu N., et al. Integrin signaling is required for maintenance and proliferation of intestinal stem cells in Drosophila. Developmental Biology 2013, 377(1):177-187. 10.1016/J.Ydbio.2013.01.032.
109. Liu J., He X.W., Corbett S.A., Lowry S.F., Graham A.M., Fassler R., et al. Integrins are required for the differentiation of visceral endoderm. Journal of Cell Science 2009, 122(2):233-242. 10.1242/Jcs.037663.
110. Loulier K., Lathia J.D., Marthiens V., Relucio J., Mughal M.R., Tang S.C., et al. beta 1 integrin maintains integrity of the embryonic neocortical stem cell niche. Plos Biology 2009, 7(8):e1000176. 10.1371/Journal.Pbio.1000176.
111. Mammoto T., Mammoto A., Ingber D.E. Mechanobiology and developmental control. Annual Review of Cell and Developmental Biology 2013, 29(29):27-61. 10.1146/Annurev-Cellbio-101512-122340.
112. Marsden M., Burke R.D. The beta L integrin subunit is necessary for gastrulation in sea urchin embryos. Developmental Biology 1998, 203(1):134-148. 10.1006/Dbio.1998.9033.
113. Marsden M., DeSimone D.W. Regulation of cell polarity, radial intercalation and epiboly in Xenopus: Novel roles for integrin and fibronectin. Development 2001, 128(18):3635-3647.
114. Marsden M., DeSimone D.W. Integrin-ECM interactions regulate cadherin-dependent cell adhesion and are required for convergent extension in Xenopus. Current Biology 2003, 13(14):1182-1191. 10.1016/S0960-9822(03)00433-0.
115. Marthiens V., Kazanis I., Moss L., Long K., Ffrench-Constant C. Adhesion molecules in the stem cell niche-More than just staying in shape?. Journal of Cell Science 2010, 123(10):1613-1622. 10.1242/Jcs.054312.
116. Martin-Bermudo M.D., Alvarez-Garcia I., Brown N.H. Migration of the Drosophila primordial midgut cells requires coordination of diverse PS integrin functions. Development 1999, 126(22):5161-5169.
117. Matus D.Q., Chang E., Makohon-Moore S.C., Hagedorn M.A., Chi Q.Y., Sherwood D.R. Cell division and targeted cell cycle arrest opens and stabilizes basement membrane gaps. Nature Communications 2014, 5:4184. 10.1038/Ncomms5184.
118. Meighan C.M., Schwarzbauer J.E. Temporal and spatial regulation of integrins during development. Current Opinion in Cell Biology 2008, 20(5):520-524. 10.1016/J.Ceb.2008.05.010.
119. Miller C.J., Davidson L.A. The interplay between cell signalling and mechanics in developmental processes. Nature Reviews Genetics 2013, 14(10):733-744. 10.1038/Nrg3513.
120. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: In command and control of cell motility. Nature Reviews Molecular Cell Biology 2005, 6(1):56-68. 10.1038/Nrm1549.
121. Moreira C.G.A., Jacinto A., Prag S. Drosophila integrin adhesion complexes are essential for hemocyte migration in vivo. Biology Open 2013, 2:795-801. 10.1242/bio.20134564.
122. Morita H., Kajiura-Kobayashi H., Takagi C., Yamamoto T.S., Nonaka S., Ueno N. Cell movements of the deep layer of non-neural ectoderm underlie complete neural tube closure in Xenopus. Development 2012, 139(8):1417-1426. 10.1242/Dev.073239.
123. Morrison S.J., Spradling A.C. Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life. Cell 2008, 132(4):598-611. 10.1016/J.Cell.2008.01.038.
124. Nair S., Schilling T.F. Chemokine signaling controls endodermal migration during zebrafish gastrulation. Science 2008, 322(5898):89-92. 10.1126/Science.1160038.
125. Naylor M.J., Li N., Cheung J., Lowe E.T., Lambert E., Marlow R., et al. Ablation of beta 1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. Journal of Cell Biology 2005, 171(4):717-728. 10.1083/Jcb.200503144.
