Glycosylation at Asn211 regulates the activation state of the discoidin domain receptor 1 (DDR1)

Journal of Biological Chemistry

Volumn 289, Issue 13, 2014, Pages 9275-9287

  Fu, Hsueh Liang ^a   Valiathan, Rajeshwari R ^a   Payne, Leo ^c   Kumarasiri, Malika ^b,d   Mahasenan, Kiran V ^b   Mobashery, Shahriar ^b   Huang, Paul ^c   Fridman, Rafael ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; COLLAGEN; DIMERIZATION; ENZYMES; LIGANDS; MASS SPECTROMETRY; PHOSPHORYLATION;

COLLAGEN BINDING DOMAIN; INHIBITORY MECHANISM; N-GLYCOSYLATION SITES; RECEPTOR ACTIVATION; RECEPTOR TYROSINE KINASE; SITE DIRECTED MUTAGENESIS; STRUCTURAL MECHANISMS; SUSTAINED ACTIVATION;

GLYCOSYLATION;

ASPARAGINE; COLLAGEN TYPE 1; DISCOIDIN DOMAIN RECEPTOR 1; MUTANT PROTEIN; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; COLLAGEN; DDR1 PROTEIN, HUMAN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL SURFACE; CONTROLLED STUDY; DIMERIZATION; EMBRYO; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ENDOCYTOSIS; GENETICS; GLYCOSYLATION; METABOLISM; MOLECULAR GENETICS; MUTAGENESIS SITE-SPECIFIC; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; RECEPTOR REGULATION;

COLLAGEN; GLYCOSYLATION; MUTAGENESIS SITE-SPECIFIC; RECEPTOR REGULATION; RECEPTOR TYROSINE KINASE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ASPARAGINE; CELL LINE; COLLAGEN TYPE I; CONSERVED SEQUENCE; ENDOCYTOSIS; GLYCOSYLATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84897435857     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.541102     Document Type: Article

References (47)

