Annexin A2 depletion delays EGFR endocytic trafficking via cofilin activation and enhances EGFR signaling and metastasis formation

Oncogene

Volumn 33, Issue 20, 2014, Pages 2610-2619

  De Graauw, M ^a   Cao, L ^b   Winkel, L ^c   Van Miltenburg, M H A M ^d   Le Devedec S E ^a   Klop, M ^a   Yan, K ^b   Pont, C ^a   Rogkoti, V M ^a   Tijsma, A ^a   Chaudhuri, A ^a   Lalai, R ^a   Price, L ^a   Verbeek, F ^b   Van De Water, B ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

AnxA2; breast cancer; EGFR; endocytosis; metastasis

Indexed keywords

COFILIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GREEN FLUORESCENT PROTEIN; LIPOCORTIN 2; PROTEIN KINASE B; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER CELL LINE; CANCER GROWTH; CELL COUNT; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FLUORESCENCE MICROSCOPY; GENE IDENTIFICATION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LUNG METASTASIS; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TUMOR VOLUME; WESTERN BLOTTING;

MUS;

ACTIN DEPOLYMERIZING FACTORS; ANIMALS; ANNEXIN A2; CELL LINE, TUMOR; ENDOCYTOSIS; GENE KNOCKDOWN TECHNIQUES; HUMANS; MICE; MICROSCOPY, FLUORESCENCE; NEOPLASM METASTASIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84899839591     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.219     Document Type: Article

References (42)

