Cadherin-6 promotes EMT and cancer metastasis by restraining autophagy

Oncogene

Volumn 36, Issue 5, 2017, Pages 667-677

  Gugnoni, M ^a   Sancisi, V ^a   Gandolfi, G ^a   Manzotti, G ^a   Ragazzi, M ^a   Giordano, D ^a   Tamagnini, I ^a   Tigano, M ^a   Frasoldati, A ^a   Piana, S ^a   Ciarrocchi, A ^a  

^a S MARIA NUOVA HOSPITAL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CADHERIN 6; PEPTIDES AND PROTEINS; PROTEIN BNIP3; PROTEIN BNIP3L; PROTEIN GABARAP; UNCLASSIFIED DRUG;

ARTICLE; AUTOPHAGY; B-CPAP CELL LINE; CANCER GROWTH; CELL INTERACTION; CELL STRUCTURE; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; THYROID CANCER; TPC-1 CELL LINE; TWO HYBRID SYSTEM; CARCINOMA; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; THYROID TUMOR;

AUTOPHAGY; CADHERINS; CARCINOMA; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION; THYROID NEOPLASMS;

EID: 84976874938     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2016.237     Document Type: Article

References (54)

1. Davies L, Welch HG. Current thyroid cancer trends in the United States. JAMA Otolaryngol Head Neck Surg 2014; 140: 317-322.
2. Davies L, Welch HG. Thyroid cancer survival in the United States: observational data from 1973 to 2005. Arch Otolaryngol Head Neck Surg 2010; 136: 440-444.
3. Pellegriti G, Frasca F, Regalbuto C, Squatrito S, Vigneri R. Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J Cancer Epidemiol 2013; 2013: 965212.
4. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT et al. Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2009; 19: 1167-1214.
5. Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ et al. Management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 2006; 16: 109-142.
6. Kalluri R. EMT: when epithelial cells decide to become mesenchymal-like cells. J Clin Invest 2009; 119: 1417-1419.
7. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: Acquisition of malignant and stem cell traits. Nat Rev Cancer 2009; 9: 265-273.
8. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009; 139: 871-890.
9. Nollet F, Kools P, van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 2000; 299: 551-572.
10. Kashef J, Kohler A, Kuriyama S, Alfandari D, Mayor R, Wedlich D. Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev 2009; 23: 1393-1398.
11. Kim SH, Li Z, Sacks DB. E-cadherin-mediated cell-cell attachment activates Cdc42. J Biol Chem 2000; 275: 36999-37005.
12. Kovacs EM, Ali RG, McCormack AJ, Yap AS. E-cadherin homophilic ligation directly signals through Rac and phosphatidylinositol 3-kinase to regulate adhesive contacts. J Biol Chem 2002; 277: 6708-6718.
13. Noren NK, Arthur WT, Burridge K. Cadherin engagement inhibits RhoA via p190RhoGAP. J Biol Chem 2003; 278: 13615-13618.
14. Zaidel-Bar R. Cadherin adhesome at a glance. J Cell Sci 2013; 126: 373-378.
15. Cho EA, Patterson LT, Brookhiser WT, Mah S, Kintner C, Dressler GR. Differential expression and function of cadherin-6 during renal epithelium development. Development 1998; 125: 803-812.
16. Inoue T, Chisaka O, Matsunami H, Takeichi M. Cadherin-6 expression transiently delineates specific rhombomeres, other neural tube subdivisions, and neural crest subpopulations in mouse embryos. Dev Biol 1997; 183: 183-194.
