Induction of entosis by epithelial cadherin expression

Cell Research

Volumn 24, Issue 11, 2014, Pages 1288-1298

  Sun, Qiang ^a,b   Cibas, Edmund S ^c,d   Huang, Hongyan ^e   Hodgson, Louis ^f   Overholtzer, Michael ^b,g  

^a BEIJING INSTITUTE OF BIOTECHNOLOGY   (China)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c Department of Pathology ^*  (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e CAPITAL MEDICAL UNIVERSITY   (China)

^f ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^g WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

actomyosin; cadherin; entosis; p190A RhoGAP; Rho GTPase; tumor suppression

Indexed keywords

ARHGAP35 PROTEIN, HUMAN; CADHERIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; REPRESSOR PROTEIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; ROCK1 PROTEIN, HUMAN; ROCK2 PROTEIN, HUMAN; SMALL INTERFERING RNA;

ANTAGONISTS AND INHIBITORS; CONFOCAL MICROSCOPY; DOWN REGULATION; ENTOSIS; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; RNA INTERFERENCE; TIME LAPSE IMAGING; TUMOR CELL LINE;

ACTOMYOSIN; CADHERINS; CELL LINE, TUMOR; DOWN-REGULATION; ENTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; MCF-7 CELLS; MICROSCOPY, CONFOCAL; MYOSINS; REPRESSOR PROTEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; RNA, SMALL INTERFERING; TIME-LAPSE IMAGING;

EID: 84908509351     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2014.137     Document Type: Article

References (46)

