Soluble E-cadherin: A critical oncogene modulating receptor tyrosine kinases, MAPK and PI3K/Akt/mTOR signaling

Oncogene

Volumn 33, Issue 2, 2014, Pages 225-235

  Brouxhon, S M ^a   Kyrkanides, S ^a   Teng, X ^a   Athar, M ^b   Ghazizadeh, S ^a   Simon, M ^a   O'banion, M K ^a   Ma, L ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

HER ErbB receptors; IGF 1R; oncogenecity; soluble E cadherin; squamous cell carcinomas; UV irradiation

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; GELATINASE A; GELATINASE B; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SOLUBLE E CADHERIN; SOMATOMEDIN C; UNCLASSIFIED DRUG; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GROWTH; CELL MOTILITY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN CARCINOGENESIS; SKIN CARCINOMA; TUMOR INVASION;

ANIMALS; CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, IGF TYPE 1; SKIN NEOPLASMS; TOR SERINE-THREONINE KINASES;

EID: 84891906452     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.563     Document Type: Article

References (47)

1. Gamallo C, Palacios J, Suarez A, Pizarro A, Navarro P, Quintanilla M et al. Correlation of E-cadherin expression with differentiation grade and histological type in breast carcinoma. Am J Pathol 1993; 142: 987-993
2. Mayer B, Johnson JP, Leitl F, Jauch KW, Heiss MM, Schildberg FW et al. E-cadherin expression in primary and metastatic gastric cancer: Down-regulation correlates with cellular dedifferentiation and glandular disintegration. Cancer Res 1993; 53: 1690-1695
3. Brouxhon S, Kyrkanides S, O'Banion MK, Johnson R, Pearce DA, Centola GM et al. Sequential down-regulation of E-cadherin with squamous cell carcinoma progression: Loss of E-cadherin via a prostaglandin E2-EP2 dependent posttranslational mechanism. Cancer Res 2007; 67: 7654-7664
4. Cavallaro U, Christofori G. Cell adhesion and signaling by cadherins and Ig-CAMs in cancer. Nat Rev Cancer 2004; 4: 118-132
5. Margulis A, Zhang W, Alt-Holland A, Crawford HC, Fusenig NE, Garlick JA. E-cadherin suppression accelerates squamous cell carcinoma progression in three-dimensional, human tissue constructs. Cancer Res 2005; 65: 1783-1791
6. Maretzky T, Reiss K, Ludwig A, Buchholz J, Scholz F, Proksch E et al. ADAM10 mediates E-cadherin shedding and regulates epithelial cell-cell adhesion, migration, and beta-catenin translocation. Proc Natl Acad Sci USA 2005; 102: 9182-9187
7. Kuefer R, Hofer MD, Gschwend JE, Pienta KJ, Sanda MG, Chinnajyan AM et al. The role of an 80 kDa fragment of E-cadherin in the metastatic progression of prostate cancer. Clin Cancer Res 2003; 9: 6447-6452
8. Chan AO, Chu KM, Lam SK, Wong BC, Kwok KF, Law S et al. Soluble E-cadherin is an independent pretherapeutic factor for long-Term survival in gastric cancer. J Clin Oncol 2003; 21: 2288-2293
9. Katayama M, Hirai S, Kamihagi K, Nakagawa K, Yasumoto M, Kato I. Soluble E-cadherin fragments increased in circulation of cancer patients. Br J Cancer 1994; 69: 580-585
10. Davies G, Jiang WG, Mason MD. Matrilysin mediates extracellular cleavage of E-cadherin from prostate cancer cells: A key mechanism in hepatocyte growth factor/scatter factor-induced cell-cell dissociation and in vitro invasion. Clin Cancer Res 2001; 7: 3289-3297
11. Nawrocki-Raby B, Gilles C, Polette M, Bruyneel E, Laronze JY, Bonnet N et al. Upregulation of MMPs by soluble E-cadherin in human lung tumor cells. Int J Cancer 2003; 105: 790-795
