Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan

Journal of Cell Biology

Volumn 149, Issue 6, 2000, Pages 1275-1288

  Li, Hedong ^a,c   Leung, Tin Chung ^a,d   Hoffman, Stanley ^b   Balsamo, Janne ^a,e   Lilien, Jack ^a,e  

^a WAYNE STATE UNIVERSITY   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c RUTGERS UNIVERSITY   (United States)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY OF IOWA   (United States)

Author keywords

Adhesion; Cadherin; Integrin; Neurite outgrowth; Tyrosine kinase Fer

Indexed keywords

BETA1 INTEGRIN; HYALURONIC ACID; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE KINASE; PROTEOCHONDROITIN SULFATE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CHICK EMBRYO; CONTROLLED STUDY; CYTOPLASM; EMBRYO; GENE EXPRESSION REGULATION; MOLECULAR INTERACTION; MORPHOGENESIS; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RETINA BIPOLAR GANGLION CELL; RETINA NEUROEPITHELIAL LAYER; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, CD29; BRAIN; CADHERINS; CELL ADHESION; CELL DIVISION; CELLS, CULTURED; CHICK EMBRYO; CLONING, MOLECULAR; FLUORESCENT ANTIBODY TECHNIQUE; LECTINS, C-TYPE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; PROTEOCHONDROITIN SULFATES; RETINA; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

ANIMALIA;

EID: 0034640983     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.6.1275     Document Type: Article

References (92)