1. Hochreiter-Hufford A, Ravichandran KS. Clearing the dead: apoptotic cell sensing, recognition, engulfment, and digestion. Cold Spring Harb Perspect Biol 2013; 5:a008748.
2. Hoeppner DJ, Hengartner MO, Schnabel R. Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans. Nature 2001; 412:202-206.
3. Reddien PW, Cameron S, Horvitz HR. Phagocytosis promotes programmed cell death in C. elegans. Nature 2001; 412:198-202.
4. Neniskyte U, Brown GC. Lactadherin/MFG-E8 is essential for microglia-mediated neuronal loss and phagoptosis induced by amyloid beta. J Neurochem 2013; 126:312-317.
5. Brown GC, Neher JJ. Eaten alive! Cell death by primary phagocytosis: 'phagoptosis'. Trends Biochem Sci 2012; 37:325-332.
6. Overholtzer M, Brugge JS. The cell biology of cell-in-cell structures. Nat Rev Mol Cell Biol 2008; 9:796-809.
7. Krajcovic M, Johnson NB, Sun Q, et al. A non-genetic route to aneuploidy in human cancers. Nat Cell Biol 2011; 13:324-330.
8. Lugini L, Matarrese P, Tinari A, et al. Cannibalism of live lymphocytes by human metastatic but not primary melanoma cells. Cancer Res 2006; 66:3629-3638.
9. Abodief WT, Dey P, Al-Hattab O. Cell cannibalism in ductal carcinoma of breast. Cytopathology 2006; 17:304-305.
10. Krajcovic M, Krishna S, Akkari L, Joyce JA, Overholtzer M. mTOR regulates phagosome and entotic vacuole fission. Mol Biol Cell 2013; 24:3736-3745.
11. Chen YH, Wang S, He MF, et al. Prevalence of heterotypic tumor/immune cell-in-cell structure in vitro and in vivo leading to formation of aneuploidy. PLoS One 2013; 8:e59418.
12. Sun Q, Luo T, Ren Y, et al. Competition between human cells by entosis. Cell Res 2014; 24:1299-1310.
13. Overholtzer M, Mailleux AA, Mouneimne G, et al. A nonapoptotic cell death process, entosis, that occurs by cellin- cell invasion. Cell 2007; 131:966-979.
14. Florey O, Kim SE, Sandoval CP, Haynes CM, Overholtzer M. Autophagy machinery mediates macroendocytic processing and entotic cell death by targeting single membranes. Nat Cell Biol 2011; 13:1335-1343.
15. Sharma N, Dey P. Cell cannibalism and cancer. Diagn Cytopathol 2011; 39:229-233.
16. Wang S, Guo Z, Xia P, et al. Internalization of NK cells into tumor cells requires ezrin and leads to programmed cell-incell death. Cell Res 2009; 19:1350-1362.
17. Cano CE, Sandi MJ, Hamidi T, et al. Homotypic cell cannibalism, a cell-death process regulated by the nuclear protein 1, opposes to metastasis in pancreatic cancer. EMBO Mol Med 2012; 4:964-979.
18. Abreu M, Sealy L. Cells expressing the C/EBPbeta isoform, LIP, engulf their neighbors. PLoS One 2012; 7:e41807.
19. 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.
20. Liu N, Yu Q, Liu TJ, et al. P-cadherin expression and basal- like subtype in breast cancers. Med Oncol 2012; 29:2606-2612.
21. Wan Q, Liu J, Zheng Z, et al. Regulation of myosin activation during cell-cell contact formation by Par3-Lgl antagonism: entosis without matrix detachment. Mol Biol Cell 2012; 23:2076-2091.
22. Purvanov V, Holst M, Khan J, Baarlink C, Grosse R. G-protein- coupled receptor signaling and polarized actin dynamics drive cell-in-cell invasion. Elife 2014 June 20. doi: 10.7554/ eLife.02786
23. Noren NK, Arthur WT, Burridge K. Cadherin engagement inhibits RhoA via p190RhoGAP. J Biol Chem 2003; 278:13615-13618.
24. Bourguignon LY, Gilad E, Brightman A, Diedrich F, Singleton P. Hyaluronan-CD44 interaction with leukemia-associated RhoGEF and epidermal growth factor receptor promotes Rho/ Ras co-activation, phospholipase C epsilon-Ca2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J Biol Chem 2006; 281:14026-14040.
25. Wildenberg GA, Dohn MR, Carnahan RH, et al. p120-catenin and p190RhoGAP regulate cell-cell adhesion by coordinating antagonism between Rac and Rho. Cell 2006; 127:1027-1039.
26. Simoes S, Denholm B, Azevedo D, et al. Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 2006; 133:4257-4267.
27. Derksen PW, Liu X, Saridin F, et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006; 10:437-449.
28. Onder TT, Gupta PB, Mani SA, et al. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008; 68:3645-3654.
29. Perrais M, Chen X, Perez-Moreno M, Gumbiner BM. E-cadherin homophilic ligation inhibits cell growth and epidermal growth factor receptor signaling independently of other cell interactions. Mol Biol Cell 2007; 18:2013-2025.
30. Frixen UH, Behrens J, Sachs M, et al. E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 1991; 113:173-185.
31. Heselmeyer-Haddad K, Berroa Garcia LY, Bradley A, et al. Single-cell genetic analysis of ductal carcinoma in situ and invasive breast cancer reveals enormous tumor heterogeneity yet conserved genomic imbalances and gain of MYC during progression. Am J Pathol 2012; 181:1807-1822.
32. Cancer Genome Atlas N. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490:61-70.
33. Ionescu Popescu C, Giusca SE, Liliac L, et al. E-cadherin expression in molecular types of breast carcinoma. Rom J Morphol Embryol 2013; 54:267-273.
34. Kowalski PJ, Rubin MA, Kleer CG. E-cadherin expression in primary carcinomas of the breast and its distant metastases. Breast Cancer Res 2003; 5:R217-R222.
35. Rodriguez FJ, Lewis-Tuffin LJ, Anastasiadis PZ. E-cadherin's dark side: possible role in tumor progression. Biochim Biophys Acta 2012; 1826:23-31.
36. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012; 22:725-736.
37. Ocana OH, Corcoles R, Fabra A, et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 2012; 22:709-724.
38. Chu K, Boley KM, Moraes R, Barsky SH, Robertson FM. The paradox of E-cadherin: role in response to hypoxia in the tumor microenvironment and regulation of energy metabolism. Oncotarget 2013; 4:446-462.
39. Xiang X, Deng Z, Zhuang X, et al. Grhl2 determines the epithelial phenotype of breast cancers and promotes tumor progression. PLoS One 2012; 7:e50781.
40. Yamada S, Nelson WJ. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J Cell Biol 2007; 178:517-527.
41. Sun Q, Zhang Y, Yang G, et al. Transforming growth factor- beta-regulated miR-24 promotes skeletal muscle differentiation. Nucleic Acids Res 2008; 36:2690-2699.
42. Sun Q, Overholtzer M. Methods for the study of entosis. Methods Mol Biol 2013; 1004:59-66.
43. Pinner S, Sahai E. PDK1 regulates cancer cell motility by antagonising inhibition of ROCK1 by RhoE. Nat Cell Biol 2008; 10:127-137.
44. Pertz O, Hodgson L, Klemke RL, Hahn KM. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 2006; 440:1069-1072.
45. Tamada M, Perez TD, Nelson WJ, Sheetz MP. Two distinct modes of myosin assembly and dynamics during epithelial wound closure. J Cell Biol 2007; 176:27-33.
46. Zhang Y, Fan KJ, Sun Q, et al. Functional screening for miRNAs targeting Smad4 identified miR-199a as a negative regulator of TGF-beta signalling pathway. Nucleic Acids Res 2012; 40:9286-9297.