Differential neural crest cell attachment and migration on avian laminin isoforms

International Journal of Developmental Neuroscience

Volumn 14, Issue 3, 1996, Pages 297-314

  Perris, Roberto ^a   Brandenberger, Ralph ^b   Chiquet, Matthias ^c  

^a Reference Center for Oncology   (Italy)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

Cell attachment; Cell migration; Integrins; Laminin isoforms; Neural crest

Indexed keywords

INTEGRIN; LAMININ; LAMININ RECEPTOR;

ANIMAL CELL; ARTICLE; AVIAN STOMACH; BINDING SITE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; GEL FILTRATION; HEART MUSCLE CELL; IMMUNOAFFINITY CHROMATOGRAPHY; NEURAL CREST CELL; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN STRUCTURE;

ANIMALIA; AVES; MAMMALIA;

EID: 0030175870     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/0736-5748(96)00015-9     Document Type: Article

References (80)

1. Anton E.S., Sandrock A. Jr., Matthew W.D. Merosin promotes neurite growth and Schwann cell migration in vitro and nerve regeneration in vivo: evidence using an antibody to merosin, ARM-1. Devl Biol. 164:1994;133-146.
2. Aumailley M., Timpl R., Sonnenberg A. Antibody to integrin α6 subunit specifically inhibits cell-binding to laminin fragment 8. Expl Cell Res. 188:1990;55-60.
3. Bayne K.E., Anderson M.J., Fambrough D.M. Extracellular matrix organization in developing muscle: correlation with acetylcholine receptor aggregates. J. Cell Biol. 99:1984;1486-1501.
4. Bilozur M.E., Hay E.B. Neural crest cell migration in 3D extracellular matrix utilizes laminin, fibronectin, or collagen. Devl Biol. 125:1988;19-33.
5. Brandenberger R., Chiquet M. Distinct heparin-binding and neurite-promoting properties of laminin isoforms isolated from chick heart. J. Cell Sci. 108:1995;3099-3108.
6. Bronner-Fraser M. Alteration in neural crest migration by an antibody that affects cell adhesion. J. Cell Biol. 100:1985;327-332.
7. Bronner-Fraser M. Perturbation of cranial neural crest migration by the HNK-1 antibody. Devl Biol. 123:1987;321-331.
8. Bronner-Fraser M., Lallier T. A monoclonal antibody against a laminin-heparan sulfate proteoglycan complex perturbs cranial neural crest migration in vivo. J. Cell Biol. 106:1988;1321-1329.
9. Brown J.C., Spragg J.H., Wheeler G.N., Taylor P.W. Identification of the B1 and B2 subunits of human placental laminin and rat parietal-yolk-sac laminin using antisera specific for murine laminin-β-galactosidase fusion proteins. Biochem. J. 270:1990;463-468.
10. Brown J.C., Goodman S.L. Different cellular receptors for human placental laminin and murine EHS laminin. FEBS Lett. 282:1991;5-8.
11. Brubacher D., Wehrle-Haller B., Chiquet M. Chick laminin: isolation by monoclonal antibodies and differential distribution of variants in the embryo. Expl Cell Res. 197:1991;290-299.
12. Bellina I., Bucciotti F., Doliana R., Zambon M., Koch M., Chiquet M., Colombatti A. and Perris R. (1996) Primary structure of the avian laminin γ1 chain and its tissue distribution in relation to known a chains. Submitted.
13. Calof A.L., Campanero M.R., O'Rear J.J., Yurchenco P.D., Lander A.D. Domain-specific activation of neuronal migration and neurite-promoting activities in laminin. Neuron. 13:1994;117-130.
14. Carter W.G., Ryan M.C., Gahr P.J. Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell. 65:1991;599-610.
15. Choi E. S.-H., Rettig W.J., Wayner E.A., Srour M.L., Clegg D.O. Functional identification of integrin laminin receptors that mediate process outgrowth by human SY5Y neuroblastoma cells. J. Neurosci. Res. 37:1994;475-488.
16. Colognato-Pyke H., O'Rear J.J., Yamada Y., Carbonetto S., Cheng Y.-S., Yurchenco P.D. Mapping of network-forming, heparin-binding, and α1β1 integrin-recognition sites within the α-chain short arm of Laminin-1. J. biol. Chem. 270:1995;9398-9406.
17. Delwel G.O., de Melker A.A., Hogervost F., Jaspars L.H., Fles D.L.A., Kuikman I., Lindblom A., Paulsson M., Timpl R., Sonnenberg A. Distinct and overlapping ligand specificities of the α3β1 and α6Aβ1 integrins: recognition of laminin isoforms. Molec. Biol. Cell. 5:1994;203-215.
