Ezrin promotes invasion and metastasis of pancreatic cancer cells

Journal of Translational Medicine

Volumn 8, Issue , 2010, Pages

  Meng, Yunxiao ^a   Lu, Zhaohui ^a   Yu, Shuangni ^a   Zhang, Qiang ^a   Ma, Yihui ^a   Chen, Jie ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EZRIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; CYTOSKELETON PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; CELL CYCLE REGULATION; CELL MOTILITY; CELL PROLIFERATION; CELL STRUCTURE; CHRONIC PANCREATITIS; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; INTRADUCTAL CARCINOMA; METASTASIS; MICROVILLUS; MOUSE; NONHUMAN; NUDE MOUSE; PANCREAS CANCER; PRECANCER; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; ANIMAL; CELL ADHESION; CELL CLONE; CELL CYCLE; CELL MOTION; CELL SURFACE; ENZYMOLOGY; METABOLISM; MIDDLE AGED; PANCREAS CARCINOMA; PANCREAS TUMOR; PATHOLOGY; PHOSPHORYLATION; TUMOR CELL LINE; ULTRASTRUCTURE;

ADULT; AGED; ANIMALS; CARCINOMA, PANCREATIC DUCTAL; CELL ADHESION; CELL CYCLE; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL SURFACE EXTENSIONS; CLONE CELLS; CYTOSKELETAL PROTEINS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE SILENCING; HUMANS; MICE; MICE, NUDE; MICROVILLI; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PANCREATIC NEOPLASMS; PANCREATITIS, CHRONIC; PHOSPHORYLATION;

EID: 77953690374     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-8-61     Document Type: Article

References (44)

