Mechanisms of ErbB receptor negative regulation and relevance in cancer

Experimental Cell Research

Volumn 315, Issue 4, 2009, Pages 697-706

  Fry, William H D ^a   Kotelawala, Lakmal ^a   Sweeney, Colleen ^a   Carraway III, Kermit L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ErbB; Negative regulator; Receptor tyrosine kinase; Ubiquitin ligase

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR 2;

ANIMAL; CHEMICAL STRUCTURE; DOWN REGULATION; GENETICS; HUMAN; NEOPLASM; PATHOPHYSIOLOGY; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; DOWN-REGULATION; HUMANS; MODELS, MOLECULAR; NEOPLASMS; RECEPTOR, ERBB-2; SIGNAL TRANSDUCTION;

EID: 62649175431     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2008.07.022     Document Type: Review

References (98)

1. T. Holbro, N.E. Hynes, ErbB receptors: directing key signaling networks throughout life, Annu. Rv. Pharmacol. Toxicol. 44 (2004) 195-217.
2. J. Downward, Y. Yarden, E. Mayes, G. Scrace, N. Totty, P. Stockwell, A. Ullrich, J. Schlessinger, M.D. Waterfield, Close similarity of epidermal growth factor receptor and v-erb-B oncogene protein sequences, Nature 307 (1984) 521-527.
3. Y. Yarden, M.X. Sliwkowski, Untangling the ErbB signaling network, Nat. Rev. Mol. Cell Biol. 2 (2001) 127-137.
4. B. Linggi,G. Carpenter, ErbB receptors: newinsights onmechanisms and biology, Trends Cell Biol. 16 (2006) 649-656.
5. T.P. Garrett, N.M. McKern, M. Lou, T.C. Elleman, T.E. Adams, G.O. Lovrecz, M. Kofler, R.N. Jorissen, E.C. Nice, A.W. Burgess, C.W. Ward, The crystal structure of a truncated ErbB2 ectodomain reveals an active conformation, poised to interact with other ErbB receptors, Mol. Cell 11 (2003) 495-505.
6. D. Graus-Porta, R.R. Beerli, J.M. Daly, N.E. Hynes, ErbB-2, the preferred heterodimerization partner of all ErbB receptors is a mediator of lateral signaling, EMBO J. 16 (1997) 1647-1655.
7. M.D. Marmor, K.B. Skaria, Y. Yarden, Signal transduction and oncogenesis by ErbB/Her receptors, Int. J. Radiat. Oncol. Biol. Phys. 58 (2004) 903-913.
8. J.J. Herbst, L.K. Opresko, B.J.Walsh, D.A. Lauffenburger, H.S. Wiley, Regulation of postendocytic trafficking of the epidermal growth factor receptor through endosomal retention, J. Biol. Chem. 269 (1994) 12865-12873.
9. H.S. Wiley, Trafficking of the ErbB receptors and its influence on signaling, Exp. Cell Res. 284 (2003) 78-88.
10. S. Confalonieri, A.E. Salcini, C. Puri, C. Tacchetti, P.P. Di Fiore, Tyrosine phosphorylation of Eps15 is required for ligand-regulated, but not constitutive, endocytosis, J. Cell. Biol. 150 (2000) 905-912.
11. K. Haglund, S. Sigismund, S. Polo, I. Szymkiewicz, P.P. Di Fiore, I. Dikic, Multiple monoubiquitination of RTKs is sufficient for their endocytosis and degradation, Nat. Cell Biol. 5 (2003) 461-466.
12. Y. Mosesson, K. Shtiegman, M. Katz, Y. Zwang, G. Vereb, J. Szollosi, Y. Yarden, Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation, J. Biol. Chem. 278 (2003) 21323-21326.
13. F. Huang, L.K. Goh, A. Sorkin, EGF receptor ubiquitination is not necessary for its internalization, Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 16904-16909.
14. J. Baulida, M.H. Kraus, M. Alimandi, P.P. Di Fiore, G. Carpenter, All ErbB receptors other than the epidermal growth factor receptor are endocytosis impaired, J. Biol. Chem. 271 (1996) 5251-5257.
15. Z. Wang, L. Zhang, T.K. Yeung, X. Chen, Endocytosis deficiency of epidermal growth factor (EGF) receptor-ErbB2 heterodimers in response to EGF stimulation, Mol. Biol. Cell 10 (1999) 1621-1636.
