36
Views
41
CrossRef citations to date
0
Altmetric
Article

The E3 Ubiquitin Ligase WWP1 Selectively Targets HER4 and Its Proteolytically Derived Signaling Isoforms for Degradation

, , , , , , & show all
Pages 892-906 | Received 11 Apr 2008, Accepted 19 Nov 2008, Published online: 21 Mar 2023

REFERENCES

  • Aqeilan, R. I., V. Donati, E. Gaudio, M. S. Nicoloso, M. Sundvall, A. Korhonen, J. Lundin, J. Isola, M. Sudol, H. Joensuu, C. M. Croce, and K. Elenius. 2007. Association of Wwox with ErbB4 in breast cancer. Cancer Res. 67:9330–9336.
  • Aqeilan, R. I., V. Donati, A. Palamarchuk, F. Trapasso, M. Kaou, Y. Pekarsky, M. Sudol, and C. M. Croce. 2005. WW domain-containing proteins, WWOX and YAP, compete for interaction with ErbB-4 and modulate its transcriptional function. Cancer Res. 65:6764–6772.
  • Barnes, N. L., S. Khavari, G. P. Boland, A. Cramer, W. F. Knox, and N. J. Bundred. 2005. Absence of HER4 expression predicts recurrence of ductal carcinoma in situ of the breast. Clin. Cancer Res. 11:2163–2168.
  • Bieche, I., P. Onody, S. Tozlu, K. Driouch, M. Vidaud, and R. Lidereau. 2003. Prognostic value of ERBB family mRNA expression in breast carcinomas. Int. J. Cancer 106:758–765.
  • Chen, C., and L. E. Matesic. 2007. The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer Metastasis Rev. 26:587–604.
  • Chen, C., X. Sun, P. Guo, X. Y. Dong, P. Sethi, W. Zhou, Z. Zhou, J. Petros, H. F. Frierson, Jr., R. L. Vessella, A. Atfi, and J. T. Dong. 2007. Ubiquitin E3 ligase WWP1 as an oncogenic factor in human prostate cancer. Oncogene 26:2386–2394.
  • Chen, C., Z. Zhou, J. S. Ross, W. Zhou, and J. T. Dong. 2007. The amplified WWP1 gene is a potential molecular target in breast cancer. Int. J. Cancer 121:80–87.
  • Cheng, Q. C., O. Tikhomirov, W. Zhou, and G. Carpenter. 2003. Ectodomain cleavage of ErbB-4: characterization of the cleavage site and m80 fragment. J. Biol. Chem. 278:38421–38427.
  • Diamonti, A. J., P. M. Guy, C. Ivanof, K. Wong, C. Sweeney, and K. L. Carraway III. 2002. An RBCC protein implicated in maintenance of steady-state neuregulin receptor levels. Proc. Natl. Acad. Sci. USA 99:2866-2871
  • Earp, H. S., III, B. F. Calvo, and C. I. Sartor. 2003. The EGF receptor family: multiple roles in proliferation, differentiation, and neoplasia with an emphasis on HER4. Trans. Am. Clin. Climatol. Assoc. 114:315–333.
  • Elenius, K., C. J. Choi, S. Paul, E. Santiestevan, E. Nishi, and M. Klagsbrun. 1999. Characterization of a naturally occurring ErbB4 isoform that does not bind or activate phosphatidyl inositol 3-kinase. Oncogene 18:2607–2615.
  • Elenius, K., G. Corfas, S. Paul, C. J. Choi, C. Rio, G. D. Plowman, and M. Klagsbrun. 1997. A novel juxtamembrane domain isoform of HER4/ErbB4. Isoform-specific tissue distribution and differential processing in response to phorbol ester. J. Biol. Chem. 272:26761–26768.
  • Feng, S. M., C. I. Sartor, D. Hunter, H. Zhou, X. Yang, L. S. Caskey, R. Dy, R. S. Muraoka-Cook, and H. S. Earp III. 2007. The HER4 cytoplasmic domain, but not its C terminus, inhibits mammary cell proliferation. Mol. Endocrinol. 21:1861–1876.
  • Flasza, M., P. Gorman, R. Roylance, A. E. Canfield, and M. Baron. 2002. Alternative splicing determines the domain structure of WWP1, a Nedd4 family protein. Biochem. Biophys. Res. Commun. 290:431–437.
