Integrin α6β1-laminin interactions regulate early myotome formation in the mouse embryo

Development

Volumn 133, Issue 9, 2006, Pages 1635-1644

  Bajanca, Fernanda ^a,b   Luz, Marta ^a,b,e   Raymond, Karine ^c   Martins, Gabriel G ^a,b   Sonnenberg, Arnoud ^c   Tajbakhsh, Shahragim ^d   Buckingham, Margaret ^d   Thorsteinsdóttir, Sólveig ^a,b  

^a UNIVERSITY OF LISBON   (Portugal)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c NETHERLANDS CANCER INSTITUTE   (Netherlands)

^d INSTITUT PASTEUR   (France)

^e MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Dermomyotome; Extracellular matrix; Integrin; Laminin; Mouse embryo; Myf5; Myotome

Indexed keywords

COLLAGEN TYPE 4; LAMININ; MYOGENIC FACTOR 5; MYOGENIN; PERLECAN; VERY LATE ACTIVATION ANTIGEN 6; MYF5 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; EMBRYO CULTURE; EXTRACELLULAR MATRIX; IMMUNOHISTOCHEMISTRY; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; COMPARATIVE STUDY; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; PRENATAL DEVELOPMENT; SKELETAL MUSCLE;

ANIMALIA;

ANIMALS; CELLS, CULTURED; EMBRYO; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; INTEGRIN ALPHA6BETA1; LAMININ; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUSCLE DEVELOPMENT; MUSCLE, SKELETAL; MYOGENIC REGULATORY FACTOR 5; MYOGENIN; ORGAN CULTURE TECHNIQUES;

EID: 33744526802     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02336     Document Type: Article

References (75)