18. Deutzmann R., Aumailley M., Wiedemann H., Pysny W., Timpl R., Edgar D. Cell adhesion, spreading and neurite stimulation by laminin fragment E8 depends on maintenance of secondary and tertiary structure in its rod and globular domain. Eur. J. Biochem. 191:1990;513-522.
19. Duband J.-L., Thiery J.-P. Distribution of laminin and collagen during avian neural crest development. Development. 101:1987;461-478.
20. Edgar D., Timpl R., Thoenen H. Structural requirements for the stimulation of neurite outgrowth by two variants of laminin and their inhibition by antibodies. J. Cell Biol. 106:1988;1299-1306.
21. Engvall E., Earvicker D., Haaparanta T., Ruoslahti E., Sanes J.R. Distribution and isolation of four laminin variants: tissue restricted distribution of heterodimers assembled from five different subunits. Cell Regul. 1:1991;731-740.
22. Erickson C.A., Perris R. Cell-cell and cell-matrix interaction in neural morphogenesis. Devl Biol. 159:1993;60-74.
23. Forsberg E., Ek B., Engström X., Johansson S. Purification and characterization of integrin α9β1. Expl Cell Res. 213:1994;183-190.
24. Forsberg E., Lindblom A., Paulsson M., Johansson S. Laminin isoforms promote attachment of hepatocytes via different integrins. Expl Cell Res. 215:1995;33-39.
25. Gehlsen K.R., Dickerson K., Argraves S.W., Engvall E., Ruoslahti E. Subunit structure of a laminin-binding integrin and localization of its binding site on laminin. J. biol. Chem. 264:1989;19034-19038.
26. Gehlsen K.R., Sriramarao P., Furcht L.T., Skubitz A.P.N. A synthetic peptide derived from the carboxy terminus of the laminin A chain represents a binding site for the α3β1 integrin. J. Cell Biol. 117:1992;449-459.
27. Glukhova M., Koteliansky V., Fondacci C., Marotte F., Rappaport L. Laminin variants and integrin laminin receptors in developing and adult human smooth muscle. Devl Biol. 157:1993;437-447.
28. Goodman S.L., Risse G., von der Mark K. The E8 subfragment of laminin promotes locomotion of myoblasts over extracellular matrix. J. Cell Biol. 109:1989;799-809.
29. Goodman S.L., Aumailley M., von der Mark H. Multiple cell surface receptors for the short arms of laminin: α1β1 integrin and RGD-dependent proteins mediate cell attachment only to domains III in murine tumor laminin. J. Cell Biol. 113:1991;931-941.
30. Hall D.E., Reichardt L.F., Crowley E., Holle B., Moezzi H., Sonnenberg A., Damsky C. The α1β1 and α6β1 integrin heterodimers mediate cell attachment to distinct sites on laminin. J. Cell Biol. 110:1990;2175-2184.
31. Hunter D.D., Shah V., Merlie J.P., Sanes J.R. A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction. Nature. 338:1989;229-234.
32. Hunter I., Schulthess T., Engel J. Laminin chain assembly by triple and double stranded coiled-coil structures. J. biol. Chem. 267:1992;6006-6011.
33. Hunter I., Schulthess T., Bruch M., Beck K., Engel J. Evidence for a specific mechanism of laminin assembly. Eur. J. Biochem. 188:1990;205-211.
34. Iivanainen A., Saino K., Sariola H., Tryggvason K. Primary structure and expression of a novel human laminin α4 chain. FEBS Lett. 365:1995;183-188.
35. Kelly T., Molony L., Burridge K. Purification of two smooth muscle proteins related to integrin. J. biol. Chem. 262:1987;17189-17199.
36. Kern A., Briesewitz R., Bank I., Marcantonio E. The role of the I domain in ligand binding of the human integrin α1β1. J. biol. Chem. 269:1994;22811-22816.
37. Koch M., Bernasconi C., Chiquet M. A major oligomeric fibroblast proteoglycan identified as a novel large form of type XII collagen. Eur. J. Biochem. 287:1992;847-856.
38. Kramer R.H., Vu M. P., Cheng Y.-F., Ramos D.M., Timpl R., Waleh N. Laminin-binding integrin α7β1: functional characterization and expression in normal and malignant melanocytes. Cell Regul. 2:1991;805-817.
39. Krotoski D.M., Domingo C., Bronner-Fraser M. Distribution of a putative cell surface receptor for fibronectin and laminin in the avian embryo. J. Cell Biol. 103:1986;1061-1071.