126. Norton J., Cooley J., Islam A.F.M.T., Cota C.D., Davidson B. Matrix adhesion polarizes heart progenitor induction in the invertebrate chordate Ciona intestinalis. Development 2013, 140(6):1301-1311. 10.1242/Dev.085548.
127. O'Reilly A.M., Lee H.H., Simon M.A. Integrins control the positioning and proliferation of follicle stem cells in the Drosophila ovary. Journal of Cell Biology 2008, 182(4):801-815. 10.1083/Jcb.200710141.
128. Petrie R.J., Gavara N., Chadwick R.S., Yamada K.M. Nonpolarized signaling reveals two distinct modes of 3D cell migration. Journal of Cell Biology 2012, 197(3):439-455. 10.1083/Jcb.201201124.
129. Petrie R.J., Koo H., Yamada K.M. Generation of compartmentalized pressure by a nuclear piston governs cell motility in a 3D matrix. Science 2014, 345(6200):1062-1065. 10.1126/science.1256965.
130. Pines M., Das R., Ellis S.J., Morin A., Czerniecki S., Yuan L., et al. Mechanical force regulates integrin turnover in Drosophila in vivo. Nature Cell Biology 2012, 14(9):935-943. 10.1038/Ncb2555.
131. Pullan S., Wilson J., Metcalfe A., Edwards G.M., Goberdhan N., Tilly J., et al. Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. Journal of Cell Science 1996, 109:631-642.
132. Qiao L.J., Gao H.W., Zhang T., Jing L.L., Xiao C., Xiao Y., et al. Snail modulates the assembly of fibronectin via alpha 5 integrin for myocardial migration in zebrafish embryos. Scientific Reports 2014, 4:4470. 10.1038/Srep04470.
133. Rallis C., Pinchin S.M., Ish-Horowicz D. Cell-autonomous integrin control of Wnt and Notch signalling during somitogenesis. Development 2010, 137(21):3591-3601. 10.1242/Dev.050070.
134. Rasmussen J.P., Reddy S.S., Priess J.R. Laminin is required to orient epithelial polarity in the C. elegans pharynx. Development 2012, 139(11):2050-2060. 10.1242/Dev.078360.
135. Reddien P.W., Horvitz H.R. The engulfment process of programmed cell death in Caenorhabditis elegans. Annual Review of Cell and Developmental Biology 2004, 20:193-221. 10.1146/Annurev.Cellbio.20.022003.114619.
136. Richardson B.E., Lehmann R. Mechanisms guiding primordial germ cell migration: Strategies from different organisms. Nature Reviews Molecular Cell Biology 2010, 11(1):37-49. 10.1038/Nrm2815.
137. Richter D.J., King N. The genomic and cellular foundations of animal origins. Annual Review of Genetics 2013, 47(47):509-537. 10.1146/Annurev-Genet-111212-133456.
138. Rohrschneider L.R. Adhesion plaques of rous-sarcoma virus-transformed cells contain the Src gene-product. Proceedings of the National Academy of Sciences of the United States of America-Biological Sciences 1980, 77(6):3514-3518. 10.1073/Pnas.77.6.3514.
139. Ross T.D., Coon B.G., Yun S., Baeyens N., Tanaka K., Ouyang M.X., et al. Integrins in mechanotransduction. Current Opinion in Cell Biology 2013, 25(5):613-618. 10.1016/J.Ceb.2013.05.006.
140. Rozario T., DeSimone D.W. The extracellular matrix in development and morphogenesis: A dynamic view. Developmental Biology 2010, 341(1):126-140. 10.1016/J.Ydbio.2009.10.026.
141. Schwartz M.A. Integrins and extracellular matrix in mechanotransduction. Cold Spring Harbor Perspectives in Biology 2010, 2:a005066. 10.1101/cshperspect.a005066.
142. Sebe-Pedros A., Irimia M., del Campo J., Parra-Acero H., Russ C., Nusbaum C., et al. Regulated aggregative multicellularity in a close unicellular relative of metazoa. Elife 2013, 2:e02187. 10.7554/eLife.01287.
143. Seifert J.R.K., Lehmann R. Drosophila primordial germ cell migration requires epithelial remodeling of the endoderm. Development 2012, 139(12):2101-2106. 10.1242/Dev.078949.