1. Arregui, C., J. Balsamo, and J. Lilien. 1999. Impaired integrin-mediated adhesion and signaling in fibroblasts expressing a dominant negative mutant PTP1B. J. Cell Biol. 143:861-873.
2. Arregui, C., P. Pathre, J. Lilien, and J. Balsamo. 2000. The nonreceptor tyrosine kinase Fer mediates cross-talk between N-cadherin and β1-integrin. J. Cell Biol. 149:1263-1273.
3. Balsamo, J., and J. Lilien. 1990. N-cadherin is stably associated with, and is an acceptor for, a cell surface N-acetylgalactosaminylphosphotransferase. J. Biol. Chem. 265:2923-2928.
4. Balsamo, J., and J. Lilien. 1993. The retina cell-surface N-acetylgalactosaminylphosphotransferase is anchored by a glycophosphatidylinositol. Biochemistry. 32:8246-8250.
5. Balsamo, J., S. Hoffman, and J. Lilien. 1996. Control of cadherin-mediated cell-cell adhesion through regulated association with the cytoskeleton. J. Braz. Assoc. Adv. Sci. 48:341-346.
6. Balsamo, J., R.S. Pratt, M.R. Emmerling, G. Grunwald, and J. Lilien. 1986. Identification of the chick neural retina cell surface N-acetylgalactosaminyltransferase using monoclonal antibodies. J. Cell Biochem. 32:125-141.
7. Balsamo, J., R. Thiboldeaux, N. Swaminathan, and J. Lilien. 1991. Antibodies to the retina N-acetylgalactosaminylphosphotransferase modulate N-cadherin-mediated adhesion and uncouple the N-cadherin transferase complex from the actin-containing cytoskeleton. J. Cell Biol. 113:429-436.
8. Balsamo, J., H. Ernst, M.K. Zanin, S. Hoffman, and J. Lilien. 1995. The interaction of the retina cell surface N-acetylgalactosaminylphosphotransferase with an endogenous proteoglycan ligand results in inhibition of cadherin-mediated adhesion. J. Cell Biol. 129:1391-1401.
9. Balsamo, J., T.-C. Leung, H. Ernst, M.K. Zanin, S. Hoffman, and J. Lilien. 1996. Regulated binding of a PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of β-catenin. J. Cell Biol. 134:801-813.
10. Balsamo, J., C. Arregui, T.-C. Leung, and J. Lilien. 1998. The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J. Cell Biol. 143:523-532.
11. Barnstable, C.J., R. Hofstein, and K. Akagawa. 1985. A marker for early amacrine cell developement in rat retina. Brain Res. 325:286-290.
12. Bauer, G.E., J. Balsamo, and J. Lilien. 1992. Cadherin-mediated adhesion in pancreatic islet cells is modulated by a cell surface N-acetylgalactosaminylphosphotransferase. J. Cell. Sci. 103:1235-1241.
13. Bause, E. 1983. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem. J. 209:331-336.
14. Birge, B., J. Fagardo, B. Mayer, and H. Hanafusa. 1992. Tyrosine phosphorylated epidermal growth factor receptor and p130 provide high affinity binding substrates to analyze Crk-phosphotyrosine-dependent interactions in vitro. J. Biol. Chem. 267:10588-10595.
15. Bixby, J.L., J. Lilien, and L.F. Reichardt. 1988. Identification of the major proteins that promote neuronal process outgrowth on Schwann cells in vitro. J. Cell Biol. 107:355-361.
16. Bourdon, M.A., T. Krusius, S. Campbell, N.B. Schwartz, and E. Ruoslahti. 1987. Identification and synthesis of a recognition signal for the attachment of glycosaminoglycans to proteins. Proc. Natl. Acad. Sci. USA. 84:3194-3198.
17. Buj-Bello, A., J. Adu, L.G.P. Pinon, A. Horton, J. Thompson, A. Rosenthal, M. Chinchetru, V.L. Buchman, and A.M. Davis. 1997. Neurturin responsiveness requires a GPI-linked receptor and the Ret receptor tyrosine kinase. Nature. 387:721-724.
18. Burden-Gulley, S.M., and S.M. Brady-Kalnay. 1999. PTPμ regulates N-cadherin-dependent neurite outgrowth. J. Cell Biol. 144:1323-1336.
19. Buskirk, D.R., J.P. Thiery, U. Rutishauser, and G.M. Edelman. 1980. Antibodies to neural cell adhesion molecule disrupt histogenesis in cultured chick retinae. Nature. 285:488-489.
20. Daniel, J.M., and A.B. Reynolds. 1997. Tyrosine phosphorylation and cadherin/catenin function. Bioessays. 19:883-891.
21. Derossi, D., A.H. Joliot, G. Chassaing, and A. Prochiantz. 1994. The third helix of the antennapedia homeodomain translocates through biological membranes. J. Biol. Chem. 269:10444-10450.
