Transformation of polarized epithelial cells by apical mistrafficking of epiregulin

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 22, 2013, Pages 8960-8965

  Singh, Bhuminder ^a,b   Bogatcheva, Galina ^a,b   Washington, Mary Kay ^c   Coffey, Robert J ^a,b,c  

^a Cell and Developmental Biology   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Epithelial transformation; Growth factor trafficking; Protein sorting; Receptor tyrosine kinase

Indexed keywords

ADAPTOR PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIREGULIN; TYROSINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL MEMBRANE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURFACE; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM CELL; MALIGNANT TRANSFORMATION; MDCK CELL; MOUSE; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PROTEIN TRANSPORT; TUMOR INVASION; UBIQUITINATION; WILD TYPE;

EPITHELIAL TRANSFORMATION; GROWTH FACTOR TRAFFICKING; PROTEIN SORTING; RECEPTOR TYROSINE KINASE;

ANIMALS; CELL POLARITY; CELL TRANSFORMATION, NEOPLASTIC; DOGS; ELECTRIC IMPEDANCE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EPIDERMAL GROWTH FACTOR; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MADIN DARBY CANINE KIDNEY CELLS; MICE; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

MUS MUSCULUS;

EID: 84878431509     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1305508110     Document Type: Article

References (40)

1. Playford RJ, et al. (1996) The epidermal growth factor receptor (EGF-R) is present on the basolateral, but not the apical, surface of enterocytes in the human gastrointestinal tract. Gut 39(2):262-266.
2. Harris RC, Chung E, Coffey RJ (2003) EGF receptor ligands. Exp Cell Res 284(1):2-13.
3. Brown CL, Coffey RJ, Dempsey PJ (2001) The proamphiregulin cytoplasmic domain is required for basolateral sorting, but is not essential for constitutive or stimulus-induced processing in polarized Madin-Darby canine kidney cells. J Biol Chem 276(31): 29538-29549.
4. Coffey RJ, Jr., et al. (1994) Acceleration of mammary neoplasia in transforming growth factor alpha transgenic mice by 7,12-dimethylbenzanthracene. Cancer Res 54(7):1678-1683.
5. Dempsey PJ, Meise KS, Yoshitake Y, Nishikawa K, Coffey RJ (1997) Apical enrichment of human EGF precursor in Madin-Darby canine kidney cells involves preferential basolateral ectodomain cleavage sensitive to a metalloprotease inhibitor. J Cell Biol 138(4):747-758.
6. Dempsey PJ, Meise KS, Coffey RJ (2003) Basolateral sorting of transforming growth factor-alpha precursor in polarized epithelial cells: Characterization of cytoplasmic domain determinants. Exp Cell Res 285(2):159-174.
7. Li C, et al. (2004) Myristoylated Naked2 escorts transforming growth factor alpha to the basolateral plasma membrane of polarized epithelial cells. Proc Natl Acad Sci USA 101(15):5571-5576.
8. Gephart JD, et al. (2011) Identification of a novel mono-leucine basolateral sorting motif within the cytoplasmic domain of amphiregulin. Traffic 12(12):1793-1804.
9. Groenestege WM, et al. (2007) Impaired basolateral sorting of pro-EGF causes isolated recessive renal hypomagnesemia. J Clin Invest 117(8):2260-2267.
10. Komurasaki T, Toyoda H, Uchida D, Morimoto S (1997) Epiregulin binds to epidermal growth factor receptor and ErbB-4 and induces tyrosine phosphorylation of epidermal growth factor receptor, ErbB-2, ErbB-3 and ErbB-4. Oncogene 15(23):2841-2848.
11. Sahin U, et al. (2004) Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J Cell Biol 164(5):769-779.
12. Park J-Y, et al. (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303(5658):682-684.
13. Song H, Lim H, Das SK, Paria BC, Dey SK (2000) Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol 14(8):1147-1161.
14. Toyoda H, Komurasaki T, Uchida D, Morimoto S (1997) Distribution of mRNA for human epiregulin, a differentially expressed member of the epidermal growth factor family. Biochem J 326(Pt 1):69-75.
15. Thøgersen VB, et al. (2001) A subclass of HER1 ligands are prognostic markers for survival in bladder cancer patients. Cancer Res 61(16):6227-6233.