1. Bajanca, F. and Thorsteinsdóttir, S. (2002). Integrin expression patterns during early limb muscle development in the mouse. Mech. Dev. 119, S131-S134.
2. Bajanca, F, Luz, M., Duxson, M. J. and Thorsteinsdóttir, S. (2004). Integrins in the mouse myotome: Developmental changes and differences between the epaxial and hypaxial lineage. Dev. Dyn. 231, 402-415.
3. Ben-Yair, R. and Kalcheim, C. (2005). Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and muscle progenitor fates. Development 132, 689-701.
4. Blaess, S., Graus-Porta, D., Belvindrah, R., Radakovits, R., Pons, S., Littlewood-Evans, A., Senften, M., Guo, H., Li, Y., Miner, J. H. et al. (2004). β1-integrins are critical for cerebellar granule cell precursor proliferation. J. Neurosci. 24,3402-3412.
5. Buckingham, M., Houzelstein, D., Lyons, G., Ontell, M., Ott, M. O. and Sassoon, D. (1992). Expression of muscle genes in the mouse embryo. Symp. Soc. Exp. Biol. 46, 203-217.
6. Burrows, T. D., King, A., Smith, S. K. and Loke, Y. W. (1995). Human trophoblast adhesion to matrix proteins: inhibition and signal transduction. Hum. Reprod. 10, 2489-2500.
7. Cachaĉo, A. S., Chuva de Sousa Lopes, S. M., Kuikman, I., Bajanca, F., Abe, K., Baudoin, C., Sonnenberg, A., Mummery, C. L. and Thorsteinsdóttir, S. (2003). Knock-in of integrin β1D affects primary but not secondary myogenesis in mice. Development 130, 1659-1671.
8. Cachaĉo, A. S., Pereira, C. S., Pardal, R. G., Bajanca, F. and Thorsteinsdóttir, S. (2005). Integrin repertoire on myogenic cells changes during the course of primary myogenesis in the mouse. Dev. Dyn. 232, 1069-1078.
9. Cheng, Y. S., Champliaud, M. F., Burgeson, R. E., Marinkovich, M. P. and Yurchenco, P. D. (1997). Self-assembly of laminin isoforms. J. Biol. Chem. 272, 31525-31532.
10. Colognato, H., Winkelmann, D. A. and Yurchenco, P. D. (1999). Laminin polymerization induces a receptor-cytoskeleton network. J. Cell Biol. 145, 619-631.
11. Colognato, H., Baron, W., Avellana-Adalid, V., Relvas, J. B., Baron-Van Evercooren, A., Georges-Labouesse, E. and ffrench-Constant, C. (2002). CNS integrins switch growth factor signalling to promote target-dependent survival. Nat. Cell Biol. 4, 833-841.
12. Cossu, G. and Borello, U. (1999). Wnt signaling and the activation of myogenesis in mammals. EMBO J. 18, 6867-6872.
13. Cossu, G., Tajbakhsh, S. and Buckingham, M. (1996). How is myogenesis initiated in the embryo? Trends Genet. 12, 218-223.
14. Currie, P. D. and Ingham, P. W. (1998). The generation and interpretation of positional information within the vertebrate myotome. Mech. Dev. 73, 3-21.
15. Darien, E. H. and Sonnenberg, A. (2003). Integrins in regulation of tissue development and function. J. Pathol. 201, 632-641.
16. De Arcangelis, A., Mark, M., Kreidberg, J., Sorokin, L. and Georges-Labouesse, E. (1999). Synergistic activities of α3 and α6 integrins are required during apical ectodermal ridge formation and organogenesis in the mouse. Development 126, 3957-3968.
17. de Curtis, I. and Reichardt, L. F. (1993). Function and spatial distribution in developing chick retina of the laminin receptor α6β1 and its isoforms. Development 118, 377-388.
18. Denetclaw, W. F, Jr, Christ, B. and Ordahl, C. P. (1997). Location and growth of epaxial myotome precursor cells. Development 124, 1601-1610.
19. DiPersio, C. M., Hodivala-Dilke, K. M., Jaenisch, R., Kreidberg, J. A. and Hynes, R. 0. (1997). α3β1 Integrin is required for normal development of the epidermal basement membrane. J. Cell Biol. 137, 729-742.
20. Ekblom, P., Lonai, P. and Talts, J. F. (2003). Expression and biological role of laminin-1. Matrix Biol. 22, 35-47.
21. Falk, M., Salmivirta, K., Durbeej, M., Larsson, E., Ekblom, M., Vestweber, D. and Ekblom, P. (1996). Integrin α6Bβ1 is involved in kidney tubulogenesis in vitro. J. Cell Sci. 109, 2801-2810.
22. Ferletta, M., Kikkawa, Y., Yu, H., Talts, J. F, Durbeej, M., Sonnenberg, A., Timpl, R., Campbell, K. P., Ekblom, P. and Genersch, E. (2003). Opposing roles of integrin α6β1 and clystroglycan in laminin-mediated extracellular signal-regulated kinase activation. Mol. Biol. Cell 14, 2088-2103.
23. Fleischmajer, R., Utani, A., MacDonald, E. D., Perlish, J. S., Pan, T C., Chu, M.L., Nomizu, M., Ninomiya, Y. and Yamada, Y. (1998). Initiation of skin basement membrane formation at the epidermo-dermal interface involves assembly of laminins through binding to cell membrane receptors. J. Cell Sci. 111, 1929-1940.
24. Georges-Labouesse, E., Mark, M., Messaddeq, N. and Gansmüller, A. (1998). Essential role of α6 integrins in cortical and retinal lamination. Curr. Biol. 8, 983-986.