  • Gilbertson, R., R. Hernan, T. Pietsch, L. Pinto, P. Scotting, R. Allibone, D. Ellison, R. Perry, A. Pearson, and J. Lunec. 2001. Novel ERBB4 juxtamembrane splice variants are frequently expressed in childhood medulloblastoma. Genes Chromosomes Cancer 31:288–294.
  • Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425–479.
  • Hynes, N. E., and H. A. Lane. 2005. ERBB receptors and cancer: the complexity of targeted inhibitors. Nat. Rev. Cancer 5:341–354.
  • Ingham, R. J., G. Gish, and T. Pawson. 2004. The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture. Oncogene 23:1972–1984.
  • Kainulainen, V., M. Sundvall, J. A. Maatta, E. Santiestevan, M. Klagsbrun, and K. Elenius. 2000. A natural ErbB4 isoform that does not activate phosphoinositide 3-kinase mediates proliferation but not survival or chemotaxis. J. Biol. Chem. 275:8641–8649.
  • Kaneki, H., R. Guo, D. Chen, Z. Yao, E. M. Schwarz, Y. E. Zhang, B. F. Boyce, and L. Xing. 2006. Tumor necrosis factor promotes Runx2 degradation through upregulation of Smurf1 and Smurf2 in osteoblasts. J. Biol. Chem. 281:4326–4333.
  • Knowlden, J. M., J. M. Gee, L. T. Seery, L. Farrow, W. J. Gullick, I. O. Ellis, R. W. Blamey, J. F. Robertson, and R. I. Nicholson. 1998. c-erbB3 and c-erbB4 expression is a feature of the endocrine responsive phenotype in clinical breast cancer. Oncogene 17:1949–1957.
  • Komuro, A., T. Imamura, M. Saitoh, Y. Yoshida, T. Yamori, K. Miyazono, and K. Miyazawa. 2004. Negative regulation of transforming growth factor-beta (TGF-β) signaling by WW domain-containing protein 1 (WWP1). Oncogene 23:6914–6923.
  • Komuro, A., M. Nagai, N. E. Navin, and M. Sudol. 2003. WW domain-containing protein YAP associates with ErbB-4 and acts as a co-transcriptional activator for the carboxyl-terminal fragment of ErbB-4 that translocates to the nucleus. J. Biol. Chem. 278:33334–33341.
  • Laine, A., and Z. Ronai. 2007. Regulation of p53 localization and transcription by the HECT domain E3 ligase WWP1. Oncogene 26:1477–1483.
  • Lee, H. J., K. M. Jung, Y. Z. Huang, L. B. Bennett, J. S. Lee, L. Mei, and T. W. Kim. 2002. Presenilin-dependent gamma-secretase-like intramembrane cleavage of ErbB4. J. Biol. Chem. 277:6318–6323.
  • Levkowitz, G., H. Waterman, E. Zamir, Z. Kam, S. Oved, W. Y. Langdon, L. Beguinot, B. Geiger, and Y. Yarden. 1998. c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor. Genes Dev. 12:3663–3674.
  • Lodge, A. J., J. J. Anderson, W. J. Gullick, B. Haugk, R. C. Leonard, and B. Angus. 2003. Type 1 growth factor receptor expression in node positive breast cancer: adverse prognostic significance of c-erbB-4. J. Clin. Pathol. 56:300–304.
  • Mahajan, N. P., Y. E. Whang, J. L. Mohler, and H. S. Earp. 2005. Activated tyrosine kinase Ack1 promotes prostate tumorigenesis: role of Ack1 in polyubiquitination of tumor suppressor Wwox. Cancer Res. 65:10514–10523.
  • Moren, A., T. Imamura, K. Miyazono, C. H. Heldin, and A. Moustakas. 2005. Degradation of the tumor suppressor Smad4 by WW and HECT domain ubiquitin ligases. J. Biol. Chem. 280:22115–22123.
  • Morin-Kensicki, E. M., B. N. Boone, M. Howell, J. R. Stonebraker, J. Teed, J. G. Alb, T. R. Magnuson, W. O'Neal, and S. L. Milgram. 2006. Defects in yolk sac vasculogenesis, chorioallantoic fusion, and embryonic axis elongation in mice with targeted disruption of Yap65. Mol. Cell. Biol. 26:77–87.