22. Doege, K., M. Sasaki, E. Horigan, J.R. Hassell, and Y. Yamada. 1987. Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J. Biol. Chem. 262:17757-17767.
23. Faissner, A., and D. Steindler. 1995. Boundaries and inhibitory molecules in developing neural tissues. Glia. 13:233-254.
24. Friedlander, D.R., P. Milev, L. Karthikeyan, R.K. Margolis, R.U. Margolis, and M. Grumet. 1994. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/LI/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J. Cell Biol. 125:669-680.
25. Fukuda, T., H. Kawano, K. Ohyama, H.P. Li, Y. Takeda, A. Oohira, and K. Kawamura. 1997. Immunohistochemical localization of neurocan and L1 in the formation of thalamocortical pathway of developing rats. J. Comp. Neurol. 382:141-152.
26. cas: a novel mechanism of protein tyrosine phosphatase substrate recognition. Oncogene. 15:877-885.
27. Gaya-Gonzalez, L., J. Balsamo, N. Swaminathan, and J. Lilien. 1991. Antibodies to the retina N-acetylgalactosaminylphosphotransferase inhibit neurite outgrowth. J. Neurosci. Res. 29:474-480.
28. Gleason, E., S. Borges, and M. Wilson. 1993. Synaptic transmission between pairs of retinal amacrine cells in culture. J. Neurosci. 13:2359-2370.
29. Goodman, C.S., and M. Tessier-Lavigne. 1997. Molecular mechanisms of axon guidance and target recognition. In Molecular and Cellular Approaches to Neural Development. W.M. Cowan, T.M. Jessel, and S.L. Zipursky, editors. Oxford University Press, New York, 108-178.
30. Greve, J.M., and D.I. Gottlied. 1982. Monoclonal antibodies which alter the morphology of cultured chick myogenic cells. J. Cell. Biochem. 18:221-229.
31. Grumet, M., A. Flaccus, and R.U. Margolis. 1993. Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J. Cell Biol. 120:815-824.
32. Grumet, M., D.R. Friedlander, and T. Sakurai. 1996. Functions of brain chondroitin sulfate proteoglycans during development: interactions with adhesion molecules. Perspect. Dev. Neurobiol. 3:319-330.
33. Halberg, D.F., G. Proulx, K. Doege, Y. Yamada, and K. Drickamer. 1988. A segment of the cartilage proteoglycan core protein has lectin-like activity. J. Biol. Chem. 263:9486-9490.
34. Hatta, K., and M. Takeichi. 1986. Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature. 320:447-449.
35. Hoffman, S., D.R. Friedlander, C.-M. Chuong, M. Grumet, and G.M. Edelman. 1986. Differential contributions of Ng-CAM and N-CAM to cell adhesion in different neural regions. J. Cell Biol. 103:145-158.
36. Iozzo, R.V. 1998. Matrix proteoglycans: from molecular design to cellular function. Annu. Rev. Biochem. 67:609-652.
37. Iwamoto, T., N. Taniguchi, N. Asai, K. Ohkusin, I. Nakashima, and M. Takahashi. 1993. cDNA cloning of mouse ret proto-oncogene and its sequence similarity to the cadherin superfamily. Oncogene. 8:1087-1091.
38. Jing, S., D. Wen, Y. Yu, P.L. Holst, Y. Luo, M. Fang, R. Tamir, L. Antonio, Z. Hu, R. Cupples, et al. 1996. GDNF-induced activation of the ret protein tyrosine kinase is mediated hy GDNFR-α. a novel receptor for GDNF. Cell. 85:1113-1124.
39. Jaworski, D.M., G.M. Kelly, and S. Hockfield. 1995. BEHAB, a member of the proteoglycan tandem repeat family of hyaluronan-binding proteins that is restricted to the brain. J. Cell Biol. 125:495-509.
40. Kim, L., and T.W. Wong. 1995. The cytoplasmic tyrosine kinase FER is associated with the catenin-like substrate pp120 and is activated by growth factors. Mol. Cell. Biol. 15:4553-4561.
41. Klein, R.D., D. Sherman, W.-H. Ho, D. Stone, G.L. Bennett, B. Moffat, R. Vandlen, L. Simmons, Q. Gu, J.-A. Hongo, et al. 1997. A GPI-linked protein that interacts with Ret to form a candidate neurturin receptor. Nature. 387: 717-721.
42. Kreuger, R.C., Jr., T.A. Fields, J. Hildreth IV, and N.B. Schwartz. 1990. Chick cartilage chondroitin sulfate proteoglycan core protein I. Generation and characterization of peptides and specificity for glycosaminoglycan attachment. J. Biol. Chem. 265:12075-12087.
43. Lemmon, V. 1985. Monoclonal antibodies specific for glia in the chick nervous system. Brain Res. 355:111-120.
44. Lemmon, V., and S.C. McLoon. 1986. The appearance of an L1-like molecule in the chick visual pathway. J. Neurosci. 6:2987-2994.