144. Shen Q., Wang Y., Kokovay E., Lin G., Chuang S.M., Goderie S.K., et al. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008, 3(3):289-300. 10.1016/J.Stem.2008.07.026.
145. Streuli C.H. Integrins and cell-fate determination. Journal of Cell Science 2009, 122(2):171-177. 10.1242/Jcs.018945.
146. Streuli C.H., Akhtar N. Signal co-operation between integrins and other receptor systems. Biochemical Journal 2009, 418:491-506. 10.1042/Bj20081948.
147. Stroka K., Jiang H., Chen S.-H., Tong Z., Wirtz D., Sun S., et al. Water permeation drives tumor cell migration in confined microenvironments. Cell 2014, 157(3):611-623. 10.1016/j.cell.2014.02.052.
148. Stupack D.G., Puente X.S., Boutsaboualoy S., Storgard C.M., Cheresh D.A. Apoptosis of adherent cells by recruitment of caspase-8 to unligated integrins. Journal of Cell Biology 2001, 155(3):459-470. 10.1083/Jcb.200106070.
149. Subramanian A., Wayburn B., Bunch T., Volk T. Thrombospondin-mediated adhesion is essential for the formation of the myotendinous junction in Drosophila. Development 2007, 134(7):1269-1278. 10.1242/Dev.000406.
150. Suga H., Chen Z.H., de Mendoza A., Sebe-Pedros A., Brown M.W., Kramer E., et al. The Capsaspora genome reveals a complex unicellular prehistory of animals. Nature Communications 2013, 4:2325. 10.1038/Ncomms3325.
151. Swift J., Discher D.E. The nuclear lamina is mechano-responsive to ECM elasticity in mature tissue. Journal of Cell Science 2014, 127(14):3005-3015. 10.1242/Jcs.149203.
152. Swift J., Ivanovska I.L., Buxboim A., Harada T., Dingal P.C.D.P., Pinter J., et al. Nuclear lamin-A scales with tissue stiffness and enhances matrix-directed differentiation. Science 2013, 341(6149):1240104. 10.1126/Science.1240104.
153. Taddei I., Deugnier M.A., Faraldo M.M., Petit V., Bouvard D., Medina D., et al. beta 1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nature Cell Biology 2008, 10(6):716-722. 10.1038/Ncb1734.
154. Tanentzapf G., Devenport D., Godt D., Brown N.H. Integrin-dependent anchoring of a stem-cell niche. Nature Cell Biology 2007, 9(12):1413-1418. 10.1038/Ncb1660.
155. Tang Y., Rowe R.G., Botvinick E.L., Kurup A., Putnam A.J., Seiki M., et al. MT1-MMP-dependent control of skeletal stem cell commitment via a beta 1-integrin/YAP/TAZ signaling axis. Developmental Cell 2013, 25(4):402-416. 10.1016/J.Devcel.2013.04.011.
156. Tavazoie M., Van der Veken L., Silva-Vargas V., Louissaint M., Colonna L., Zaidi B., et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008, 3(3):279-288. 10.1016/J.Stem.2008.07.025.
157. Testaz S., Duband J.L. Central role of the alpha 4 beta 1 integrin in the coordination of avian truncal neural crest cell adhesion, migration, and survival. Developmental Dynamics 2001, 222(2):127-140. 10.1002/Dvdy.1181.
158. Theveneau E., Steventon B., Scarpa E., Garcia S., Trepat X., Streit A., et al. Chase-and-run between adjacent cell populations promotes directional collective migration. Nature Cell Biology 2013, 15(7):763-772. 10.1038/Ncb2772.
159. Tian A.G., Jiang J. Intestinal epithelium-derived BMP controls stem cell self-renewal in Drosophila adult midgut. Elife 2014, 3:e01857. 10.7554/eLife.01857.
160. Trappmann B., Gautrot J.E., Connelly J.T., Strange D.G.T., Li Y., Oyen M.L., et al. Extracellular-matrix tethering regulates stem-cell fate. Nature Materials 2012, 11(8):742. (vol. 11, p. 642, 2012). 10.1038/Nmat3387.