1. Eccles SA. The epidermal growth factor receptor/Erb-B/HER family in normal and malignant breast biology. Int J Dev Biol 2011; 55: 685-696
2. Badovinac-Crnjevic T, Jakic-Razumovic J, Podolski P, Plestina S, Sarcevic B, Munjas R et al. Significance of epidermal growth factor receptor expression in breast cancer. Med Oncol 2011; 28(Suppl 1): S121-S128
3. Grandal MV, Madshus IH. Epidermal growth factor receptor and cancer: Control of oncogenic signalling by endocytosis. J Cell Mol Med 2008; 12: 1527-1534
4. Geldner N, Jurgens G. Endocytosis in signalling and development. Curr Opin Plant Biol 2006; 9: 589-594. (Pubitemid 44540404
5. Murphy JE, Padilla BE, Hasdemir B, Cottrell GS, Bunnett NW. Endosomes: A legitimate platform for the signaling train. Proc Natl Acad Sci USA 2009; 106: 17615-17622
6. Jiang X, Huang F, Marusyk A, Sorkin A. Grb2 regulates internalization of EGF receptors through clathrin-coated pits. Mol Biol Cell 2003; 14: 858-870. (Pubitemid 36337438
7. Waterman H, Levkowitz G, Alroy I, Yarden Y. The RING finger of c-Cbl mediates desensitization of the epidermal growth factor receptor. J Biol Chem 1999; 274: 22151-22154
8. Mosesson Y, Mills GB, Yarden Y. Derailed endocytosis: An emerging feature of cancer. Nat Rev Cancer 2008; 8: 835-850
9. Cao L, Yan K, Winkel L, de Graauw M, Verbeek FJ. Pattern recognition in highcontent cytomics screens for target discovery. Proceedings of the 6th IAPR International Conference on Pattern Recognition in Bioinformatics. Springer-Verlag:: Berlin2012: Pp 330-342, .
10. Grieve AG, Moss SE, Hayes MJ. Annexin A2 at the interface of actin and membrane dynamics: A focus on its roles in endocytosis and cell polarization. Int J Cell Biol 2012; 2012: 852430
11. de Graauw M, van Miltenburg MH, Schmidt MK, Pont C, Lalai R, Kartopawiro J et al. Annexin A1 regulates TGF-beta signaling and promotes metastasis formation of basal-like breast cancer cells. Proc Natl Acad Sci USA 2010; 107: 6340-6345
12. Minn AJ, Gupta GP, Padua D, Bos P, Nguyen DX, Nuyten D et al. Lung metastasis genes couple breast tumor size and metastatic spread. Proc Natl Acad Sci USA 2007; 104: 6740-6745. (Pubitemid 47175571
13. Sharma MR, Koltowski L, Ownbey RT, Tuszynski GP, Sharma MC. Angiogenesisassociated protein annexin II in breast cancer: Selective expression in invasive breast cancer and contribution to tumor invasion and progression. Exp Mol Pathol 2006; 81: 146-156. (Pubitemid 44715786
14. de Graauw M, Tijdens I, Smeets MB, Hensbergen PJ, Deelder AM, van De Water B. Annexin A2 phosphorylation mediates cell scattering and branching morphogenesis via cofilin Activation. Mol Cell Biol 2008; 28: 1029-1040. (Pubitemid 351160059
15. Okreglak V, Drubin DG. Cofilin recruitment and function During actin-mediated endocytosis dictated by actin nucleotide state. J Cell Biol 2007; 178: 1251-1264. (Pubitemid 47480230
16. Llado A, Timpson P, Vila de MS, Moreto J, Pol A, Grewal T et al. Protein kinase Cdelta and calmodulin regulate epidermal growth factor receptor recycling from early endosomes through Arp2/3 complex and cortactin. Mol Biol Cell 2008; 19: 17-29. (Pubitemid 351186129
17. Marcoux N, Vuori K. EGF receptor activity is essential for adhesion-induced stress fiber formation and cofilin phosphorylation. Cell Signal 2005; 17: 1449-1455. (Pubitemid 41206654
18. Miyamoto Y, Yamauchi J, Itoh H. Src kinase regulates the activation of a novel FGD-1-related Cdc42 guanine nucleotide exchange factor in the signaling pathway from the endothelin A receptor to JNK. J Biol Chem 2003; 278: 29890-29900. (Pubitemid 36962377
19. Richnau N, Aspenstrom P. Rich, a rho GTPase-Activating protein Domaincontaining protein involved in signaling by Cdc42 and Rac1. J Biol Chem 2001; 276: 35060-35070
20. Pepinsky RB, Sinclair LK. Epidermal growth factor-dependent phosphorylation of lipocortin. Nature 1986; 321: 81-84. (Pubitemid 16080891
21. Vila de MS, Timpson P, Cubells L, Evans R, Hayes TE, Rentero C et al. Annexin A6 inhibits Ras signalling in breast cancer cells. Oncogene 2009; 28: 363-377
22. Grewal T, Koese M, Rentero C, Enrich C. Annexin A6-regulator of the EGFR/Ras signalling pathway and cholesterol homeostasis. Int J Biochem Cell Biol 2010; 42: 580-584