16. C. Haslekas, K. Breen, K.W. Pedersen, L.E. Johannessen, E. Stang, I.H. Madshus, The inhibitory effect of ErbB2 on epidermal growth factor-induced formation of clathrin-coated pits correlates with retention of epidermal growth factor receptor-ErbB2 oligomeric complexes at the plasma membrane, Mol. Biol. Cell 16 (2005) 5832-5842.
17. B.S. Hendriks, H.S. Wiley, D. Lauffenburger, HER2-mediated effects on EGFR endosomal sorting: analysis of biophysical mechanisms, Biophys. J. 85 (4) (2003) 2732-2745.
18. C.D. Austin, A.M. De Maziere, P.I. Pisacane, S.M. van Dijk, C. Eigenbrot, M.X. Sliwkowski, J. Klumperman, R.H. Scheller, Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin, Mol. Biol. Cell 15 (2004) 5268-5282.
19. X.L. Yang, Y.Z. Huang, W.C. Xiong, L. Mei, Neuregulin-induced expression of the acetylcholine receptor requires endocytosis of ErbB receptors, Mol. Cell Neurosci. 28 (2005) 335-346.
20. P. Peschard, M. Park, Escape from Cbl-mediated downregulation: a recurrent theme for oncogenic deregulation of receptor tyrosine kinases, Cancer Cell 3 (2003) 519-523.
21. C.J. Witton, J.R. Reeves, J.J. Going, T.G. Cooke, J.M. Bartlett, Expression of the HER1-4 family of receptor tyrosine kinases in breast cancer, J. Pathol. 200 (2003) 290-297.
22. T. Holbro, G. Civenni, N.E. Hynes, The ErbB receptors and their role in cancer progression, Exp. Cell Res. 284 (2003) 99-110.
23. D.J. Slamon, G.M. Clark, S.G. Wong, W.J. Levin, A. Ullrich, W.L. McGuire, Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene, Science 235 (1987) 177-182.
24. D.J. Slamon, W. Godolphin, L.A. Jones, J.A. Holt, S.G. Wong, D.E. Keith, W.J. Levin, S.G. Stuart, J. Udove, A. Ullrich, Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer, Science 244 (1989) 707-712.
25. F.M. Yakes, W. Chinratanalab, C.A. Ritter, W. King, S. Seelig, C.L. Arteaga, Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, cyclin D1, and antitumor action, Cancer Res. 62 (2002) 4132-4141.
26. P.N. Munster, D.C. Marchion, A.D. Basso, N. Rosen, Degradation of HER2 by ansamycins induces growth arrest and apoptosis in cellswith HER2 overexpression via a HER3, phosphatidylinositol 3-kinase-AKT-dependent pathway, Cancer Res. 62 (2002) 3132-3137.
27. T. Holbro, R.R. Beerli, F. Maurer, M. Koziczak, C.F. Barbas III, N.E. Hynes, The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 8933-8938.
28. N.R. Lemoine, D.M. Barnes, D.P. Hollywood, C.M. Hughes, P. Smith, E. Dublin, S.A. Prigent, W.J. Gullick, H.C. Hurst, Expression of the ErbB3 gene product in breast cancer, Br. J. Cancer 66 (1992) 1116-1121.
29. R. Naidu, M. Yadav, S. Nair, M.K. Kutty, Expression of c-erbB3 protein in primary breast carcinomas, Br. J. Cancer 78 (1998) 1385-1390.
30. C.T. Guy, M.A. Webster, M. Schaller, T.J. Parsons, R.D. Cardiff, W.J. Muller, Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease, Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 10578-10582.
31. J.K. Miller, D.L. Shattuck, E.Q. Ingalla, L. Yen, A.D. Borowsky, L.J. Young, R.D. Cardiff, K.L. Carraway III, C. Sweeney. Suppression of the negative regulator LRIG1 contributes to ErbB2 overexpression in breast cancer. Cancer Res., in press.
32. K.L. Carraway III, L. Yen, E. Ingalla, C. Sweeney, Negative regulation of signaling by the EGFR family, in: J.D. Haley, W.J. Gullick (Eds.), Cancer Drug Discovery and Development: EGFR Signaling Networks in Cancer Therapy, Humana Press, Totowa, N.J., 2008
33. L. Yen, Z. Cao, X. Wu, E.R. Ingalla, C. Baron, L.J. Young, J.P. Gregg, R.D. Cardiff, A.D. Borowsky, C. Sweeney, K.L. Carraway III, Loss of Nrdp1 enhances ErbB2/ErbB3-dependent breast tumor cell growth, Cancer Res. 66 (2006) 11279-11286.