1. Leitinger, B. (2011) Transmembrane collagen receptors. Annu. Rev. Cell Dev. Biol. 27, 265-290
2. Yeh, Y. C., Lin, H. H., and Tang, M. J. (2012) A tale of two collagen receptors, integrin β1 and discoidin domain receptor 1, in epithelial cell differentiation. Am. J. Physiol. Cell Physiol. 303, C1207-C1217
3. Vogel, W. F., Abdulhussein, R., and Ford, C. E. (2006) Sensing extracellular matrix: an update on discoidin domain receptor function. Cell. Signal. 18, 1108-1116 (Pubitemid 43674043)
4. Leitinger, B., and Hohenester, E. (2007) Mammalian collagen receptors. Matrix Biol. 26, 146-155 (Pubitemid 46401227)
5. Fu, H. L., Valiathan, R. R., Arkwright, R., Sohail, A., Mihai, C., Kumarasiri, M., Mahasenan, K. V., Mobashery, S., Huang, P., Agarwal, G., and Fridman, R. (2013) Discoidin domain receptors: unique receptor tyrosine kinases in collagen-mediated signaling. J. Biol. Chem. 288, 7430-7437
6. Valiathan, R. R., Marco, M., Leitinger, B., Kleer, C. G., and Fridman, R. (2012) Discoidin domain receptor tyrosine kinases: new players in cancer progression. Cancer Metastasis Rev. 31, 295-321
7. Carafoli, F., and Hohenester, E. (2013) Collagen recognition and transmembrane signalling by discoidin domain receptors. Biochim. Biophys. Acta 1834, 2187-2194
8. Leitinger, B., and Kwan, A. P. (2006) The discoidin domain receptor DDR2 is a receptor for type X collagen. Matrix Biol. 25, 355-364 (Pubitemid 44175833)
9. Vogel, W., Gish, G. D., Alves, F., and Pawson, T. (1997) The discoidin domain receptor tyrosine kinases are activated by collagen. Mol. Cell 1, 13-23 (Pubitemid 127376389)
10. Noordeen, N. A., Carafoli, F., Hohenester, E., Horton, M. A., and Leitinger, B. (2006) A transmembrane leucine zipper is required for activation of the dimeric receptor tyrosine kinase DDR1. J. Biol. Chem. 281, 22744-22751
11. Mihai, C., Chotani, M., Elton, T. S., and Agarwal, G. (2009) Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy. J. Mol. Biol. 385, 432-445
12. Curat, C. A., Eck, M., Dervillez, X., and Vogel, W. F. (2001) Mapping of epitopes in discoidin domain receptor 1 critical for collagen binding. J. Biol. Chem. 276, 45952-45958
13. Abdulhussein, R., McFadden, C., Fuentes-Prior, P., and Vogel, W. F. (2004) Exploring the collagen-binding site of the DDR1 tyrosine kinase receptor. J. Biol. Chem. 279, 31462-31470 (Pubitemid 39037814)
14. Phan, T. N., Wong, E. L., Sun, X., Kim, G., Jung, S. H., Yoon, C. N., and Yang, B. S. (2013) Low stability and a conserved N-glycosylation site are associated with regulation of the discoidin domain receptor family by glucose via post-translational N-glycosylation. Biosci. Biotechnol. Biochem. 77, 1907-1916
15. Fu, H. L., Sohail, A., Valiathan, R. R., Wasinski, B. D., Kumarasiri, M., Mahasenan, K. V., Bernardo, M. M., Tokmina-Roszyk, D., Fields, G. B., Mobashery, S., and Fridman, R. (2013) Shedding of discoidin domain receptor 1 by membrane-type matrix metalloproteinases. J. Biol. Chem. 288, 12114-12129
16. Xu, H., Raynal, N., Stathopoulos, S., Myllyharju, J., Farndale, R. W., and Leitinger, B. (2011) Collagen binding specificity of the discoidin domain receptors: binding sites on collagens II and III and molecular determinants for collagen IV recognition by DDR1. Matrix Biol. 30, 16-26
17. Wang, Y., Fu, X., Gaiser, S., Köttgen, M., Kramer-Zucker, A., Walz, G., and Wegierski, T. (2007) OS-9 regulates the transit and polyubiquitination of TRPV4 in the endoplasmic reticulum. J. Biol. Chem. 282, 36561-36570
18. Iwai, L. K., Chang, F., and Huang, P. H. (2013) Phosphoproteomic analysis identifies insulin enhancement of discoidin domain receptor 2 phosphorylation. Cell Adh. Migr. 7, 161-164
19. Iwai, L. K., Payne, L. S., Luczynski, M. T., Chang, F., Xu, H., Clinton, R. W., Paul, A., Esposito, E. A., Gridley, S., Leitinger, B., Naegle, K. M., and Huang, P. H. (2013) Phosphoproteomics of collagen receptor networks reveals SHP-2 phosphorylation downstream of wild-type DDR2 and its lung cancer mutants. Biochem. J. 454, 501-513
20. Carafoli, F., Mayer, M. C., Shiraishi, K., Pecheva, M. A., Chan, L. Y., Nan, R., Leitinger, B., and Hohenester, E. (2012) Structure of the discoidin domain receptor 1 extracellular region bound to an inhibitory Fab fragment reveals features important for signaling. Structure 20, 688-697
21. McGuffin, L. J., Bryson, K., and Jones, D. T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16, 404-405 (Pubitemid 30417087)
22. Cole, C., Barber, J. D., and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201
23. Leitinger, B. (2003) Molecular analysis of collagen binding by the human discoidin domain receptors, DDR1 and DDR2. Identification of collagen binding sites in DDR2. J. Biol. Chem. 278, 16761-16769
24. Petrescu, A. J., Milac, A. L., Petrescu, S. M., Dwek, R. A., and Wormald, M. R. (2004) Statistical analysis of the protein environment of N-glycosylation sites: implications for occupancy, structure, and folding. Glycobiology 14, 103-114 (Pubitemid 38263095)
25. 1 integrin. J. Biol. Chem. 275, 5779-5784
