Suppression of heregulin β signaling by the single N-glycan deletion mutant of soluble ErbB3 protein

Journal of Biological Chemistry

Volumn 288, Issue 46, 2013, Pages 32910-32921

  Takahashi, Motoko ^a   Hasegawa, Yoshihiro ^a   Ikeda, Yoshitaka ^b   Wada, Yoshinao ^c   Tajiri, Michiko ^c   Ariki, Shigeru ^a   Takamiya, Rina ^a   Nishitani, Chiaki ^a   Araki, Motoko ^a   Yamaguchi, Yoshiki ^d   Taniguchi, Naoyuki ^d   Kuroki, Yoshio ^a  

^a SAPPORO MEDICAL UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b SAGA UNIVERSITY   (Japan)

^c RESEARCH INSTITUTE FOR MATERNAL AND CHILD HEALTH   (Japan)

^d RIKEN   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTICANCER EFFECTS; DELETION MUTANTS; EXTRACELLULAR DOMAINS; HUMAN BREAST CANCER CELLS; RECEPTOR ACTIVATION; SMALL INTERFERING RNA (SIRNA); SUPPRESSING EFFECTS; TUMOR PROLIFERATION;

CELL CULTURE; LIGANDS; POLYSACCHARIDES;

SIGNALING;

ANTINEOPLASTIC AGENT; ASPARAGINE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GLYCAN; HEREGULIN BETA; LAPATINIB; N GLYCAN; NEU DIFFERENTIATION FACTOR; SOLUBLE EPIDERMAL GROWTH FACTOR RECEPTOR 3; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG MECHANISM; DRUG POTENTIATION; MUTATIONAL ANALYSIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

EPIDERMAL GROWTH FACTOR RECEPTOR (EGFR); GLYCOSYLATION; GROWTH FACTORS; MASS SPECTROMETRY (MS); RECEPTORS;

AMINO ACID SUBSTITUTION; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; HUMANS; MAP KINASE SIGNALING SYSTEM; MUTATION, MISSENSE; NEUREGULIN-1; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; QUINAZOLINES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3;

EID: 84887848085     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.491902     Document Type: Article

References (51)