25. George-Weinstein, M., Gerhart, J., Reed, R., Flynn, J., Callihan, B., Mattiacci, M., Miehle, C., Foti, G., Lash, J. W. and Weintraub, H. (1996). Skeletal myogenesis: the preferred pathway of chick embryo epiblast cells in vitro. Dev Biol. 173, 279-291.
26. Ghosh, S. and Stack, M. S. (2000). Proteolytic modification of laminins: functional consequences. Microsc. Res. Tech. 51, 238-246.
27. Gros, J., Scaal, M. and Marcelle, C. (2004). A two-step mechanism for myotome formation in chick. Dev. Cell 6, 875-882.
28. Gros, J., Manceau, M, Thome, V. and Marcelle, C. (2005). A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435, 954-958.
29. Gullberg, D., Veiling, T., Lohikangas, L. and Tiger, C. R (1998). Integrins during muscle development and in muscular dystrophies. Front. Biosci. 3, D1039-D1050.
30. Henry, M. D., Satz, J. S., Brakebusch, C., Costell, M., Gustafsson, E., Fässler, R. and Campbell, K. P. (2001). Distinct roles for dystroglycan, β1 integrin and perlecan in cell surface laminin organization. J. Cell Sci. 114, 1137-1144.
31. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1986). Manipulating the Mouse Embryo. A Laboratory Manual. 332 pp. New York: Cold Spring Harbor Laboratory Press.
32. Hogervorst, F., Kuikman, I., van Kessel, A. G. and Sonnenberg, A. (1991). Molecular cloning of the human α6 integrin subunit. Alternative splicing of α6 mRNA and chromosomal localization of the α6 and β4 genes. Eur J. Biochem. 199, 425-433.
33. Houzelstein, D., Auda-Boucher, G., Chéraud, Y., Rouaud, T., Blanc, I., Tajbakhsh, S., Buckingham, M., Fontaine-Pérus, J. and Robet, B. (1999). The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimbs. Development 126, 2689-2701.
34. Hynes, R. O. (1992). Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.
35. Hynes, R. O. (1996). Targeted mutations in cell adhesion genes: what have we learned from them? Dev. Biol. 180, 402-412.
36. Jiang, F. X., Georges-Labouesse, E. and Harrison, L. C. (2001). Regulation of laminin 1-induced pancreatic β-cell differentiation by α6 integrin and α1-dystroglycan. Mol. Med. 7, 107-114.
37. Kahane, N., Cinnamon, Y. and Kalcheim, C. (1998). The cellular mechanism by which the dermomyotome contributes to the second wave of myotome development. Development 125, 4259-4271.
38. Kassar-Duchossoy, L., Gayraud-Morel, B., Gomes, D., Rocancourt, D., Buckingham, M., Shinin, V. and Tajbakhsh, S. (2004). Mrf4 determines skeletal muscle identity in Myf5:MyoD double-mutant mice. Nature 431, 466-471.
39. Kassar-Duchossoy, L., Giacone, E., Gayraud-Morel, B., Jory, A., Gomes, D. and Tajbakhsh, S. (2005). Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev. 19, 1426-1431.
40. Kill, S. H., Krull, C. E., Cann, G., Clegg, D. and Bronner-Fraser, M. (1998). The α subunit of integrin is important for neural crest cell migration. Dev Biol. 202, 29-42.
41. Kreidberg, J. A., Donovan, M. J., Goldstein, S. L., Rennke, H., Shepherd, K., Jones, R. C. and Jaenisch, R. (1996). Alpha 3 beta 1 integrin has a crucial role in kidney and lung organogenesis. Development 122, 3537-3547.
42. Li, S., Harrison, D., Carbonetto, S., Fässler, R., Smyth, N., Edgar, D. and Yurchenco, R D. (2002). Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157, 1279-1290.
43. Miner, J. H., Patton, B. L., Lentz, S. I., Gilbert, D. J., Snider, W. D., Jenkins, N. A., Copeland, N. G. and Sanes, J. R. (1997). The laminin α chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J. Cell Biol. 137, 685-701.
44. Miranti, C. K. and Brugge, J. S. (2002). Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4, E83-E90.
45. Ott, M. O., Bober, E., Lyons, G., Arnold, H. and Buckingham, M. (1991). Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097-1107.
46. Paulsson, M. (1994). Biosynthesis, tissue distribution and isolation of laminins. in The Laminins (ed. P. Ekblom and R. Timpl), pp. 1-26. Amsterdam: Harwood Academic Publishers.
47. Pons, S., Trejo, J. L., Martinez-Morales, J. R. and Marti, E. (2001). Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128,1481-1492.
48. Pownall, M. E., Gustafsson, M. K. and Emerson, C. P., Jr (2002). Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 18, 747-783.
49. Relaix, F., Rocancourt, D., Mansouri, A. and Buckingham, M. (2005). A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435, 948-953.
50. Sasaki, T., Forsberg, E., Bloch, W., Addicks, K., Fässler, R. and Timpl, R. (1998). Deficiency of β1 integrins in teratoma interferes with basement membrane assembly and laminin-1 expression. Exp. Cell Res. 238, 70-81.
51. Sastry, S. K., Lakonishok, M., Thomas, D. A., Muschler, J. and Horwitz, A. F (1996). Integrin α subunit ratios, cytoplasmic domains, and growth factor synergy regulate muscle proliferation and differentiation. J. Cell Biol. 133, 169-184.