34. P.M. Siegel, E.D. Ryan, R.D. Cardiff,W.J. Muller, Elevated expression of activated forms of Neu/ErbB-2 and ErbB-3 are involved in the induction of mammary tumors in transgenic mice: implications for human breast cancer, EMBO J. 18 (1999) 2149-2164.
35. R. Nahta, D. Yu, M.C. Hung, G.N. Hortobagyi, F.J. Esteva, Mechanisms of disease: understanding resistance to HER2-targeted therapy in human breast cancer, Nat. Clin. Pract. Oncol. 3 (2006) 269-280.
36. N.V. Sergina, M. Rausch, D. Wang, J. Blair, B. Hann, K.M. Shokat, M.M. Moasser, Escape from HER-family tyrosine kinase inhibitor therapy by the kinase-inactive HER3, Nature 445 (2007) 437-441.
37. N. Perrimon, A.P. McMahon, Negative feedback mechanisms and their roles during pattern formation, Cell 97 (1999) 13-16.
38. M. Freeman, Feedback control of intercellular signalling in development, Nature 408 (2000) 313-319.
39. R. Schweitzer, R. Howes, R. Smith, B.Z. Shilo, M. Freeman, Inhibition of Drosophila EGF receptor activation by the secreted protein Argos, Nature 376 (1995) 699-702.
40. M.H. Jin, K. Sawamoto, M. Ito, H. Okano, The interaction between the Drosophila secreted protein argos and the epidermal growth factor receptor inhibits dimerization of the receptor and binding of secreted spitz to the receptor, Mol. Cell Biol. 20 (2000) 2098-2107.
41. J. Vinos, M. Freeman, Evidence that Argos is an antagonistic ligand of the EGF receptor, Oncogene 19 (2000) 3560-3562.
42. D.E. Klein, V.M. Nappi, G.T. Reeves, S.Y. Shvartsman, M.A. Lemmon, Argos inhibits epidermal growth factor receptor signalling by ligand sequestration, Nature 430 (2004) 1040-1044.
43. D. Alvarado, T.A. Evans, R. Sharma, M.A. Lemmon, J.B. Duffy, Argos mutants define an affinity threshold for spitz inhibition in vivo, J. Biol. Chem. 281 (2006) 28993-29001.
44. D.E. Klein, S.E. Stayrook, F. Shi, K. Narayan, M.A. Lemmon, Structural basis for EGFR ligand sequestration by Argos, Nature 453 (2008) 1271-1275.
45. C. Ghiglione, K.L. Carraway III, L.T. Amundadottir, R.E. Boswell, N. Perrimon, J.B. Duffy, The transmembrane molecule kekkon-1 acts in a feedback loop to negatively regulate the activity of the Drosophila EGF receptor during oogenesis, Cell 96 (1999) 847-856.
46. D. Alvarado, A.H. Rice, J.B. Duffy, Knockouts of Kekkon1 define sequence elements essential for Drosophila epidermal growth factor receptor inhibition, Genetics 166 (2004) 201-211.
47. C. Ghiglione, L. Amundadottir, M. Andresdottir, D. Bilder, J.A. Diamonti, S. Noselli, N. Perrimon, K.L. Carraway III, Mechanism of inhibition of the Drosophila and mammalian EGF receptors by the transmembrane protein Kekkon 1, Development 130 (2003) 4483-4493.
48. D. Alvarado, A.H. Rice, J.B. Duffy, Bipartite inhibition of Drosophila epidermal growth factor receptor by the extracellular and transmembrane domains of Kekkon1, Genetics 167 (2004) 187-202.
49. R.L. Williams, S. Urbe, The emerging shape of the ESCRT machinery, Nat. Rev. Mol. Cell Biol. 8 (2007) 355-368.
50. P.E. Row, I.A. Prior, J. McCullough, M.J. Clague, S. Urbe, The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor downregulation, J. Biol. Chem. 281 (2006) 12618-12624.