  • Muraoka-Cook, R. S., L. S. Caskey, M. A. Sandahl, D. M. Hunter, C. Husted, K. E. Strunk, C. I. Sartor, W. A. Rearick, Jr., W. McCall, M. K. Sgagias, K. H. Cowan, and H. S. Earp III. 2006. Heregulin-dependent delay in mitotic progression requires HER4 and BRCA1. Mol. Cell. Biol. 26:6412–6424.
  • Muraoka-Cook, R. S., N. Dumont, and C. L. Arteaga. 2005. Dual role of transforming growth factor beta in mammary tumorigenesis and metastatic progression. Clin. Cancer Res. 11:937s–943s.
  • Muraoka-Cook, R. S., M. Sandahl, C. Husted, D. Hunter, L. Miraglia, S. M. Feng, K. Elenius, and H. S. Earp III. 2006. The intracellular domain of ErbB4 induces differentiation of mammary epithelial cells. Mol. Biol. Cell 17:4118–4129.
  • Ni, C. Y., M. P. Murphy, T. E. Golde, and G. Carpenter. 2001. γ-Secretase cleavage and nuclear localization of ErbB-4 receptor tyrosine kinase. Science 294:2179–2181.
  • Ohta, T., and M. Fukuda. 2004. Ubiquitin and breast cancer. Oncogene 23:2079–2088.
  • Omerovic, J., L. Santangelo, E. M. Puggioni, J. Marrocco, C. Dall'Armi, C. Palumbo, F. Belleudi, L. Di Marcotullio, L. Frati, M. R. Torrisi, G. Cesareni, A. Gulino, and M. Alimandi. 2007. The E3 ligase Aip4/Itch ubiquitinates and targets ErbB-4 for degradation. FASEB J. 21:2849–2862.
  • Pawlowski, V., F. Revillion, M. Hebbar, L. Hornez, and J. P. Peyrat. 2000. Prognostic value of the type I growth factor receptors in a large series of human primary breast cancers quantified with a real-time reverse transcription-polymerase chain reaction assay. Clin. Cancer Res. 6:4217–4225.
  • Penington, D. J., I. Bryant, and D. J. Riese II. 2002. Constitutively active ErbB4 and ErbB2 mutants exhibit distinct biological activities. Cell Growth Differ. 13:247–256.
  • Qiu, X. B., and A. L. Goldberg. 2002. Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3. Proc. Natl. Acad. Sci. USA 99:14843-14848.
  • Rio, C., J. D. Buxbaum, J. J. Peschon, and G. Corfas. 2000. Tumor necrosis factor-alpha-converting enzyme is required for cleavage of erbB4/HER4. J. Biol. Chem. 275:10379–10387.
  • Roskoski, R., Jr. 2004. The ErbB/HER receptor protein-tyrosine kinases and cancer. Biochem. Biophys. Res. Commun. 319:1–11.
  • Sardi, S. P., J. Murtie, S. Koirala, B. A. Patten, and G. Corfas. 2006. Presenilin-dependent ErbB4 nuclear signaling regulates the timing of astrogenesis in the developing brain. Cell 127:185–197.
  • Sartor, C. I., H. Zhou, E. Kozlowska, K. Guttridge, E. Kawata, L. Caskey, J. Harrelson, N. Hynes, S. Ethier, B. Calvo, and H. S. Earp III. 2001. Her4 mediates ligand-dependent antiproliferative and differentiation responses in human breast cancer cells. Mol. Cell. Biol. 21:4265–4275.
  • Seo, S. R., F. Lallemand, N. Ferrand, M. Pessah, S. L'Hoste, J. Camonis, and A. Atfi. 2004. The novel E3 ubiquitin ligase Tiul1 associates with TGIF to target Smad2 for degradation. EMBO J. 23:3780–3792.
  • Shen, R., M. Chen, Y. J. Wang, H. Kaneki, L. Xing, J. O'Keefe, R., and D. Chen. 2006. Smad6 interacts with Runx2 and mediates Smad ubiquitin regulatory factor 1-induced Runx2 degradation. J. Biol. Chem. 281:3569–3576.