23. Croxtall JD, Choudhury Q, Flower RJ. Glucocorticoids act within minutes to inhibit recruitment of signalling factors to activated EGF receptors through a receptordependent, transcription-independent mechanism. Br J Pharmacol 2000; 130: 289-298. (Pubitemid 30261038
24. White IJ, Bailey LM, Aghakhani MR, Moss SE, Futter CE. EGF stimulates annexin 1-dependent inward vesiculation in a multivesicular endosome subpopulation. EMBO J 2006; 25: 1-12. (Pubitemid 43077290
25. Emoto K, Yamada Y, Sawada H, Fujimoto H, Ueno M, Takayama T et al. Annexin II overexpression correlates with stromal tenascin-C overexpression: A prognostic marker in colorectal carcinoma. Cancer 2001; 92: 1419-1426. (Pubitemid 32947825
26. Zheng L, Foley K, Huang L, Leubner A, Mo G, Olino K et al. Tyrosine 23 phosphorylation-dependent cell-surface localization of annexin A2 is required for invasion and metastases of pancreatic cancer. PLoS One 2011; 6: E19390
27. Wu B, Zhang F, Yu M, Zhao P, Ji W, Zhang H et al. Up-regulation of Anxa2 gene promotes proliferation and invasion of breast cancer MCF-7 cells. Cell Prolif 2012; 45: 189-198
28. Jost M, Zeuschner D, Seemann J, Weber K, Gerke V. Identification and characterization of a novel type of annexin-membrane interaction: Ca2 is not required for the association of annexin II with early endosomes. J Cell Sci 1997; 110(Pt 2): 221-228. (Pubitemid 27075866
29. Harder T, Gerke V. The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. J Cell Biol 1993; 123: 1119-1132. (Pubitemid 23352422
30. Mayran N, Parton RG, Gruenberg J. Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J 2003; 22: 3242-3253. (Pubitemid 36834855
31. Shetty PK, Thamake SI, Biswas S, Johansson SL, Vishwanatha JK. Reciprocal regulation of annexin A2 and EGFR with Her-2 in Her-2 negative and herceptinresistant breast cancer. PLoS One 2012; 7: E44299
32. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ et al. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/ epidermal growth factor paracrine loop. Cancer Res 2005; 65: 5278-5283. (Pubitemid 40827339
33. Le Devedec SE, van RW, Maria N, Grimbergen M, Pont C, Lalai R et al. An improved model to study tumor cell autonomous metastasis programs using MTLn3 cells and the Rag2(-/-) gammac (-/-) mouse. Clin Exp Metastasis 2009; 26: 673-684
34. Babbin BA, Parkos CA, Mandell KJ, Winfree LM, Laur O, Ivanov AI et al. Annexin 2 regulates intestinal epithelial cell spreading and wound closure through Rho-related signaling. Am J Pathol 2007; 170: 951-966. (Pubitemid 47339364
35. Rescher U, Ludwig C, Konietzko V, Kharitonenkov A, Gerke V. Tyrosine phosphorylation of annexin A2 regulates Rho-mediated actin rearrangement and cell adhesion. J Cell Sci 2008; 121: 2177-2185
36. Nishimura Y, Yoshioka K, Bernard O, Bereczky B, Itoh K. A role of LIM kinase 1/cofilin pathway in regulating endocytic trafficking of EGF receptor in human breast cancer cells. Histochem Cell Biol 2006; 126: 627-638. (Pubitemid 44484907
37. Wang W, Eddy R, Condeelis J. The cofilin pathway in breast cancer invasion and metastasis. Nat Rev Cancer 2007; 7: 429-440. (Pubitemid 46809168
38. Sidani M, Wessels D, Mouneimne G, Ghosh M, Goswami S, Sarmiento C et al. Cofilin Determines the migration behavior and turning frequency of metastatic cancer cells. J Cell Biol 2007; 179: 777-791. (Pubitemid 350146261
39. Huigsloot M, Tijdens IB, Mulder GJ, van De Water B. Differential regulation of doxorubicin-induced mitochondrial dysfunction and apoptosis by Bcl-2 in mammary adenocarcinoma (MTLn3) cells. J Biol Chem 2002; 277: 35869-35879
40. Lombaerts M, van WT, Philippo K, Dierssen JW, Zimmerman RM, Oosting J et al. E-cadherin transcriptional downregulation by promoter methylation but not mutation is related to epithelial-To-mesenchymal transition in breast cancer cell lines. Br J Cancer 2006; 94: 661-671. (Pubitemid 43361897
41. de Graauw M, Tijdens I, Cramer R, Corless S, Timms JF, van De Water B. Heat shock protein 27 is the major differentially phosphorylated protein involved in renal epithelial cellular stress response and controls focal adhesion organization and apoptosis. J Biol Chem 2005; 280: 29885-29898. (Pubitemid 41177066
42. van Roosmalen W, Le Devedec SE, Zovko S, de BH, van De WB. Functional screening with a live cell imaging-based random cell migration assay. Methods Mol Biol 2011; 769: 435-448