1. Ferguson, K. M., Berger, M. B., Mendrola, J. M., Cho, H. S., Leahy, D. J., and Lemmon, M. A. (2003) EGF activates its receptor by removing interactions that autoinhibit ectodomain dimerization. Mol. Cell 11, 507-517
2. Burgess, A. W., Cho, H. S., Eigenbrot, C., Ferguson, K. M., Garrett, T. P., Leahy, D. J., Lemmon, M. A., Sliwkowski, M. X., Ward, C. W., and Yokoyama, S. (2003) An open-and-shut case? Recent insights into the activation of EGF/ErbB receptors. Mol. Cell 12, 541-552
3. Dawson, J. P., Bu, Z., and Lemmon, M. A. (2007) Ligand-induced structural transitions in ErbB receptor extracellular domains. Structure 15, 942-954
4. Lemmon, M. A. (2009) Ligand-induced ErbB receptor dimerization. Exp. Cell Res. 315, 638-648
5. Yarden, Y., and Sliwkowski, M. X. (2001) Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137
6. Wheeler, D. L., Huang, S., Kruser, T. J., Nechrebecki, M. M., Armstrong, E. A., Benavente, S., Gondi, V., Hsu, K. T., and Harari, P. M. (2008) Mechanisms of acquired resistance to cetuximab. Role of HER (ErbB) family members. Oncogene 27, 3944-3956
7. Hudziak, R. M., Lewis, G. D., Winget, M., Fendly, B. M., Shepard, H. M., and Ullrich, A. (1989) p185HER2 monoclonal antibody has antiproliferative effects in vitro and sensitizes human breast tumor cells to tumor necrosis factor. Mol. Cell. Biol. 9, 1165-1172
8. Baselga, J., Norton, L., Albanell, J., Kim, Y. M., and Mendelsohn, J. (1998) Recombinant humanized anti-HER2 antibody (Herceptin) enhances the antitumor activity of paclitaxel and doxorubicin against HER2/neu overexpressing human breast cancer xenografts. Cancer Res. 58, 2825-2831
9. Fry, D. W., Kraker, A. J., McMichael, A., Ambroso, L. A., Nelson, J. M., Leopold, W. R., Connors, R. W., and Bridges, A. J. (1994) A specific inhibitor of the epidermal growth factor receptor tyrosine kinase. Science 265, 1093-1095
10. Ward, W. H., Cook, P. N., Slater, A. M., Davies, D. H., Holdgate, G. A., and Green, L. R. (1994) Epidermal growth factor receptor tyrosine kinase. Investigation of catalytic mechanism, structure-based searching, and discovery of a potent inhibitor. Biochem. Pharmacol. 48, 659-666
11. Rusnak, D. W., Affleck, K., Cockerill, S. G., Stubberfield, C., Harris, R., Page, M., Smith, K. J., Guntrip, S. B., Carter, M. C., Shaw, R. J., Jowett, A., Stables, J., Topley, P., Wood, E. R., Brignola, P. S., Kadwell, S. H., Reep, B. R., Mullin, R. J., Alligood, K. J., Keith, B. R., Crosby, R. M., Murray, D. M., Knight, W. B., Gilmer, T. M., and Lackey, K. (2001) The characterization of novel, dual ErbB-2/EGFR, tyrosine kinase inhibitors. Potential therapy for cancer. Cancer Res. 61, 7196-7203
12. Doherty, J. K., Bond, C., Jardim, A., Adelman, J. P., and Clinton, G. M. (1999) The HER-2/neu receptor tyrosine kinase gene encodes a secreted autoinhibitor. Proc. Natl. Acad. Sci. U.S.A. 96, 10869-10874
13. Azios, N. G., Romero, F. J., Denton, M. C., Doherty, J. K., and Clinton, G. M. (2001) Expression of herstatin, an autoinhibitor of HER-2/neu, inhibits transactivation of HER-3 by HER-2 and blocks EGF activation of the EGF receptor. Oncogene 20, 5199-5209
14. Lee, H., Akita, R. W., Sliwkowski, M. X., and Maihle, N. J. (2001) A naturally occurring secreted human ErbB3 receptor isoform inhibits heregulin- stimulated activation of ErbB2, ErbB3, and ErbB4. Cancer Res. 61, 4467-4473
15. Lindzen, M., Carvalho, S., Starr, A., Ben-Chetrit, N., Pradeep, C. R., Köstler, W. J., Rabinkov, A., Lavi, S., Bacus, S. S., and Yarden, Y. (2012) A recombinant decoy comprising EGFR and ErbB-4 inhibits tumor growth and metastasis. Oncogene 31, 3505-3515
16. Yoon, S. J., Nakayama, K., Hikita, T., Handa, K., and Hakomori, S. I. (2006) Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 18987-18991