52. Schwander, M., Leu, M., Stumm, M., Dorchies, O. M., Ruegg, U. T, Schittny, J. and Müller, U. (2003). β1 integrins regulate myoblast fusion and sarcomere assembly. Dev. Cell 4, 673-685.
53. Sonnenberg, A., Daams, H., van der Valk, M. A., Hilkens, J. and Hilgers, J. (1986). Development of mouse mammary gland: identification of stages in differentiation of luminal and myoepithelial cells using monoclonal antibodies and polyvalent antiserum against keratin. J. Histochem. Cytochem. 34, 1037-1046.
54. Sonnenberg, A., Janssen, H., Hogervorst, F., Calafat, J. and Hilgers, J. (1987). A complex of platelet glycoproteins Ic and IIa identified by a rat monoclonal antibody. J. Biol. Chem. 262, 10376-10383.
55. Sonnenberg, A., Janssen, H., Hogervorst, F., Calafat, J. and Hilgers, J. (1988). Laminin receptor on platelets is the integrin VLA-6. Nature 336, 487-489.
56. Sonnenberg, A., Linders, C. J., Modderman, P. W., Damsky, C. H., Aumailley, M. and Timpl, R. (1990). Integrin recognition of different cell-binding fragments of laminin (P1, E3, E8) and evidence that α6β1 but not α6β4 functions as a major receptor for fragment E8. J. Cell Biol. 110, 2145-2155.
57. Stephens, L. E., Sutherland, A. E., Klimanskaya, I. V., Andrieux, A., Meneses, J., Pedersen, R. A. and Damsky, C. H. (1995). Deletion of β1 integrins in mice results in inner cell mass failure and peri-implantation lethality Genes Dev. 9, 1883-1895.
58. Tajbakhsh, S. and Buckingham, M. (2000). The birth of muscle progenitor cells in the mouse: spatiotemporal considerations. In Somitogrenesis, Current Topics in Developmental Biology, Vol. 47 (ed. C. P. Ordahl), pp. 225-268. London: Academic Press.
59. Tajbakhsh, S., Rocancourt, D. and Buckingham, M. (1996). Muscle progenitor cells failing to respond to positional cues adopt non-myogenic fates in myf-5 null mice. Nature 384, 266-270.
60. Tajbakhsh, S., Rocancourt, D., Cossu, G. and Buckingham, M. (1997). Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89, 127-138.
61. Tamura, R. N., Cooper, H. M., Collo, G. and Quaranta, V. (1991). Cell type-specific integrin variants with alternative a chain cytoplasmic domains. Proc Natl. Acad. Sci. USA 88, 10183-10187.
62. Thorsteinsdóttir, S., Roelen, B. A., Freund, E., Gaspar, A. C., Sonnenberg, A. and Mummery, C. L. (1995). Expression patterns of laminin receptor splice variants α6β1 and α6Bβ1 suggest different roles in mouse development. Dev. Dyn. 204, 240-258.
63. Tosney, K. W., Dehnbostel, D. B. and Erickson, C. A. (1994). Neural crest cells prefer the myotome's basal lamina over the sclerotome as a substratum. Dev Biol. 163, 389-406.
64. Tunggal, P., Smyth, N., Paulsson, M. and Ott, M. C. (2000). Laminins: structure and genetic regulation. Microsc. Res. Tech. 51, 214-227.
65. van der Flier, A. and Sonnenberg, A. (2001). Function and interactions of integrins. Cell Tissue Res. 305, 285-298.
66. van der Flier, A., Gaspar, A. C., Thorsteinsdóttir, S., Baudoin, C., Groeneveld, E., Mummery, C. L. and Sonnenberg, A. (1997). Spatial and temporal expression of the β1D integrin during mouse development. Dev. Dyn. 210, 472-486.
67. Venters, S. J., Thorsteinsdóttir, S. and Duxson, M. J. (1999). Early development of the myotome in the mouse. Dev. Dyn. 216, 219-232.
68. Walker, J. L. and Menko, A. S. (1999). α6 Integrin is regulated with lens cell differentiation by linkage to the cytoskeleton and isoform switching. Dev. Biol. 210, 497-511.
69. Walker, J. L., Zhang, L. and Menko, A. S. (2002). A signaling role for the uncleaved form of α6 integrin in differentiating lens fiber cells. Dev. Biol. 251, 195-205.
70. Webb, D. J., Asmussen, H., Murase, S. and Horwitz, A. F. (2002). Cell migration in slice cultures. In Methods in Cell-Matrix Adhesion, Methods in Cell Biology, Vol. 69 (ed. J. C. Adams), pp. 341-358. San Diego: Academic Press.
71. Wei, J., Shaw, L. M. and Mercurio, A. M. (1998). Regulation of mitogen-activated protein kinase activation by the cytoplasmic domain of the α6 integrin subunit. J. Biol. Chem. 273, 5903-5907.
72. Yurchenco, P. D. and Cheng, Y. S. (1993). Self-assembly and calcium-binding sites in laminin. A three-arm interaction model. J. Biol. Chem. 268, 17286-17299.
73. Yurchenco, P. D. and Wadsworth, W. G. (2004). Assembly and tissue functions of early embryonic laminins and netrins. Curr. Opin. Cell Biol. 16, 572-579.
74. Yurchenco, P. D., Tsilibary, E. C., Charonis, A. S. and Furthmayr, H. (1985). Laminin polymerization in vitro. Evidence for a two-step assembly with domain specificity. J. Biol. Chem. 260, 7636-7644.
75. Yurchenco, P. D., Amenta, R S. and Patton, B. L. (2004). Basement membrane assembly, stability and activities observed through a developmental lens. Matrix Biol. 22, 521-538.