40. Bronner-Fraser M., Lallier T. A monoclonal antibody against a laminin-heparan sulfate proteoglycan perturbs cranial neural crest migration in vivo. J. Cell Biol. 106:1988;1321-1329.
41. Lallier T., Bronner-Fraser M. Avian neural crest cell attachment to laminin: involvement of divalent cation dependent and independent integrins. Development. 113:1991;1069-1084.
42. 2+-independent manner. J. Cell Biol. 119:1992;1335-1345.
43. Lallier T., Bronner-Fraser M. Substrate specific inhibition of neural crest cell attachment by integrin antisense oligonucleotides. Science. 259:1993;692-695.
44. Lallier T., Artinger M., Matthew W., Bronner-Fraser M. Distribution and biochemical characterization of the INO antigen during neural crest cell migration. Neurosci. Res. 13:1990;126-140.
45. Lallier T., Leblanc G., Bronner-Fraser M. Cranial and trunk neural crest cells use different mechanisms for attachment to extracellular matrices. Development. 116:1992;531-541.
46. Lallier T., Deutzmann R., Perris R., Bronner-Fraser M. Neural crest cell interactions with laminin: structural requirements and localization of the α1β1 binding site. Devl Biol. 162:1994;451-464.
47. Lessitzky J.C., Cantau P., Martin P.M. Heterotrimeric configuration is essential to the adhesive function of laminin. J. Cell Biochem. 48:1992;141-149.
48. Lindblom A., Marsh T., Fauser C., Engel J., Paulsson M. Characterization of native laminin from bovine kidney and comparison with other laminin variants. Eur. J. Biochem. 219:1994;383-392.
49. Marinkovich M.P., Lunstrum G.P., Keene D. R., Burgeson R.E. The dermal-epidermal junction of human skin contains a novel laminin variant. J. Cell Biol. 119:1992;695-703.
50. Martins-Green M., Erickson C.A. Basal lamina is not a barrier to neural crest migration: documentation by TEM and by immunofluorescent and immunogold labeling. Development. 103:1987;683-706.
51. Newgreen D.F. Spreading of explants of embryonic chick mesenchyme and epithelia on fibronectin and laminin. Connect. Tiss. Res. 236:1984;265-277.
52. Noakes P.G., Gautam M., Mudd J., Sanes J.R., Merlie J.P. Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/β2 laminin. Nature. 374:1995;258-262.
53. Paulsson M., Aumailley M., Deutzmann R., Timpl R., Beck K., Engel J. Laminin-nidogen complex extraction with chelating agents and structural characterization. Eur. J. Biochem. 166:1987;11-19.
54. Paulsson M., Saladin K. Mouse heart laminin: purification of the native protein and structural comparison with EHS tumor laminin. J. biol. Chem. 264:1989;18726-18732.
55. Paulsson M., Saladin K., Engvall E. Structure of laminin variants. The 300-kDa chains of murine and bovine heart laminin are related to the human placenta merosin heavy chain and replace the A chain in some laminin variants. J. biol. Chem. 266:1991;17545-17551.
56. Perris R., Johansson S. Amphibian neural crest cell migration on purified extracellular matrix components. A chondroitin sulfate proteoglycan inhibits locomotion on fibronectin substrates. J. Cell Biol. 105:1987;2511-2521.
57. Perris R., Paulsson M., Bronner-Fraser M. Molecular mechanisms of neural crest cell migration on fibronectin and laminin. Devl Biol. 136:1989;222-238.
58. Perris R., Kuo H.-J., Glanville R.W., Leibold S., Bronner-Fraser M. Neural crest cell interaction with type VI collagen is mediated by multiple cooperative binding sites within triple-helix and globular domains. Expl Cell Res. 209:1993;103-117.
59. Pfaff M., Göhring W., Brown J.C., Timpl R. Binding of purified collagen receptors (α1β1, α2β1) and RGD-dependent integrins to laminin and laminin fragment. Eur. J. Biochem. 225:1994;975-984.
60. Porter B.E., Weis J., Sanes J.R. A motorneuron selective stop signal in the synaptic protein s-laminin. Neuron. 14:1995;549-559.
61. Pöschl E., Fox J.W., Block D., Mayer U., Timpl R. Two non-contiguous regions contribute to nidogen binding to a single EGF-like motif of the γ1 chain. EMBO J. 13:1994;3741-3747.