17. Kawashima, N., Yoon, S. J., Itoh, K., and Nakayama, K. (2009) Tyrosine kinase activity of epidermal growth factor receptor is regulated by GM3 binding through carbohydrate to carbohydrate interactions. J. Biol. Chem. 284, 6147-6155
18. 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
19. 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
20. Sato, Y., Takahashi, M., Shibukawa, Y., Jain, S. K., Hamaoka, R., Miyagawa, J. i., Yaginuma, Y., Honke, K., Ishikawa, M., and Taniguchi, N. (2001) Overexpression of N-acetylglucosaminyltransferase III enhances the epidermal growth factor-induced phosphorylation of ERK in HeLaS3 cells by up-regulation of the internalization rate of the receptors. J. Biol. Chem. 276, 11956-11962
21. Gu, J., Zhao, Y., Isaji, T., Shibukawa, Y., Ihara, H., Takahashi, M., Ikeda, Y., Miyoshi, E., Honke, K., and Taniguchi, N. (2004) β1,4-N- Acetylglucosaminyltransferase III down-regulates neurite outgrowth induced by costimulation of epidermal growth factor and integrins through the Ras/ERK signaling pathway in PC12 cells. Glycobiology 14, 177-186
22. 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
23. Yokoe, S., Takahashi, M., Asahi, M., Lee, S. H., Li, W., Osumi, D., Miyoshi, E., and Taniguchi, N. (2007) The Asn-418-linked N-glycan of ErbB3 plays a crucial role in preventing spontaneous heterodimerization and tumor promotion. Cancer Res. 67, 1935-1942
24. Takahashi, M., Yokoe, S., Asahi, M., Lee, S. H., Li, W., Osumi, D., Miyoshi, E., and Taniguchi, N. (2008)N-Glycan of ErbB family plays a crucial role in dimer formation and tumor promotion. Biochim. Biophys. Acta 1780, 520-524
25. Garrett, T. P., McKern, N. M., Lou, M., Elleman, T. C., Adams, T. E., Lovrecz, G. O., Kofler, M., Jorissen, R. N., Nice, E. C., Burgess, A. W., and Ward, C. W. (2003) The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors. Mol. Cell 11, 495-505
26. Cho, H. S., Mason, K., Ramyar, K. X., Stanley, A. M., Gabelli, S. B., Denney, D. W., Jr., and Leahy, D. J. (2003) Structure of the extracellular region of HER2 alone and in complex with the Herceptin Fab. Nature 421, 756-760
27. Cho, H. S., and Leahy, D. J. (2002) Structure of the extracellular region of HER3 reveals an interdomain tether. Science 297, 1330-1333
28. Bouyain, S., Longo, P. A., Li, S., Ferguson, K. M., and Leahy, D. J. (2005) The extracellular region of ErbB4 adopts a tethered conformation in the absence of ligand. Proc. Natl. Acad. Sci. U.S.A. 102, 15024-15029
29. Chen, W., and Stanley, P. (2003) Five Lec1CHOcell mutants have distinct Mgat1 gene mutations that encode truncatedN-acetylglucosaminyltransferase I. Glycobiology 13, 43-50
30. Hong, Y., and Stanley, P. (2003) Lec3 Chinese hamster ovary mutants lack UDP-N-acetylglucosamine 2-epimerase activity because of mutations in the epimerase domain of the Gne gene. J. Biol. Chem. 278, 53045-53054
31. Wada, Y., Tajiri, M., and Yoshida, S. (2004) Hydrophilic affinity isolation and MALDI multiple-stage tandem mass spectrometry of glycopeptides for glycoproteomics. Anal Chem. 76, 6560-6565
32. Tajiri, M., Yoshida, S., and Wada, Y. (2005) Differential analysis of sitespecific glycans on plasma and cellular fibronectins. Application of a hydrophilic affinity method for glycopeptide enrichment. Glycobiology 15, 1332-1340
33. Wada, Y., Tajiri, M., and Ohshima, S. (2010) Quantitation of saccharide compositions of O-glycans by mass spectrometry of glycopeptides and its application to rheumatoid arthritis. J Proteome Res 9, 1367-1373
34. Sithanandam, G., and Anderson, L. M. (2008) The ERBB3 receptor in cancer and cancer gene therapy. Cancer Gene Ther. 15, 413-448
35. Baselga, J., and Swain, S. M. (2009) Novel anticancer targets. Revisiting ERBB2 and discovering ERBB3. Nat. Rev. Cancer 9, 463-475