  • Srinivasan, R., C. E. Gillett, D. M. Barnes, and W. J. Gullick. 2000. Nuclear expression of the c-erbB-4/HER-4 growth factor receptor in invasive breast cancers. Cancer Res. 60:1483–1487.
  • Stern, D. F. 2003. ErbBs in mammary development. Exp. Cell Res. 284:89–98.
  • Strunk, K. E., C. Husted, L. C. Miraglia, M. Sandahl, W. A. Rearick, D. M. Hunter, H. S. Earp III, and R. S. Muraoka-Cook. 2007. HER4 d-box sequences regulate mitotic progression and degradation of the nuclear HER4 cleavage product s80HER4. Cancer Res. 67:6582–6590.
  • Sudol, M., H. I. Chen, C. Bougeret, A. Einbond, and P. Bork. 1995. Characterization of a novel protein-binding module: the WW domain. FEBS Lett. 369:67–71.
  • Sundvall, M., L. Peri, J. A. Maatta, D. Tvorogov, I. Paatero, M. Savisalo, O. Silvennoinen, Y. Yarden, and K. Elenius. 2007. Differential nuclear localization and kinase activity of alternative ErbB4 intracellular domains. Oncogene 26:6905–6914.
  • Suo, Z., B. Risberg, M. G. Kalsson, K. Willman, A. Tierens, E. Skovlund, and J. M. Nesland. 2002. EGFR family expression in breast carcinomas: c-erbB-2 and c-erbB-4 receptors have different effects on survival. J. Pathol. 196:17–25.
  • Tovey, S. M., C. J. Witton, J. M. Bartlett, P. D. Stanton, J. R. Reeves, and T. G. Cooke. 2004. Outcome and human epidermal growth factor receptor (HER) 1-4 status in invasive breast carcinomas with proliferation indices evaluated by bromodeoxyuridine labeling. Breast Cancer Res. 6:R246–R251.
  • Vecchi, M., J. Baulida, and G. Carpenter. 1996. Selective cleavage of the heregulin receptor ErbB-4 by protein kinase C activation. J. Biol. Chem. 271:18989–18995.
  • Vecchi, M., and G. Carpenter. 1997. Constitutive proteolysis of the ErbB-4 receptor tyrosine kinase by a unique, sequential mechanism. J. Cell Biol. 139:995–1003.
  • Wang, X., L. C. Trotman, T. Koppie, A. Alimonti, Z. Chen, Z. Gao, J. Wang, H. Erdjument-Bromage, P. Tempst, C. Cordon-Cardo, P. P. Pandolfi, and X. Jiang. 2007. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Cell 128:129–139.
  • Williams, C. C., J. G. Allison, G. A. Vidal, M. E. Burow, B. S. Beckman, L. Marrero, and F. E. Jones. 2004. The ERBB4/HER4 receptor tyrosine kinase regulates gene expression by functioning as a STAT5A nuclear chaperone. J. Cell Biol. 167:469–478.
  • Witton, C. J., J. R. Reeves, J. J. Going, T. G. Cooke, and J. M. Bartlett. 2003. Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer. J. Pathol. 200:290–297.
  • Xu, W., M. Marcu, X. Yuan, E. Mimnaugh, C. Patterson, and L. Neckers. 2002. Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu. Proc. Natl. Acad. Sci. USA 99:12847–12852.
  • Yokouchi, M., T. Kondo, A. Houghton, M. Bartkiewicz, W. C. Horne, H. Zhang, A. Yoshimura, and R. Baron. 1999. Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J. Biol. Chem. 274:31707–31712.
  • Zhao, M., M. Qiao, B. O. Oyajobi, G. R. Mundy, and D. Chen. 2003. E3 ubiquitin ligase Smurf1 mediates core-binding factor α1/Runx2 degradation and plays a specific role in osteoblast differentiation. J. Biol. Chem. 278:27939–27944.
  • Zhou, P., N. Fernandes, I. L. Dodge, A. L. Reddi, N. Rao, H. Safran, T. A. DiPetrillo, D. E. Wazer, V. Band, and H. Band. 2003. ErbB2 degradation mediated by the co-chaperone protein CHIP. J. Biol. Chem. 278:13829–13837.
  • Zhou, P., and P. M. Howley. 1998. Ubiquitination and degradation of the substrate recognition subunits of SCF ubiquitin-protein ligases. Mol. Cell 2:571–580.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.