12. Symowicz J, Adley BP, Gleason KJ, Johnson JJ, Ghosh S, Fishman DA et al. Engagement of collagen-binding integrins promotes matrix metalloproteinase-9- dependent E-cadherin ectodomain shedding in ovarian carcinoma cells. Cancer Res 2007; 67: 2030-2039
13. Bol D, Kiguchi K, Gimenez-Conti I, Rupp T, DiGiovanni J. Overexpression of insulinlike growth factor-1 induces hyperplasia, dermal abnormalities, and spontaneous tumor formation in transgenic mice. Oncogene 1997; 14: 1725-1734
14. El-Abaseri TB, Putta S, Hansen LA. Ultraviolet irradiation induces keratinocyte proliferation and epidermal hyperplasia through the activation of the epidermal growth factor receptor. Carcinogenesis 2006; 27: 225-231
15. Madson JG, Hansen LA. Multiple mechanisms of Erbb2 action after ultraviolet irradiation of the skin. Mol Carcinog 2007; 4: 624-628
16. Wan YS, Wang ZQ, Shao Y, Voorhees JJ, Fisher GJ. Ultraviolet irradiation activates PI 3-kinase/AKT survival pathway via EGF receptors in human skin in vivo. Int J Oncol 2001; 18: 461-466
17. Wilker E, Lu J, Rho O, Carbajal S, Beltrán L, DiGiovanni J. Role of PI3K/Akt signaling in insulin-like growth factor-1 (IGF-1) skin tumor promotion. Mol Carcinog 2005; 44: 137-145
18. Hynes NE, Lane HA. ERBB receptors and cancer: The complexity of targeted inhibitors. Nat Rev Cancer 2005; 5: 341-354
19. Dlugosz AA, Hansen L, Cheng C, Alexander N, Denning MF, Threadgill DW et al. Targeted disruption of the epidermal growth factor receptor impairs growth of squamous papillomas expressing the v-ras(Ha) oncogene but does not block in vitro keratinocyte responses to oncogenic ras. Cancer Res 1997; 57: 3180-3188
20. El-Abaseri TB, Fuhrman J, Trempus C, Shendrik I, Tennant RW, Hansen LA. Chemoprevention of UV light-induced skin tumorigenesis by inhibition of the epidermal growth factor receptor. Cancer Res 2005; 65: 3958-3965
21. Vassar R, Fuchs E. Transgenic mice provide new insights into the role of TGF-Alpha during epidermal development and differentiation. Genes Dev 1991; 5: 714-727
22. Bol D, Kiguchi K, Beltrán L, Rupp T, Moats S, Gimenez-Conti I et al. Severe follicular hyperplasia and spontaneous papilloma formation in transgenic mice expressing the neu oncogene under the control of the bovine keratin 5 promoter. Mol Carcinog 1998; 21: 2-12
23. DiGiovanni J, Bol DK, Wilker E, Beltrán L, Carbajal S, Moats S et al. Constitutive expression of insulin-like growth factor-1 in epidermal basal cells of transgenic mice leads to spontaneous tumor promotion. Cancer Res 2000; 60: 1561-1570
24. Galer CE, Corey CL, Wang Z, Younes MN, Gomez-Rivera F, Jasser SA et al. Dual inhibition of epidermal growth factor receptor and insulin-like growth factor receptor I: Reduction of angiogenesis and tumor growth in cutaneous squamous cell carcinoma. Head Neck 2011; 33: 189-198
25. Najy AJ, Day KC, Day ML. The ectodomain shedding of E-cadherin by ADAM15 supports ErbB receptor activation. J Biol Chem 2008; 283: 18393-18401
26. Inge LJ, Barwe SP, D'Ambrosio J, Gopal J, Lu K, Ryazantsev S et al. Soluble E-cadherin promotes cell survival by activating epidermal growth factor receptor. Exp Cell Res 2011; 317: 838-848
27. Kim AL, Athar M, Bickers DR, Gautier J. Stage-specific alterations of cyclin expression during UVB-induced murine skin tumor development. Photochem Photobiol 2002; 75: 58-67