17. Inoue YU, Asami J, Inoue T. Cadherin-6 gene regulatory patterns in the postnatal mouse brain. Mol Cell Neurosci 2008; 39: 95-104.
18. Jia L, Liu F, Hansen SH, Ter Beest MB, Zegers MM. Distinct roles of cadherin-6 and E-cadherin in tubulogenesis and lumen formation. Mol Biol Cell 2011; 22: 2031-2041.
19. Kobel M, Kalloger SE, Boyd N, McKinney S, Mehl E, Palmer C et al. Ovarian carcinoma subtypes are different diseases: implications for biomarker studies. PLoS Med 2008; 5: e232.
20. Shimazui T, Oosterwijk E, Akaza H, Bringuier P, Ruijter E, van Berkel H et al. Expression of cadherin-6 as a novel diagnostic tool to predict prognosis of patients with E-cadherin-absent renal cell carcinoma. Clin Cancer Res 1998; 4: 2419-2424.
21. Ciarrocchi A, Piana S, Valcavi R, Gardini G, Casali B. Inhibitor of DNA binding-1 induces mesenchymal features and promotes invasiveness in thyroid tumour cells. Eur J Cancer 2011; 47: 934-945.
22. Sancisi V, Gandolfi G, Ragazzi M, Nicoli D, Tamagnini I, Piana S et al. Cadherin 6 is a new RUNX2 target in TGF-beta signalling pathway. PLoS ONE 2013; 8: e75489.
23. Tojkander S, Gateva G, Lappalainen P. Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 2012; 125: 1855-1864.
24. Clay MR, Halloran MC. Cadherin 6 promotes neural crest cell detachment via F-actin regulation and influences active Rho distribution during epithelialto-mesenchymal transition. Development 2014; 141: 2506-2515.
25. Cali G, Gentile F, Mogavero S, Pallante P, Nitsch R, Ciancia G et al. CDH16/ Ksp-cadherin is expressed in the developing thyroid gland and is strongly down-regulated in thyroid carcinomas. Endocrinology 2012; 153: 522-534.
26. Boutet A, De Frutos CA, Maxwell PH, Mayol MJ, Romero J, Nieto MA. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J 2006; 25: 5603-5613.
27. Slobodkin MR, Elazar Z. The Atg8 family: multifunctional ubiquitin-like key regulators of autophagy. Essays Biochem 2013; 55: 51-64.
28. Ney PA. Mitochondrial autophagy: Origins, significance, and role of BNIP3 and NIX. Biochim Biophys Acta 2015; 1853(10 Pt B): 2775-2783.
29. Schwarten M, Mohrluder J, Ma P, Stoldt M, Thielmann Y, Stangler T et al. Nix directly binds to GABARAP: A possible crosstalk between apoptosis and autophagy. Autophagy 2009; 5: 690-698.
30. Galluzzi L, Pietrocola F, Bravo-San Pedro JM, Amaravadi RK, Baehrecke EH, Cecconi F et al. Autophagy in malignant transformation and cancer progression. EMBO J 2015; 34: 856-880.
31. Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim Biophys Acta 2013; 1833: 205-212.
32. Desai SP, Bhatia SN, Toner M, Irimia D. Mitochondrial localization and the persistent migration of epithelial cancer cells. Biophys J 2013; 104: 2077-2088.
33. Serasinghe MN, Wieder SY, Renault TT, Elkholi R, Asciolla JJ, Yao JL et al. Mitochondrial division is requisite to RAS-induced transformation and targeted by oncogenic MAPK pathway inhibitors. Mol Cell 2015; 57: 521-536.
34. Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci 2014; 127: 3-9.
35. Gandolfi G, Sancisi V, Piana S, Ciarrocchi A. Time to re-consider the meaning of BRAF V600E mutation in papillary thyroid carcinoma. Int J Cancer 2015; 137: 1001-1011.
36. Friedl P, Gilmour G. Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 2009; 10: 445-457.
