Soluble-E-cadherin activates HER and IAP family members in HER2+ and TNBC human breast cancers

Molecular Carcinogenesis

Volumn 53, Issue 11, 2014, Pages 893-906

  Brouxhon, Sabine M ^a   Kyrkanides, Stephanos ^b   Teng, Xiaofei ^a   O'Banion, M Kerry ^c   Clarke, Robert ^d   Byers, Stephen ^d   Ma, Li ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^d GEORGETOWN UNIVERSITY   (United States)

Author keywords

Akt; HER1 4; IAPs; MTOR; PI3K; SEcad

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; EPIDERMAL GROWTH FACTOR RECEPTOR 4; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; UVOMORULIN; CADHERIN; EGFR PROTEIN, HUMAN; ERBB2 PROTEIN, HUMAN; ERBB3 PROTEIN, HUMAN; MTOR PROTEIN, HUMAN; PROTEIN KINASE B; TARGET OF RAPAMYCIN KINASE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CARCINOGENESIS; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN EPIDERMAL GROWTH FACTOR RECEPTOR 2 POSITIVE BREAST CANCER; HUMAN TISSUE; LIMIT OF QUANTITATION; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRIPLE NEGATIVE BREAST CANCER; TUMOR GROWTH; TUMOR INVASION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL MOTION; DRUG EFFECTS; FEMALE; MCF 7 CELL LINE; METABOLISM; MIDDLE AGED; MOLECULARLY TARGETED THERAPY; PATHOLOGY; TRIPLE NEGATIVE BREAST NEOPLASMS; TUMOR CELL LINE;

AGED; ANIMALS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FEMALE; HUMANS; MCF-7 CELLS; MICE; MIDDLE AGED; MOLECULAR TARGETED THERAPY; NEOPLASM INVASIVENESS; PHOSPHATIDYLINOSITOL 3-KINASE; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTOR, ERBB-2; RECEPTOR, ERBB-3; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TRIPLE NEGATIVE BREAST NEOPLASMS;

EID: 84907951215     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.22048     Document Type: Article

References (49)