28. Moll R, Mitze M, Frixen UH, Birchmeier W. Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol 1993; 143: 1731-1742
29. Takeichi M. Cadherins in cancer: Implications for invasion and metastasis. Curr Opin Cell Biol 1993; 5: 806-811
30. Batistatou A, Charalabopoulos AK, Scopa CD, Nakanishi Y, Kappas A, Hirohashi S et al. Expression patterns of dysadherin and E-cadherin in lymph node metastases of colorectal carcinoma. Virchows Arch 2006; 448: 763-767
31. Bongiorno PF, al-Kasspooles M, Lee SW, Rachwal WJ, Moore JH, Whyte RI et al. E-cadherin expression in primary and metastatic thoracic neoplasms and in Barrett's oesophagus. Br J Cancer 1995; 71: 166-172
32. Saha B, Chaiwun B, Imam SS, Tsao-Wei DD, Groshen S, Naritoku WY et al. Overexpression of E-cadherin protein in metastatic breast cancer cells in bone. Anticancer Res 2007; 27: 3903-3908
33. Yang J, Dai DQ. A comparative study of E-cadherin mRNA expression in primary tumors and metastatic foci of gastric cancer. Zhonghua Zhong Liu Za Zhi 2005; 27: 25-28
34. Fujii K, Furukawa F, Matsuyoshi N. Ligand activation of overexpressed epidermal growth factor receptor results in colony dissociation and disturbed E-cadherin function in HSC-1 human cutaneous squamous carcinoma cells. Exp Cell Res 1996; 223: 50-62
35. Hazan RB, Norton L. The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J Biol Chem 1998; 273: 9078-9084
36. Wilding J, Vousden KH, Soutter WP, McCrea PD, Del Buono R, Pignatelli M. E-cadherin transfection down-regulates the epidermal growth factor receptor and reverses the invasive phenotype of human papilloma virus-Transfected keratinocytes. Cancer Res 1996; 56: 5285-5292
37. Nahta R, Yuan LX, Zhang B, Kobayashi R, Esteva FJ. Insulin-like growth factor-I receptor/human epidermal growth factor receptor 2 heterodimerization contributes to trastuzumab resistance of breast cancer cells. Cancer Res 2005; 65: 11118-11128
38. Higgins MJ, Baselga J. Targeted therapies for breast cancer. J Clin Invest 2011; 121: 3797-3803
39. Bjornsti MA, Houghton PJ. The TOR pathway: A target for cancer therapy. Nat Rev Cancer 2004; 4: 335-348
40. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev 2004; 18: 1926-1945
41. Esch TR, Jonsson MV, Levanos VA, Poveromo JD, Sorkin BC. Leukocytes infiltrating the submandibular glands of NOD mice express E-cadherin. J Autoimmun 2000; 15: 387-393
42. Fong KP, Barry C, Tran AN, Traxler EA, Wannemacher KM, Tang HY. Deciphering the human platelet sheddome. Blood 2011; 117: E15-e26
43. Uchida Y, Kawai K, Ibusuki A, Kanekura T. Role for E-cadherin as an inhibitory receptor on epidermal gamma delta T cells. J Immunol 2011; 186: 6945-6954
44. Van den Bossche J, Malissen B, Mantovani A, De Baetselier P, Van Ginderachter JA. Regulation and function of the E-cadherin/catenin complex in cells of the monocyte-macrophage lineage and DCs. Blood 2012; 119: 1623-1633
45. Maretzky T, Scholz F, KÖ ten B, Proksch E, Saftig P, Reiss K. ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J Invest Dermatol 2008; 128: 1737-1746
46. Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 1975; 6: 331-344
47. Kyrkanides S, Miller JH, Tallents R, Brouxhon S, Centola G, Olschowka J. Intraperitoneal inoculation of Sandhoff mouse neonates with an HIV-1 based lentiviral vector exacerbates the attendant neuroinflammation and disease phenotype. J Neuroimmunol 2007; 188: 39-47