16. Shigeishi H, et al. (2008) Expression of epiregulin, a novel epidermal growth factor ligand associated with prognosis in human oral squamous cell carcinomas. Oncol Rep 19(6):1557-1564.
17. Baba I, et al. (2000) Involvement of deregulated epiregulin expression in tumorigenesis in vivo through activated Ki-Ras signaling pathway in human colon cancer cells. Cancer Res 60(24):6886-6889.
18. Khambata-Ford S, et al. (2007) Expression of epiregulin and amphiregulin and K-ras mutation status predict disease control in metastatic colorectal cancer patients treated with cetuximab. J Clin Oncol 25(22):3230-3237.
19. Jacobs B, et al. (2009) Amphiregulin and epiregulin mRNA expression in primary tumors predicts outcome in metastatic colorectal cancer treated with cetuximab. J Clin Oncol 27(30):5068-5074.
20. Gupta GP, et al. (2007) Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 446(7137):765-770.
21. Scheiffele P, Peränen J, Simons K (1995) N-glycans as apical sorting signals in epithelial cells. Nature 378(6552):96-98.
22. Yeaman C, et al. (1997) The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J Cell Biol 139(4):929-940.
23. Bonifacino JS, Dell'Angelica EC (1999) Molecular bases for the recognition of tyrosinebased sorting signals. J Cell Biol 145(5):923-926.
24. Fölsch H, Ohno H, Bonifacino JS, Mellman I (1999) A novel clathrin adaptor complex mediates basolateral targeting in polarized epithelial cells. Cell 99(2):189-198.
25. Gravotta D, et al. (2007) AP1B sorts basolateral proteins in recycling and biosynthetic routes of MDCK cells. Proc Natl Acad Sci USA 104(5):1564-1569.
26. Carvajal-Gonzalez JM, et al. (2012) Basolateral sorting of the coxsackie and adenovirus receptor through interaction of a canonical YXXPhi motif with the clathrin adaptors AP-1A and AP-1B. Proc Natl Acad Sci USA 109(10):3820-3825.
27. Simmen T, Höning S, Icking A, Tikkanen R, Hunziker W (2002) AP-4 binds basolateral signals and participates in basolateral sorting in epithelial MDCK cells. Nat Cell Biol 4(2):154-159.
28. Vermeer PD, et al. (2003) Segregation of receptor and ligand regulates activation of epithelial growth factor receptor. Nature 422(6929):322-326.
29. Rodriguez-Boulan E, Nelson WJ (1989) Morphogenesis of the polarized epithelial cell phenotype. Science 245(4919):718-725.
30. Mohapatra B, et al. (2013) Protein tyrosine kinase regulation by ubiquitination: Critical roles of Cbl-family ubiquitin ligases. Biochim Biophys Acta 1833(1):122-139.
31. Fry WH, Kotelawala L, Sweeney C, Carraway KL, 3rd (2009) Mechanisms of ErbB receptor negative regulation and relevance in cancer. Exp Cell Res 315(4): 697-706.
32. Tomic S, et al. (1995) Association of SH2 domain protein tyrosine phosphatases with the epidermal growth factor receptor in human tumor cells: Phosphatidic acid activates receptor dephosphorylation by PTP1C. J Biol Chem 270(36):21277-21284.
33. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5):646-674.
34. Gerl MJ, et al. (2012) Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol 196(2):213-221.
35. Threadgill DW, et al. (1995) Targeted disruption of mouse EGF receptor: Effect of genetic background on mutant phenotype. Science 269(5221):230-234.
36. Citri A, Yarden Y (2006) EGF-ERBB signalling: Towards the systems level. Nat Rev Mol Cell Biol 7(7):505-516.
37. Powell AE, et al. (2012) The pan-ErbB negative regulator Lrig1 is an intestinal stem cell marker that functions as a tumor suppressor. Cell 149(1):146-158.
38. Dempsey PJ, Coffey RJ (1994) Basolateral targeting and efficient consumption of transforming growth factor-alpha when expressed in Madin-Darby canine kidney cells. J Biol Chem 269(24):16878-16889.
39. Memorial Sloan Kettering Cancer Center (2013) cBio Cancer Genomics Portal: Tumor samples TCGA-D3-A2JF, TCGA-EE-A20C, and TCGA-D1-A17Q (TCGA provisional). Available at http://www.cbioportal.org. Accessed March 15, 2013.
40. Utepbergenov DI, Fanning AS, Anderson JM (2006) Dimerization of the scaffolding protein ZO-1 through the second PDZ domain. J Biol Chem 281(34):24671-24677.