161. Tucker R.P. Antisense knockdown of the ≤1 integrin subunit in the chicken embryo results in abnormal neural crest cell development. The International Journal of Biochemistry & Cell Biology 2004, 36(6):1135-1139. doi:10.1016/j.biocel.2004.01.010.
162. Urbano J.M., Dominguez-Gimenez P., Estrada B., Martin-Bermudo M.D. PS integrins and laminins: Key regulators of cell migration during Drosophila embryogenesis. Plos One 2011, 6(9):e23893. 10.1371/journal.pone.0023893.
163. Vied C., Reilein A., Field N.S., Kalderon D. Regulation of stem cells by intersecting gradients of long-range niche signals. Developmental Cell 2012, 23(4):836-848. 10.1016/J.Devcel.2012.09.010.
164. Viveiros R., Hutter H., Moerman D.G. Membrane extensions are associated with proper anterior migration of muscle cells during Caenorhabditis elegans embryogenesis. Developmental Biology 2011, 358(1):189-200. 10.1016/J.Ydbio.2011.07.026.
165. Wang X.M., Harris R.E., Bayston L.J., Ashe H.L. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008, 455(7209):72-77. 10.1038/Nature07214.
166. Watt F.M., Huck W.T.S. Role of the extracellular matrix in regulating stem cell fate. Nature Reviews Molecular Cell Biology 2013, 14(8):467-473. 10.1038/Nrm3620.
167. Weber G.F., Bjerke M.A., DeSimone D.W. Integrins and cadherins join forces to form adhesive networks. Journal of Cell Science 2011, 124(8):1183-1193. 10.1242/Jcs.064618.
168. Wickstrom S.A., Radovanac K., Fassler R. Genetic analyses of integrin signaling. Cold Spring Harbor Perspectives in Biology 2011, 3:a005116. 10.1101/cshperspect.a005116.
169. Wieschaus E. From molecular patterns to morphogenesis-The lessons from studies on the fruit fly Drosophila (nobel lecture). Angewandte Chemie, International Edition in English 1996, 35(19):2188-2194. 10.1002/anie.199621881.
170. Williams B.D., Waterston R.H. Genes critical for muscle development and function in Caenorhabditis-elegans identified through lethal mutations. Journal of Cell Biology 1994, 124(4):475-490. 10.1083/Jcb.124.4.475.
171. Wright T.R.F. The phenogenetics of the embryonic mutant, lethal myospheroid, in Drosophila melanogaster. Journal of Experimental Zoology 1960, 143(1):77-99. 10.1002/Jez.1401430107.
172. Yang J.T., Bader B.L., Kreidberg J.A., Ullmann-Cullere M., Trevithick J.E., Hynes R.O. Overlapping and independent functions of fibronectin receptor integrins in early mesodermal development. Developmental Biology 1999, 215(2):264-277. 10.1006/Dbio.1999.9451.
173. Yuan L., Fairchild M.J., Perkins A.D., Tanentzapf G. Analysis of integrin turnover in fly myotendinous junctions. Journal of Cell Science 2010, 123(6):939-946. 10.1242/Jcs.063040.
174. Zaidel-Bar R., Itzkovitz S., Ma'ayan A., Iyengar R., Geiger B. Functional atlas of the integrin adhesome. Nature Cell Biology 2007, 9(8):858-868. 10.1038/Ncb0807-858.
175. Zamir E.A., Rongish B.J., Little C.D. The ECM moves during primitive streak formation-computation of ECM versus cellular motion. Plos Biology 2008, 6(10):2163-2171. 10.1371/journal.pbio.0060247.
176. Zervas C.G., Gregory S.L., Brown N.H. Drosophila integrin-linked kinase is required at sites of integrin adhesion to link the cytoskeleton to the plasma membrane. Journal of Cell Biology 2001, 152(5):1007-1018. 10.1083/Jcb.152.5.1007.
177. Zhang X., Jiang G., Cai Y., Monkley S.J., Critchley D.R., Sheetz M.P. Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nature Cell Biology 2008, 10(9):1062-1068. 10.1038/Ncb1765.