45. Lilien, J., J. Balsamo, S. Hoffman, and C. Eisenberg. 1997. β-Catenin is a target for extracellular signals controlling cadherin function: the neurocan-Gal-NAcPTase connection. Curr. Top. Dev. Biol. 35:161-189.
46. Lilien, J., C. Arregui, H. Li, and J. Balsamo. 1999. The juxtamembrane domain of cadherin regulates integrin-mediated adhesion and neurite outgrowth. J. Neurosci. Res. 58:727-734.
47. Lilienbaum, A., A.A. Reszka, A.F. Horwitz, and C.E. Holt. 1995. Chimeric integrins expressed in retinal ganglion cells impairs process outgrowth in vivo. Mol. Cell. Neurosci. 6:139-152.
48. cas. J. Biol. Chem. 271:31290-31295.
49. Margolis, R.U., and R.K. Margolis. 1994. Aggrecan-versican-neurocan family proteoglycans. Methods Enzymol. 245:105-126.
50. Margolis, R.U., and R.K. Margolis. 1997. Chondroitin sulfate proteoglycans as mediators of axon growth and pathfinding. Cell Tissue Res. 290:343-348.
51. Matsuda, M., and T. Kurata. 1996. Emerging components of the Crk oncogene product: the first identified adaptor protein. Cell Signal. 8:335-340.
52. Matsui, F., M. Nishizuka, Y. Yasuda, S. Aono, E. Watanabe, and A. Oohira. 1998. Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum. Brain Res. 790:45-51.
53. Matsununga, M., K. Hatta, and M. Takeichi. 1988. Role of N-cadherin cell adhesion molecules in the histogenesis of neural retina. Neuron. 1:289-295.
54. Meyer-Puttlitz, B., P. Milev, E. Junker, I. Zimmer, R.U. Margolis, and R.K. Margolis. 1995. Chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of nervous tissue: developmental changes of neurocan and phosphocan. J. Neurochem. 65:2327-2337.
55. Milev, P., P. Maurel, M. Haring, R.K. Margolis, and R.U. Margolis. 1996. TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphocan/protein-tyrosine phosphatase-zeta/beta, and N-CAM. J. Biol. Chem. 271:15716-15723.
56. Miura, R., A. Aspberg, I.M. Ethell, K. Hagihara, R.L. Schnaar, E. Ruoslahti. and Y. Yamaguchi. 1999. The proteoglycan lectin domain binds sulfated cell surface glycolipids and promotes cell adhesion. J. Biol. Chem. 274:11431-11438.
57. Mueller, B.K. 1999. Growth cone guidance: first steps towards a deeper understanding. Annu. Rev. Neurosci. 22:351-388.
58. Neugebauer, K.M., K.J. Tomaselli, J. Lilien, and L.R. Reichardt. 1988. N-cadherin, NCAM, and integrins promote retinal neurite outgrowth on astrocytes in vitro. J. Cell Biol. 107:1177-1187.
59. cas, a Src-homology 3-containing molecule having multiple Src homology 2-binding motifs. J. Biol. Chem. 270:15398-15402.
60. Oohira, A., F. Matsui, E. Watanabe, Y. Kushima, and N. Maeda. 1994. Developmentally regulated expression of a brain specific species of chondroitin sulfate proteoglycan, neurocan, identified with a monoclonal antibody IG2 in the rat cerebrum. Neuroscience. 60:145-157.
61. Perez, F., A. Joliot, E. Bloch-Gallego, A. Zahroui, A. Triller, and A. Prochiantz. 1992. Antennapedia homeobox as a signal for the cellular internalization and nuclear addressing of a small exogenous peptide. J. Cell. Sci. 102: 717-722.
62. Petch, L.A., S.M. Bockholt, A. Bouton, J.T. Parsons, and K. Burridge. 1995. Adhesion induced tyrosine phosphorylation of the p130 src substrate. J. Cell. Sci. 108:1371-1379.
63. cas. Proc. Natl. Acad. Sci. USA. 92:10678-10682.
64. Powell, S.K., and H.K. Kleinman. 1997. Neuronal laminins and their cellular receptors. Int. J. Biochem. Cell Biol. 29:401-414.
65. Prange, C.K., L.A. Pennacchio, K. Lieuallen, W. Fan, and G.G. Lennon. 1998. Characterization of the human neurocan gene, CSPG3. Gene. 221:199-205.
66. Piochiantz, A. 1996. Getting hydrophilic compounds into cells: lessons from homeopeptides. Curr. Opin. Neurobiol. 6:629-634.
67. Rauch, U. 1997. Modeling an extracellular environment for axonal pathfinding and fasciculation in the central nervous system. Cell Tissue Res. 290:349-356.
68. Rauch, U., L. Karthikeyan, P. Maurel, R.U. Margolis, and R.K. Margolis. 1992. Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J. Biol. Chem. 267: 19536-19547.
69. Rauch, U., B. Grimpe, G. Kulbe, I. Arnold-Ammer, D.R. Beier, and R. Fassler. 1995. Structure and chromosomal localization of the mouse neurocan gene. Genomics. 28:405-410.