36. Campbell, M. R., Amin, D., and Moasser, M. M. (2010) HER3 comes of age. New insights into its functions and role in signaling, tumor biology, and cancer therapy. Clin. Cancer Res. 16, 1373-1383
37. Tzahar, E., Waterman, H., Chen, X., Levkowitz, G., Karunagaran, D., Lavi, S., Ratzkin, B. J., and Yarden, Y. (1996) A hierarchical network of interreceptor interactions determines signal transduction by Neu differentiation factor/neuregulin and epidermal growth factor. Mol. Cell. Biol. 16, 5276-5287
38. Pinkas-Kramarski, R., Soussan, L., Waterman, H., Levkowitz, G., Alroy, I., Klapper, L., Lavi, S., Seger, R., Ratzkin, B. J., Sela, M., and Yarden, Y. (1996) Diversification of Neu differentiation factor and epidermal growth factor signaling by combinatorial receptor interactions. EMBO J. 15, 2452-2467
39. Zhang, Q., Park, E., Kani, K., and Landgraf, R. (2012) Functional isolation of activated and unilaterally phosphorylated heterodimers of ERBB2 and ERBB3 as scaffolds in ligand-dependent signaling. Proc. Natl. Acad. Sci. U.S.A. 109, 13237-13242
40. Shibukawa, Y., Takahashi, M., Laffont, I., Honke, K., and Taniguchi, N. (2003) Down-regulation of hydrogen peroxide-induced PKC delta activation in N-acetylglucosaminyltransferase III-transfected HeLaS3 cells. J. Biol. Chem. 278, 3197-3203
41. Isaji, T., Gu, J., Nishiuchi, R., Zhao, Y., Takahashi, M., Miyoshi, E., Honke, K., Sekiguchi, K., and Taniguchi, N. (2004) Introduction of bisecting GlcNAc into integrin α5β1 reduces ligand binding and down-regulates cell adhesion and cell migration. J. Biol. Chem. 279, 19747-19754
42. Lee, S. H., Takahashi, M., Honke, K., Miyoshi, E., Osumi, D., Sakiyama, H., Ekuni, A., Wang, X., Inoue, S., Gu, J., Kadomatsu, K., and Taniguchi, N. (2006) Loss of core fucosylation of low-density lipoprotein receptor-related protein-1 impairs its function, leading to the upregulation of serum levels of insulin-like growth factor-binding protein 3 in Fut8-/- mice. J Biochem. 139, 391-398
43. Li, W., Takahashi, M., Shibukawa, Y., Yokoe, S., Gu, J., Miyoshi, E., Honke, K., Ikeda, Y., and Taniguchi, N. (2007) Introduction of bisecting GlcNAc in N-glycans of adenylyl cyclase III enhances its activity. Glycobiology 17, 655-662
44. Osumi, D., Takahashi, M., Miyoshi, E., Yokoe, S., Lee, S. H., Noda, K., Nakamori, S., Gu, J., Ikeda, Y., Kuroki, Y., Sengoku, K., Ishikawa, M., and Taniguchi, N. (2009) Core fucosylation of E-cadherin enhances cell-cell adhesion in human colon carcinoma WiDr cells. Cancer Sci. 100, 888-895
45. Takahashi, M., Kuroki, Y., Ohtsubo, K., and Taniguchi, N. (2009) Core fucose and bisecting GlcNAc, the direct modifiers of the N-glycan core. Their functions and target proteins. Carbohydr. Res. 344, 1387-1390
46. Alvarado, D., Klein, D. E., and Lemmon, M. A. (2009) ErbB2 resembles an autoinhibited invertebrate epidermal growth factor receptor. Nature 461, 287-291
47. 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
48. Xu, J., He, J., Castleberry, A. M., Balasubramanian, S., Lau, A. G., and Hall, R. A. (2003) Heterodimerization of α2A- and β1-adrenergic receptors. J. Biol. Chem. 278, 10770-10777
49. Watty, A., and Burden, S. J. (2002) MuSK glycosylation restrains MuSK activation and acetylcholine receptor clustering. J. Biol. Chem. 277, 50457-50462
50. Horan, T., Wen, J., Arakawa, T., Liu, N., Brankow, D., Hu, S., Ratzkin, B., and Philo, J. S. (1995) Binding of Neu differentiation factor with the extracellular domain of Her2 and Her3. J. Biol. Chem. 270, 24604-24608
51. Ferguson, K. M., Darling, P. J., Mohan, M. J., Macatee, T. L., and Lemmon, M. A. (2000) Extracellular domains drive homo- but not hetero-dimerization of erbB receptors. EMBO J. 19, 4632-4643