37. Gray RS, Cheung KJ, Ewald AJ. Cellular mechanisms regulating epithelial morphogenesis and cancer invasion. Curr Opin Cell Biol 2010; 22: 640-650.
38. Friedl P, Locker J, Sahai E, Segall JE. Classifying collective cancer cell invasion. Nat Cell Biol 2012; 14: 777-783.
39. Tsuji T, Ibaragi S, Hu GF. Epithelial-mesenchymal transition and cell cooperativity in metastasis. Cancer Res 2009; 69: 7135-7139.
40. Choi PW, Yang J, Ng SK, Feltmate C, Muto MG, Hasselblatt K et al. Loss of E-cadherin disrupts ovarian epithelial inclusion cyst formation and collective cell movement in ovarian cancer cells. Oncotarget 2015; 7: 4110-4121.
41. Cai D, Chen SC, Prasad M, He L, Wang X, Choesmel-Cadamuro V et al. Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 2014; 157: 1146-1159.
42. Scheumman GF, Hoang-Vu C, Cetin Y, Gimm O, Behrends J, von Wasielewski R et al. Clinical significance of E-cadherin as a prognostic marker in thyroid carcinomas. J Clin Endocrinol Metab 1995; 80: 2168-2172.
43. Brabant G, Hoang-Vu C, Cetin Y, Dralle H, Scheumann G, Mölne J et al. E-cadherin: A differentiation marker in thyroid malignancies. Cancer Res 1993; 53: 4987-4993.
44. Catalano M, D'Alessandro G, Lepore F, Corazzari M, Caldarola S, Valacca C et al. Autophagy induction impairs migration and invasion by reversing EMT in glioblastoma cells. Mol Oncol 2015; 9: 1612-1625.
45. Kashatus JA, Nascimento A, Myers LJ, Sher A, Byrne FL, Hoehn KL et al. Erk2 phosphorylation of Drp1 promotes mitochondrial fission and MAPK-driven tumor growth. Mol Cell 2015; 57: 537-551.
46. Rehman J, Zhang HJ, Toth PT, Zhang Y, Marsboom G, Hong Z et al. Inhibition of mitochondrial fission prevents cell cycle progression in lung cancer. FASEB J 2012; 26: 2175-2186.
47. Xie Q, Wu Q, Horbinski CM, Flavahan WA, Yang K, Zhou W et al. Mitochondrial control by DRP1 in brain tumor initiating cells. Nat Neurosci 2015; 18: 501-510.
48. Zhao J, Zhang J, Yu M, Xie Y, Huang Y, Wolff DW et al. Mitochondrial dynamics regulates migration and invasion of breast cancer cells. Oncogene 2013; 32: 4814-4824.
49. Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P et al. Epithelial-tomesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res 2013; 73: 2418-2427.
50. Peng YF, Shi YH, Ding ZB, Ke AW, Gu CY, Hui B et al. Autophagy inhibition suppresses pulmonary metastasis of HCC in mice via impairing anoikis resistance and colonization of HCC cells. Autophagy 2013; 9: 2056-2068.
51. Wang H, Olsen RW. Binding of the GABA(A) receptor-associated protein (GABARAP) to microtubules and microfilaments suggests involvement of the cytoskeleton in GABARAPGABA(A) receptor interaction. J Neurochem 2000; 75: 644-655.
52. Chen L, Wang H, Vicini S, Olsen RW. The gamma-aminobutyric acid type A (GABAA) receptor-associated protein (GABARAP) promotes GABAA receptor clustering and modulates the channel kinetics. Proc Natl Acad Sci USA 2000; 97: 11557-11562.
53. Maes H, Van Eygen S, Krysko DV, Vandenabeele P, Nys K, Rillaerts K et al. BNIP3 supports melanoma cell migration and vasculogenic mimicry by orchestrating the actin cytoskeleton. Cell Death Dis 2014; 5: e1127.
54. Sancisi V, Borettini G, Maramotti S, Ragazzi M, Tamagnini I, Nicoli D et al. Runx2 isoform I controls a panel of proinvasive genes driving aggressiveness of papillary thyroid carcinomas. J Clin Endocrinol Metab 2012; 97: E2006-E2015.