51. Y.M. Ma, E. Boucrot, J. Villen, B. Affar el, S.P. Gygi, H.G. Gottlinger, T. Kirchhausen, Targeting of AMSH to endosomes is required for epidermal growth factor receptor degradation, J. Biol. Chem. 282 (2006) 9805-9812.
52. W.Y. Langdon, J.W. Hartley, S.P. Klinken, S.K. Ruscetti, H.C. Morse III, v-cbl, an oncogene from a dual-recombinant murine retrovirus that induces early B-lineage lymphomas, Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 1168-1172.
53. G. Levkowitz, H. Waterman, E. Zamir, Z. Kam, S. Oved, W.Y. Langdon, L. Beguinot, B. Geiger, Y. Yarden, c-Cbl/Sli-1 regulates endocytic sorting and ubiquitination of the epidermal growth factor receptor, Genes Dev. 12 (1998) 3663-3674.
54. G. Levkowitz, H. Waterman, S.A. Ettenberg, M. Katz, A.Y. Tsygankov, I. Alroy, S. Lavi, K. Iwai, Y. Reiss, A. Ciechanover, S. Lipkowitz, Y. Yarden, Ubiquitin ligase activity and tyrosine phosphorylation underlie suppression of growth factor signaling by c-Cbl/Sli-1, Mol. Cell 4 (1999) 1029-1040.
55. H. Waterman, M. Katz, C. Rubin, K. Shtiegman, S. Lavi, A. Elson, T. Jovin, Y. Yarden, A mutant EGF-receptor defective in ubiquitylation and endocytosis unveils a role for Grb2 in negative signaling, EMBO J. 21 (2002) 303-313.
56. E. Kario, M.D. Marmor, K. Adamsky, A. Citri, I. Amit, N. Amariglio, G. Rechavi, Y. Yarden, Suppressors of cytokine signaling 4 and 5 regulate epidermal growth factor receptor signaling, J. Biol. Chem. 280 (2005) 7038-7048.
57. W.S. Alexander, D.J. Hilton, The role of suppressors of cytokine signaling (SOCS) proteins in regulation of the immune response, Annu. Rev. Immunol. 22 (2004) 503-529.
58. S.Wormald, D.J. Hilton, Inhibitors of cytokine signal transduction, J. Biol. Chem. 279 (2004) 821-824.
59. A.M. Hommelgaard, M. Lerdrup, B. van Deurs, Association with membrane protrusions makes ErbB2 an internalization-resistant receptor, Mol. Biol. Cell 4 (2004) 1557-1567.
60. W. Xu, M. Marcu, X. Yuan, E. Mimnaugh, C. Patterson, L. Neckers, Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu, Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 12847-12852.
61. L. Neckers, S.P. Ivy, Heat shock protein 90, Curr. Opin. Oncol. 15 (2003) 419-424.
62. S. Modi, A.T. Stopeck, M.S. Gordon, D. Mendelson, D.B. Solit, R. Bagatell,W. Ma, J.Wheler, N. Rosen, L. Norton, G.F. Cropp, R.G. Johnson, A.L. Hannah, C.A. Hudis, Combination of trastuzumab and tanespimycin (17-AAG, KOS-953) is safe and active in trastuzumab-refractory HER-2-overexpressing breast cancer: a phase I dose-escalation study, J. Clin. Oncol. 25 (2007) 5410-5417.
63. W. Xu, X. Yuan, K. Beebe, Z. Xiang, L. Neckers, Loss of Hsp90 association up-regulates Src-dependent ErbB2 activity, Mol. Cell Biol. 27 (2007) 220-228.
64. J. Nie, M.A. McGill, M. Dermer, S.E. Dho, C.D.Wolting, C.J. McGlade, LNX functions as a RING type E3 ubiquitin ligase that targets thecell fate determinant Numb for ubiquitin-dependent degradation, EMBO J. 21 (2002) 93-102.
65. P. Young, J. Nie, X.Wang, C.J. McGlade, M.M. Rich, G. Feng, LNX1 is a perisynaptic Schwann cell specific E3 ubiquitin ligase that interacts with ErbB2, Mol. Cell Neurosci. 2 (2005) 238-248.
66. J. Chen, J. Xu, W. Zhao, G. Hu, H. Cheng, Y. Kang, Y. Xie, Y. Lu, Characterization of human LNX, a novel ligand of Numb protein X that is downregulated in human gliomas, Int. J. Biochem. Cell Biol. 37 (2005) 2273-2283.