26. Kim, H. G., Hwang, S. Y., Aaronson, S. A., Mandinova, A., and Lee, S. W. (2011) DDR1 receptor tyrosine kinase promotes prosurvival pathway through Notch1 activation. J. Biol. Chem. 286, 17672-17681
27. Kim, H. G., Tan, L., Weisberg, E. L., Liu, F., Canning, P., Choi, H. G., Ezell, S. A., Wu, H., Zhao, Z., Wang, J., Mandinova, A., Griffin, J. D., Bullock, A. N., Liu, Q., Lee, S. W., and Gray, N. S. (2013) Discovery of a potent and selective DDR1 receptor tyrosine kinase inhibitor. ACS Chem. Biol. 8, 2145-2150
28. L'hôte, C. G., Thomas, P. H., and Ganesan, T. S. (2002) Functional analysis of discoidin domain receptor 1: effect of adhesion on DDR1 phosphorylation. FASEB J. 16, 234-236
29. Shrivastava, A., Radziejewski, C., Campbell, E., Kovac, L., McGlynn, M., Ryan, T. E., Davis, S., Goldfarb, M. P., Glass, D. J., Lemke, G., and Yancopoulos, G. D. (1997) An orphan receptor tyrosine kinase family whose members serve as nonintegrin collagen receptors. Mol. Cell 1, 25-34 (Pubitemid 127376390)
30. Arancibia-Carcamo, I. L., Fairfax, B. P., Moss, S. J., and Kittler, J. T. (2006) in The Dynamic Synapse: Molecular Methods in Ionotropic Receptor Biology (Kittler, J. T., and Moss, S. J., eds) CRC Press, Inc., Boca Raton, FL
31. Cho, J. A., Osenkowski, P., Zhao, H., Kim, S., Toth, M., Cole, K., Aboukameel, A., Saliganan, A., Schuger, L., Bonfil, R. D., and Fridman, R. (2008) The inactive 44-kDa processed form of membrane type 1 matrix metalloproteinase (MT1-MMP) enhances proteolytic activity via regulation of endocytosis of active MT1-MMP. J. Biol. Chem. 283, 17391-17405
32. Agarwal, G., Mihai, C., and Iscru, D. F. (2007) Interaction of discoidin domain receptor 1 with collagen type 1. J. Mol. Biol. 367, 443-455 (Pubitemid 46295432)
33. Liu, Y. C., Yen, H. Y., Chen, C. Y., Chen, C. H., Cheng, P. F., Juan, Y. H., Chen, C. H., Khoo, K. H., Yu, C. J., Yang, P. C., Hsu, T. L., and Wong, C. H. (2011) Sialylation and fucosylation of epidermal growth factor receptor suppress its dimerization and activation in lung cancer cells. Proc. Natl. Acad. Sci. U.S.A. 108, 11332-11337
34. Whitson, K. B., Whitson, S. R., Red-Brewer, M. L., McCoy, A. J., Vitali, A. A., Walker, F., Johns, T. G., Beth, A. H., and Staros, J. V. (2005) Functional effects of glycosylation at Asn-579 of the epidermal growth factor receptor. Biochemistry 44, 14920-14931 (Pubitemid 41612271)
35. Takahashi, M., Tsuda, T., Ikeda, Y., Honke, K., and Taniguchi, N. (2004) Role of N-glycans in growth factor signaling. Glycoconj. J. 20, 207-212
36. Tsuda, T., Ikeda, Y., and Taniguchi, N. (2000) The Asn-420-linked sugar chain in human epidermal growth factor receptor suppresses ligand-independent spontaneous oligomerization. Possible role of a specific sugar chain in controllable receptor activation. J. Biol. Chem. 275, 21988-21994 (Pubitemid 30621773)
37. Watson, F. L., Porcionatto, M. A., Bhattacharyya, A., Stiles, C. D., and Segal, R. A. (1999) TrkA glycosylation regulates receptor localization and activity. J. Neurobiol. 39, 323-336 (Pubitemid 29190637)
38. Yokoe, S., Takahashi, M., Asahi, M., Lee, S. H., Li, W., Osumi, D., Miyoshi, E., and Taniguchi, N. (2007) The Asn418-linked N-glycan of ErbB3 plays a crucial role in preventing spontaneous heterodimerization and tumor promotion. Cancer Res. 67, 1935-1942 (Pubitemid 46424209)
39. Mazumder, R., Morampudi, K. S., Motwani, M., Vasudevan, S., and Goldman, R. (2012) Proteome-wide analysis of single-nucleotide variations in the N-glycosylation sequon of human genes. PLoS One 7, e36212
40. Lemeer, S., Bluwstein, A., Wu, Z., Leberfinger, J., Müller, K., Kramer, K., and Kuster, B. (2012) Phosphotyrosine mediated protein interactions of the discoidin domain receptor 1. J. Proteomics 75, 3465-3477
41. Wang, C. Z., Su, H. W., Hsu, Y. C., Shen, M. R., and Tang, M. J. (2006) A discoidin domain receptor 1/SHP-2 signaling complex inhibits α2β1-integrin-mediated signal transducers and activators of transcription 1/3 activation and cell migration. Mol. Biol. Cell 17, 2839-2852
42. Finger, C., Escher, C., and Schneider, D. (2009) The single transmembrane domains of human receptor tyrosine kinases encode self-interactions. Sci. Signal. 2, ra56
43. Guo, H. B., Johnson, H., Randolph, M., Lee, I., and Pierce, M. (2009) Knockdown of GnT-Va expression inhibits ligand-induced downregulation of the epidermal growth factor receptor and intracellular signaling by inhibiting receptor endocytosis. Glycobiology 19, 547-559
44. Chung, I., Akita, R., Vandlen, R., Toomre, D., Schlessinger, J., and Mellman, I. (2010) Spatial control of EGF receptor activation by reversible dimerization on living cells. Nature 464, 783-787
45. Shan, Y., Eastwood, M. P., Zhang, X., Kim, E. T., Arkhipov, A., Dror, R. O., Jumper, J., Kuriyan, J., and Shaw, D. E. (2012) Oncogenic mutations counteract intrinsic disorder in the EGFR kinase and promote receptor dimerization. Cell 149, 860-870
46. Lemmon, M. A., and Schlessinger, J. (2010) Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134
47. Ohtsubo, K., and Marth, J. D. (2006) Glycosylation in cellular mechanisms of health and disease. Cell 126, 855-867 (Pubitemid 44310784)