70. Retzler, C., W. Gohring, and U. Rauch. 1996a. Analysis of neurocan structures interacting with the neural cell adhesion molecule N-CAM. J. Biol. Chem. 271:27304-27310.
71. Retzler, C., H. Wiedemann, G. Kulbe, and U. Rauch. 1996b. Structural and electron microscopic analysis of neurocan and recombinant neurocan fragments. J. Biol. Chem. 271:17107-17113.
72. Riehl, R., K. Johnson, R. Bradley, G.B. Grunwald, E. Cornel, A. Lilienbaum, and C.E. Holt. 1996. Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron. 17:837-848.
73. Rosato, R., J.M. Veltmaat, J. Groffen, and N. Heistrekamp. 1998. Involvement of the tyrosine kinase Fer in cell adhesion. Mol. Cell. Biol. 18:5762-5770.
74. Ruoslahti, E. 1996. Brain extracellular matrix. Glycobiology. 6:489-492.
75. Saleque, S., N. Ruiz, and K. Drickamer. 1993. Expression and characterization of a carbohydrate-binding fragment of rat aggrecan. Glycobiology. 3:185-210.
76. Schwartz, N.B., E.W. Pirok III, J.R. Mensch Jr., and M.S. Domowicz. 1999. Domain organization, genomic structure, evolution, and regulation of expression of the aagrecan gene family. Prog. Nucleic Acid Res. Mol. Biol. 62:177-225.
77. Scott, L.J., J. Balsamo, J.R. Sanes, and J. Lilien. 1990. Synaptic localization and neural regulation of an N-acetylgalaclosaminyltransferase in skeletal muscle. J. Neurosci. 10:346-350.
78. Snow, D.M., W. Watanabe, P.C. Letourneau, and J. Silver. 1991. A chondroitin sulfate proteoglycan may influence the direction of retinal ganglion cell outgrowth. Development. 113:1473-1485.
79. Song, H.-J., and M.-M. Poo. 1999. Signal transduction underlying growth cone guidance by diffusible factors. Curr. Opin. Neurobiol. 9:355-363.
80. Stone, K.E., and D.S. Sakaguchi. 1996. Perturbation of the developing Xenopus retinotectal projection following injections of antibodies against β1-integrin receptors and N-cadherin. Develop. Biol. 180:297-310.
81. Svennevik, E., and P.J. Linser. 1993. The inhibitory effects of integrin antibodies and the RGD tripeptide on early eye development. Invest. Ophth. Vis. Sci. 34:1774-1784.
82. Takeda, H., Y. Shimoyama, A. Nagafuchi, and S. Hirohashi. 1999. E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat. Struct. Biol. 6:310-312.
83. Tomaselli, K.J., L.F. Reichardt, and J.L. Bixby. 1986. Distinct molecular interactions mediate process outgrowth on nonneuronal cell surfaces and extracellular matrices. J. Cell Biol. 106:2659-2672.
84. Tomaselli, K.J., K.M. Neugebauer, J.L. Bixby, J. Lilien, and L.F. Reichardt. 1989. N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron. 1:33-43.
85. Treanor, J.J.S., L. Goodman, F. de Sauvage, D.M. Stone, K.T. Poulsen, C.D. Beck, C. Gray, M.P. Armanini, R.A. Pollock, F. Hefti, et al. 1996. Characterization of a multicomponent receptor for GDNF. Nature. 382:80-83.
86. Ujita, M., T. Shinomura, K. Ito, Y. Kitagawa, and K. Kimata. 1994. Expression and binding activity of the carboxyl-terminal portion of the core protein of PG-M, a large chondroitin sulfate proteoglycan. J. Biol. Chem. 269:27603-27609.
87. cas and cortactin accompanies integrin-mediated cell adhesion to extracellular matrix. J. Biol. Chem. 270:22257-22262.
88. Yamada, H., K. Watanabe, M. Shimonaka, and Y. Yamaguchi. 1994. Molecular cloning of brevican, a novel brain proteoglycan of the aggrecan/versican family. J. Biol. Chem. 269:10119-10126.
89. Yap, A.S., W.M. Bricher, M. Pruschy, and B.M. Gumbiner. 1997. Lateral clustering of the adhesive ectodomain: a fundamental determinant of cadherin function. Curr. Biol. 7:308-315.
90. Zanin, M.K.B., J. Bundy, H. Ernst, A. Wessels, J.S. Conway, and S. Hoffman. 1999. Distinct spatial and temporal distributions of aggrecan and versican in the embryonic chick heart. Anat. Rec. 256:366-380.
91. Zeiner, M., and U. Gehring. 1994. Cloning of 5′ cDNA regions by inverse PCR. Biotechnology. 17:1050-1052.
92. Zimmermann, D.R., and E. Ruoslahti. 1989. Multiple domains of the large fibroblast proteoglycan, versican. EMBO. (Eur. Mol. Biol. Organ.) J. 8:2975-2981.