1. Berx G, Van Roy F. The E-cadherin/catenin complex: An important gatekeeper in breast cancer tumorigenesis and malignant progression. Cancer Res 2001; 3:289-293.
2. Maretzky T, Reiss K, Ludwig A, 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.
3. 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.
4. 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.
5. Noë V, Fingleton B, Jacobs K, et al. Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 2001; 114:111-118.
6. Symowicz J, Adley BP, Gleason KJ, 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.
7. Kuefer R, Hofer MD, Gschwend JE, et al. The role of an 80kDa fragment of E-cadherin in the metastatic progression of prostate cancer. Clin Cancer Res 2003; 9:6447-6452.
8. Hofmann G, Dandachi N, Balic M, et al. Quantitative measurement of soluble E-cadherin in sera of breast cancer patients treated with neoadjuvant anthracycline-based chemotherapy and its predictive and prognostic value. J Clin Oncol 2005; 23:768.
9. Katayama M, Hirai S, Kamihagi K, et al. Soluble E-cadherin fragments increased in circulation of cancer patients. Br J Cancer 1994; 69:580-585.
10. Holbro T, Beerli RR, Maurer F, et al. The ErbB2/ErbB3 heterodimer functions as an oncogenic unit: ErbB2 requires ErbB3 to drive breast tumor cell proliferation. Proc Natl Acad Sci USA 2003; 100:8933-8938.
11. Yarden Y, Sliwkowski MX. Untangling the ErbB signaling network. Nat Rev Mol Cell Biol 2001; 2:127-137.
12. Olayioye MA, Neve RM, Lane HA, Hynes NE. The ErbB signaling network: Receptor heterodimerization in development and cancer. EMBO J 2000; 19:3159-3167.
13. Klapper LN, Kirschbaum MH, Sela M, Yarden Y. Biochemical and clinical implications of the ErbB/HER signaling network or growth factor receptors. Adv Cancer Res 2000; 77:25-79.
14. Salvesen GS, Duckett CS. IAP proteins: Blocking the road to death's door. Nat Rev Mol Cell Biol 2002; 3:401-410.
15. Wright CW, Duckett CS. Reawakening the cellular death program in neoplasia through the therapeutic blockade of IAP function. J Clin Invest 2005; 115:2673-2678.
16. Yang L, Cao Z, Yan H, Wood WC. Coexistence of high levels of apoptotic signaling and inhibitor of apoptosis proteins in human tumor cells: Implication for cancer specific therapy. Cancer Res 2003; 63:6815-6824.
17. Altieri DC. Validating survivin as a cancer therapeutic target. Nature Rev Cancer 2003; 3:46-54.
18. Ambrosini G, Adida C, Altieri DC. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Med 1997; 3:917-921.
19. Hinnis AR, Luckett JCA, Walker RA. Survivin is an independent predictor of short-term survival in poor prognostic breast cancer patients. Br J Cancer 2007; 96:639-645.
20. Wang J, Liu Y, Ji R, Gu Q, Zhao X, Sun B. Prognostic value of the X-linked inhibitor of apoptosis protein for invasive ductal breast cancer with triple-negative phenotype. Hum Pathol 2010; 41:1186-1195.
21. Schimmer AD, Welsh K, Pinilla C, et al. Small-molecule antagonists of apoptosis suppressor XIAP exhibit broad antitumor activity. Cancer Cell 2004; 5:25-35.
22. Vucic D, Fairbrother WJ. The Inhibitor of apoptosis proteins as therapeutic targets in cancer. Clin Cancer Res 2007; 13:5995-6000.
23. Xia W, Bisi J, Strum J, et al. Regulation of survivin by ErbB2 signaling: Therapeutic implications for ErbB2-overexpressing breast cancers. Cancer Res 2006; 66:1640-1647.
24. Asanuma H, Torigoe T, Kamiguchi K, et al. Survivin expression is regulated by coexpression of human epidermal growth factor receptor 2 and epidermal growth factor receptor via phosphatidylinositol 3-kinase/AKT signaling pathway in breast cancer cells. Cancer Res 2005; 65:11018-11025.
25. Inge LJ, Barwe SP, D'Ambrosio J, et al. Soluble E-cadherin promotes cell survival by activating epidermal growth factor receptor. Exp Cell Res 2011; 317:838-848.
26. Zuo JH, Zhu W, Li MY, et al. Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin. J Cell Biochem 2011; 112:2508-2517.
27. Brouxhon S, Kyrkanides S, O'Banion MK, 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.
28. Hennessy BT, Smith DL, Ram PT, Lu Y, Mills GB. Exploiting the PI3K/Akt pathway for cancer drug discovery. Nat Rev Drug Discov 2005; 4:988-1004.
29. Carracedo A, Ma L, Teruya-Feldstein J, et al. Inhibition of mTORC1 leads to MAPK pathway activation through a PI3K-dependent feedback loop in human cancer. J Clin Invest 2008; 118:3065-3074.
30. Oliveras-Ferraros C, Vazquez-Martin A, Cufí S, et al. Inhibitor of apoptosis (IAP) survivin is indispensable for survival of HER2 gene-amplified breast cancer cells with primary resistance to HER1/2-targeted therapies. Biochem Biophys Res Commun 2011; 407:412-419.
31. Machesky LM. Lamellipodia and filopodia in metastasis and invasion. FEBS Lett 2008; 582:2102-2111.
32. Sahin O, Fröhlich H, Löbke C, et al. Modeling ERBB receptor-regulated G1/S transition to find novel targets for de novo trastuzumab resistance. BMC Syst Biol 2009; 3:1-20.
33. Gofuku J, Shiozaki H, Doki Y, et al. Characterization of soluble E-cadherin as a disease marker in gastric cancer patients. Br J Cancer 1998; 78:1095-1101.
34. Kashiwagi S, Yashiro M, Takashima T, et al. Significance of E-cadherin expression in triple-negative breast cancer. Br J Cancer 2010; 103:249-255.
35. Yamanaka K, Nakata M, Kaneko N, et al. YM155, a selective survivin suppressant, inhibits tumor spread and prolongs survival in a spontaneous metastatic model of human triple negative breast cancer. Int J Oncol 2011; 39:569-575.
36. Choi KS, Lee TH, Jung MH. Ribozyme-mediated cleavage of the human survivin mRNA and inhibition of antiapoptotic function of survivin in MCF-7 cells. Cancer Gene Ther 2003; 10:87-95.
37. Mesri M, Wall NR, Li J, Kim RW, Altieri DC. Cancer gene therapy using a survivin mutant adenovirus. J Clin Invest 2001; 108:981-990.
38. Jaffer S, Orta L, Sunkara S, Sabo E, Burstein DE. Immunohistochemical detection of antiapoptotic protein X-linked inhibitor of apoptosis in mammary carcinoma. Hum Pathol 2007; 38:864-870.
39. Yagihashi A, Ohmura T, Asanuma K, et al. Detection of autoantibodies to survivin and livin in sera from patients with breast cancer. Clin Chim Acta 2005; 362:125-130.
40. Li J, Feng Q, Kim JM, et al. Human ovarian cancer and cisplatin resistance: Possible role of inhibitor of apoptosis proteins. Endocrinology 2001; 142:370-380.
41. Asselin E, Wang Y, Tsang BK. X-linked inhibitor of apoptosis protein activates the phosphatidylinositol 3-kinase/Akt pathway in rat granulosa cells during follicular development. Endocrinology 2001; 142:2451-2457.
42. Asselin E, Mills GB, Tsang BK. Xiap regulates Akt activity and caspase-3-dependent cleavage during cisplatin-induced apoptosis in human ovarian epithelial cancer cells. Cancer Res 2001; 61:1862-1868.
43. Siddiqa A, Long LM, Li L, Marciniak RA, Kazhdan I. Expression of HER-2 in MCF-7 breast cancer cells modulates anti-apoptotic proteins survivin and Bcl-2 via the extracellular signal-related kinase (ERK) and phosphoinositide-3 kinase (PI3K) signalling pathways. BMC Cancer 2008; 8:129.
44. Zhu H, Zhang G, Wang Y, et al. Inhibition of ErbB2 by Herceptin reduces survivin expression via the ErbB2-b-catenin/TCF4-survivin pathway in ErbB2-overexpressed breast cancer cells. Cancer Sci 2012; 101:1156-1162.
45. Riedl E, Stöckl J, Majdic O, Scheinecker C, Knapp W, Strobl H. Ligation of E-cadherin on in vitro-generated immature Langerhans type dendritic cells inhibits their maturation. Blood 2000; 96:4276-4284.
46. Siddiqui KR, Laffont S, Powrie F. E-cadherin marks a subset of inflammatory dendritic cells that promote T cell-mediated Colitis. Immunity 2010; 32:557-567.
47. Maretzky T, Scholz F, Köten 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.
48. Pittard AJ, Banks RE, Galley HF, Webster NR. Soluble E-cadherin concentrations in patients with systemic inflammatory response syndrome and multiorgan dysfunction syndrome. Br J Anaesth 1996; 76:629-631.
49. Riese DJ, Komurasakii T, Plowman GD, Stern DF. Activation of ErbB4 by the bifunctional epidermal growth factor family hormone epiregulin is regulated by ErbB2. J Biol Chem 1998; 273:11288-11294.