67. A.J. Diamonti, P.M. Guy, C. Ivanof, K. Wong, C. Sweeney, K.L. Carraway III, An RBCC protein implicated in maintenance of steady-state neuregulin receptor levels, Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 2866-2871.
68. X.B. Qiu, A.L. Goldberg, Nrdp1/FLRF is a ubiquitin ligase promoting ubiquitination and degradation of the epidermal growth factor receptor family member, ErbB3, Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 14843-14848.
69. X. Wu, L. Yen, L. Irwin, C. Sweeney, K.L. Carraway III, Stabilization of the E3 ubiquitin ligase Nrdp1 by the deubiquitinating enzyme USP8, Mol. Cell Biol. 24 (2004) 7748-7757.
70. Z. Cao, X. Wu, L. Yen, C. Sweeney, K.L. Carraway III, Neuregulininduced ErbB3 downregulation is mediated by a protein stability cascade involving the E3 ubiquitin ligase Nrdp1, Mol. Cell Biol. 27 (2007) 2180-2188.
71. J.K. Doherty, C. Bond, A. Jardim, J.P. Adelman, G.M. Clinton, The HER-2/neu receptor tyrosine kinase gene encodes a secreted autoinhibitor, Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 10869-10874.
72. N.G. Azios, F.J. Romero, M.C. Denton, J.K. Doherty, G.M. Clinton, 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 (2001) 5199-5209.
73. P. Hu, T. Zhou, L. Qian, J. Wang, M. Shi, M. Yu, Y. Yang, X. Zhang, B. Shen, N. Guo, Sequestering ErbB2 in endoplasmic reticulum by its autoinhibitor from translocation to cell surface: an autoinhibition mechanism of ErbB2 expression, Biochem. Biophys. Res. Commun. 342 (2006) 19-27.
74. Q.A. Justman, G.M. Clinton, Herstatin, an autoinhibitor of the human epidermal growth factor receptor 2 tyrosine kinase, modulates epidermal growth factor signaling pathways resulting in growth arrest, J. Biol. Chem. 277 (2002) 20618-20624.
75. F. Jhabvala-Romero, A. Evans, S. Guo, M. Denton, G.M. Clinton, Herstatin inhibits heregulin-mediated breast cancer cell growth and overcomes tamoxifen resistance in breast cancer cells that overexpress HER-2, Oncogene 22 (2003) 8178-8186.
76. J.A. Staverosky, L.L. Muldoon, S. Guo, A.J. Evans, E.A. Neuwelt, G.M. Clinton, Herstatin, an autoinhibitor of the epidermal growth factor receptor family, blocks the intracranial growth of glioblastoma, Clin. Cancer Res. 11 (2005) 335-340.
77. Y. Yu, A.K. Rishi, J.R. Turner, D. Liu, E.D. Black, J.A. Moshier, A.P. Majumdar, Cloning of a novel EGFR-related peptide: a putative negative regulator of EGFR, Am. J. Physiol. Cell Physiol. 280 (2001) 1083-1089.
78. H. Xu, Y. Yu, D. Marciniak, A.K. Rishi, F.H. Sarkar, O. Kucuk, A.P. Majumdar, Epidermal growth factor receptor (EGFR)-related protein inhibits multiple members of the EGFR family in colon and breast cancer cells, Mol. Cancer Ther. 4 (2005) 435-442.
79. J.L. Reiter, N.J. Maihle, G.M. Clinton, Therapeutic potential of epidermal growth factor receptor-related protein, Mol. Cancer Ther. 5 (2006) 2954.
80. H. Lee, R.W. Akita, M.X. Sliwkowski, N.J. Maihle, A naturally occurring secreted human ErbB3 receptor isoform inhibits heregulin-stimulated activation of ErbB2, ErbB3, and ErbB4, Cancer Res. 61 (2001) 4467-4473.
81. L. Fiorentino, C. Pertica, M. Fiorini, C. Talora, M. Crescenzi, L. Castellani, S. Alema, P. Benedetti, O. Segatto, Inhibition of ErbB-2 mitogenic and transforming activity by RALT, a mitogen-induced signal transducer which binds to the ErbB-2 kinase domain, Mol. Cell Biol. 20 (2000) 7735-7750.
82. S. Anastasi, L. Fiorentino, M. Fiorini, R. Fraioli, G. Sala, L. Castellani, S. Alema, M. Alimandi, O. Segatto, Feedback inhibition by RALT controls signal output by the ErbB network, Oncogene 22 (2003) 4221-4234.