62. Richards A.J., Al-Imara L., Carter N.P., Lloyd J.C., Leversha M., Pope F.M. Localization of the gene (LAMA4) to chromosome 6q21 and isolation of a partial cDNA encoding for a variant laminin A chain. Genomics. 22:1994;237-239.
63. Rogers S.L., Edson K.J., Letourneau P.C., McLoon S.C. Distribution of laminin in the developing peripheral nervous system of the chick. Devl Biol. 113:1986;429-435.
64. Schulze B., Mann K., Pöschl E., Yamada Y., Timpl R. Structural and functional analysis of the globular domains IVa of the laminin α1 chain and its impact on an adjacent RGD site. Biochem. J. 314:1996;847-851.
65. Rousselle P., Aumailley M. Kalinin is more efficient than laminin in promoting adhesion of primary keratinocytes and some other epithelial cells and has a different requirement for integrin receptors. J. Cell Biol. 125:1995;205-214.
66. Rovasio R., Delouvee A., Timpl R., Yamada K., Thiery J.P. Neural crest cell adhesion and migration: requirements for exogenous fibronectin and high cell density. J. Cell Biol. 96:1983;462-473.
67. Schittny J.C., Yurchenco P.D. Terminal short arm domains of basement membrane laminin are critical for its self-assembly. J. Cell Biol. 110:1990;825-832.
68. Sorokin L., Girg W., Göpfert Hallmann R., Deutzmann R. Expression of novel 400-kDa laminin chains by mouse and bovine endothelial cells. Eur. J. Biochem. 223:1994;603-609.
69. Sung U., O'Rear J.J., Yurchenco P.D. Cell and heparin binding in the distal long arma of laminin: identification of active and cryptic sites with recombinant and hybrid glycoprotein. J. Cell Biol. 123:1983;1255-1268.
70. Syfrig J., Mann K., Paulsson M. An abundant chick gizzard integrin is the avian α1β1 integrin heterodimer and functions as a divalent cation-dependent collagen IV receptor. Expl Cell Res. 194:1991;165-173.
71. Tawil N.J., Houde M., Blacher R., Esch F., Reichardt L.F., Turner D.C., Carbonetto S. α1β1 integrin heterodimer functions as a dual laminin/collagen receptor in neural cells. Biochemistry. 29:1990;6540-6544.
72. Tomaselli K.J., Hall D.E., Flier L.A., Gehlsen K.R., Turner D.C., Carbonetto S., Reichardt L.F. A neural cell line (PC12) expresses two β1-class integrins, α1β1 and α3β1, that recognize different neurite outgrowth promoting domains of laminin. Neuron. 5:1990;651-662.
73. Tomaselli K.J., Doherty P., Emmett C.J., Damsky C.H., Walsh F.S., Reichardt L.F. Expression of β1 integrins in sensory neurons of the dorsal root ganglion and their function in neurite outgrowth on two laminan isoforms. J. Neurosci. 13:1993;4880-4888.
74. Verrando P., Lissitzky J.-C., Sarret Y., Winberg J.O., Gedde-Dahl T. Jr., Schmitt D., Bruckner-Tuderman L. Keratinocytes from junctional epidermolysis bullosa do adhere and migrate on the basement membrane protein nicein through α3β1 integrin. Lab. Invest. 71:1994;567-574.
75. von der Mark H., Durr J., Sonnenberg A., von der Mark K., Deutzmann R., Goodman S.L. Skeletal myoblasts utilize a novel β1-series integrin and not α6β1 for binding to the E8 and T8 fragments of laminin. J. Cell Biol. 266:1991;23593-23601.
76. Vuolteenaho R., Nissinen M., Saino K., Byers M., Eddy R., Hirvonen H., Shows T.B., Sariola H., Engvall E., Tryggvason K. Human laminin-M chain (merosin) - Complete primary structure, chromosomal assignment, and expression of M-chain and A-chain in human fetal tissues. J. Cell Biol. 124:1994;381-394.
77. Wayner E.A., Gil S.G., Murphy G.F., Wilke M.S., Carter W.G. Epiligrin, a component of epithelial basement membranes, is an adhesive ligand for α3β1 positive T lymphocytes. J. Cell Biol. 121:1993;1141-1152.
78. Yin Z., Lindblom A., Deutzmann R., Messina D., Paulsson M., Colombatti A. and Perris R. (1996) A novel laminin isoform from kidney is a potent adhesive substrate for neoplastic hematopoietic cells (in preparation).
79. Yip J.W., Yip Y.P.L. Laminin developmental expression and role in axonal outgrowth in the peripheral nervous system of the chick. Devl Brain Res. 68:1992;23-33.
80. Yurchenco P.D. Laminin forms an independent network in basement membranes. J. Cell Biol. 117:1992;1119-1133.