83. X. Zhang, K.A. Pickin, R. Bose, N. Jura, P.A. Cole, J. Kuriyan, Inhibition of the EGF receptor by binding of MIG6 to an activating kinase domain interface, Nature 450 (2007) 741-744.
84. C. Ballaro, S. Ceccarelli, C. Tiveron, L. Tatangelo, A.M. Salvatore, O. Segatto, S. Alema, Targeted expression of RALT in mouse skin inhibits epidermal growth factor receptor signalling and generates a Waved-like phenotype, EMBO. Rep. 6 (2005) 755-761.
85. I. Ferby, M. Reschke, O. Kudlacek, P. Knyazev, G. Pante, K. Amann, W. Sommergruber, N. Kraut, A. Ullrich, R. Fassler, R. Klein, Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumor formation, Nature Med. 12 (2006) 568-573.
86. Y.W. Zhang, B. Staal, Y. Su, P. Swiatek, P. Zhao, B. Cao, J. Resau, R. Sigler, R. Bronson, G.F. Vande Woude, Evidence that MIG-6 is a tumor-suppressor gene, Oncogene 26 (2007) 269-276.
87. M. Santra, C.C. Reed, R.V. Iozzo, Decorin binds to a narrow region of the epidermal growth factor (EGF) receptor, partially overlapping but distinct from the EGF-binding epitope, J. Biol. Chem. 277 (2002) 35671-35681.
88. J.X. Zhu, S. Goldoni, G. Bix, R.T. Owens, D.J. McQuillan, C.C. Reed, R.V. Iozzo, Decorin evokes protracted internalization and degradation of the epidermal growth factor receptor via caveolar endocytosis, J. Biol. Chem. 280 (37) (2005) 32468-32479.
89. C.C. Reed, A. Waterhouse, S. Kirby, P. Kay, R.T. Owens, D.J. McQuillan, R.V. Iozzo, Decorin prevents metastatic spreading of breast cancer, Oncogene 24 (2005) 1104-1110.
90. J. Nilsson, C. Vallbo, D. Guo, I. Golovleva, B. Hallberg, R. Henriksson, H. Hedman, Cloning, characterization, and expression of human LIG1, Biochem. Biophys. Res. Commun. 284 (2001) 1155-1161.
91. J. Nilsson, A. Starefeldt, R. Henriksson, H. Hedman, LRIG1 protein in human cells and tissues, Cell Tissue Res. 312 (2003) 65-71.
92. H. Hedman, J. Nilsson, D. Guo, R. Henriksson, Is LRIG1 a tumour suppressor gene at chromosome 3p14.3? Acta. Oncol. 41 (2002) 352-354.
93. Y. Suzuki, H. Miura, A. Tanemura, K. Kobayashi, G. Kondoh, S. Sano, K. Ozawa, S. Inui, A. Nakata, T. Takagi, M. Tohyama, K. Yoshikawa, S. Itami, Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia, FEBS. Lett. 521 (2002) 67-71.
94. R. Vassar, E. Fuchs, Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation, Genes Dev. 5 (1991) 714-727.
95. P.W. Cook, M. Piepkorn, C.H. Clegg, G.D. Plowman, J.M. DeMay, J.R. Brown, M.R. Pittelkow, Transgenic expression of the human amphiregulin gene induces a psoriasis-like phenotype, J. Clin. Invest. 100 (1997) 2286-2294.
96. G. Gur, C. Rubin, M. Katz, I. Amit, A. Citri, J. Nilsson, N. Amariglio, R. Henriksson, G. Rechavi, H. Hedman, R. Wides, Y. Yarden, LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation, EMBO. J. 23 (2004) 3270-3281.
97. M.B. Laederich, M. Funes-Duran, L. Yen, E. Ingalla, X. Wu, K.L. Carraway III, C. Sweeney, The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases, J. Biol. Chem. 279 (2004) 47050-47056.
98. S. Goldoni, R.A. Iozzo, P. Kay, S. Campbell, A. McQuillan, C. Agnew, J.X. Zhu, D.R. Keene, C.C. Reed, R.V. Iozzo, A soluble ectodomain of LRIG1 inhibits cancer cell growth by attenuating basal and ligand-dependent EGFR activity, Oncogene 26 (2007) 368-381.