1. Sato N, Funayama N, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S. A gene family consisting of ezrin, radixin and moesin. Its specific localization at actin filament/plasma membrane association sites. J Cell Sci 1992, 103(Pt 1):131-143.
2. Bretscher A, Edwards K, Fehon RG. ERM proteins and merlin: integrators at the cell cortex. Nat Rev Mol Cell Biol 2002, 3(8):586-599. 10.1038/nrm882, 12154370.
3. Pujuguet P, Del Maestro L, Gautreau A, Louvard D, Arpin M. Ezrin regulates E-cadherin-dependent adherens junction assembly through Rac1 activation. Mol Biol Cell 2003, 14(5):2181-2191. 10.1091/mbc.E02-07-0410, 165106, 12802084.
4. Gautreau A, Louvard D, Arpin M. ERM proteins and NF2 tumor suppressor: the Yin and Yang of cortical actin organization and cell growth signaling. Curr Opin Cell Biol 2002, 14(1):104-109. 10.1016/S0955-0674(01)00300-3, 11792551.
5. Mielgo A, Brondani V, Landmann L, Glaser-Ruhm A, Erb P, Stupack D, Günthert U. The CD44 standard/ezrin complex regulates Fas-mediated apoptosis in Jurkat cells. Apoptosis 2007, 12(11):2051-2061. 10.1007/s10495-007-0115-3, 17726647.
6. Hiscox S, Jiang WG. Ezrin regulates cell-cell and cell-matrix adhesion, a possible role with E-cadherin/beta-catenin. J Cell Sci 1999, 112(Pt 18):3081-3090.
7. Louvet-Vallée S. ERM proteins: from cellular architecture to cell signaling. Biol Cell 2000, 92(5):305-316. 10.1016/S0248-4900(00)01078-9, 11071040.
8. Yonemura S, Hirao M, Doi Y, Takahashi N, Kondo T, Tsukita S, Tsukita S. Ezrin/radixin/moesin (ERM) proteins bind to a positively charged amino acid cluster in the juxta-membrane cytoplasmic domain of CD44, CD43, and ICAM-2. J Cell Biol 1998, 140(4):885-895. 10.1083/jcb.140.4.885, 2141743, 9472040.
9. Wu KL, Khan S, Lakhe-Reddy S, Jarad G, Mukherjee A, Obejero-Paz CA, Konieczkowski M, Sedor JR, Schelling JR. The NHE1 Na+/H+ exchanger recruits ezrin/radixin/moesin proteins to regulate Akt-dependent cell survival. J Biol Chem 2004, 279(25):26280-26286. 10.1074/jbc.M400814200, 15096511.
10. Yonemura S, Matsui T, Tsukita S, Tsukita S. Rho-dependent and -independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J Cell Sci 2002, 115(Pt 12):2569-2580.
11. Gautreau A, Poullet P, Louvard D, Arpin M. Ezrin, a plasma membrane-microfilament linker, signals cell survival through the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci USA 1999, 96(13):7300-7305. 10.1073/pnas.96.13.7300, 22080, 10377409.
12. Fievet BT, Gautreau A, Roy C, Del Maestro L, Mangeat P, Louvard D, Arpin M. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol 2004, 164(5):653-659. 10.1083/jcb.200307032, 2172172, 14993232.
13. Wick W, Grimmel C, Wild-Bode C, Platten M, Arpin M, Weller M. Ezrin-dependent promotion of glioma cell clonogenicity, motility, and invasion mediated by BCL-2 and transforming growth factor-beta2. J Neurosci 2001, 21(10):3360-3368.
14. Crepaldi T, Gautreau A, Comoglio PM, Louvard D, Arpin M. Ezrin is an effector of hepatocyte growth factor-mediated migration and morphogenesis in epithelial cells. J Cell Biol 1997, 138(2):423-434. 10.1083/jcb.138.2.423, 2138186, 9230083.
15. Lugini L, Lozupone F, Matarrese P, Funaro C, Luciani F, Malorni W, Rivoltini L, Castelli C, Tinari A, Piris A, Parmiani G, Fais S. Potent phagocytic activity discriminates metastatic and primary human malignant melanomas: a key role of ezrin. Lab Invest 2003, 83(11):1555-1567. 10.1097/01.LAB.0000098425.03006.42, 14615410.
16. Geiger KD, Stoldt P, Schlote W, Derouiche A. Ezrin immunoreactivity is associated with increasing malignancy of astrocytic tumors but is absent in oligodendrogliomas. Am J Pathol 2000, 157(6):1785-1793. 1885782, 11106550.
17. Yu Y, Khan J, Khanna C, Helman L, Meltzer PS, Merlino G. Expression profiling identifies the cytoskeletal organizer ezrin and the developmental homeoprotein Six-1 as key metastatic regulators. Nat Med 2004, 10(2):175-181. 10.1038/nm966, 14704789.
18. Wei YC, Li CF, Yu SC, Chou FF, Fang FM, Eng HL, Uen YH, Tian YF, Wu JM, Li SH, Huang WW, Li WM, Huang HY. Ezrin overexpression in gastrointestinal stromal tumors: an independent adverse prognosticator associated with the non-gastric location. Mod Pathol 2009, 22(10):1351-60. 10.1038/modpathol.2009.107, 19648886.
19. Khanna C, Khan J, Nguyen P, Prehn J, Caylor J, Yeung C, Trepel J, Meltzer P, Helman L. Metastasis-associated differences in gene expression in a murine model of osteosarcoma. Cancer Res 2001, 61(9):3750-3759.
20. Khanna C, Wan X, Bose S, Cassaday R, Olomu O, Mendoza A, Yeung C, Gorlick R, Hewitt SM, Helman LJ. The membrane-cytoskeleton linker ezrin is necessary for osteosarcoma metastasis. Nat Med 2004, 10(2):182-186. 10.1038/nm982, 14704791.
21. Li Q, Wu M, Wang H, Xu G, Zhu T, Zhang Y, Liu P, Song A, Gang C, Han Z, Zhou J, Meng L, Lu Y, Wang S, Ma D. Ezrin silencing by small hairpin RNA reverses metastatic behaviors of human breast cancer cells. Cancer Lett 2008, 261(1):55-63. 10.1016/j.canlet.2007.11.018, 18155831.
22. Curto M, McClatchey AI. Ezrin...a metastatic detERMinant?. Cancer Cell 2004, 5(2):113-114. 10.1016/S1535-6108(04)00031-5, 14998486.
23. Yeh TS, Tseng JH, Liu NJ, Chen TC, Jan YY, Chen MF. Significance of cellular distribution of ezrin in pancreatic cystic neoplasms and ductal adenocarcinoma. Arch Surg 2005, 140(12):1184-1190. 10.1001/archsurg.140.12.1184, 16365240.
24. Kitamura N, Iwamura T, Taniguchi S, Yamanari H, Kawano MA, Hollingsworth K, Setoguchi T. High collagenolytic activity in spontaneously highly metastatic variants derived from a human pancreatic cancer cell line (SUIT-2) in nude mice. Clin Exp Metastasis 2000, 18(7):561-571. 10.1023/A:1011900818419, 11688961.
25. Hustinx SR, Fukushima N, Zahurak ML, Riall TS, Maitra A, Brosens L, Cameron JL, Yeo CJ, Offerhaus GJ, Hruban RH, Goggins M. Expression and prognostic significance of 14-3-3sigma and ERM family protein expression in periampullary neoplasms. Cancer Biol Ther 2005, 4(5):596-601.
26. Akisawa N, Nishimori I, Iwamura T, Onishi S, Hollingsworth MA. High levels of ezrin expressed by human pancreatic adenocarcinoma cell lines with high metastatic potential. Biochem Biophys Res Commun 1999, 258(2):395-400. 10.1006/bbrc.1999.0653, 10329398.
27. Cui Y, Li T, Zhang D, Han J. Expression of Ezrin and phosphorylated Ezrin (pEzrin) in pancreatic ductal adenocarcinoma. Cancer Invest 2010, 28(3):242-247. 10.3109/07357900903124498, 20158339.
28. Kocher HM, Sandle J, Mirza TA, Li NF, Hart IR. Ezrin interacts with cortactin to form podosomal rosettes in pancreatic cancer cells. Gut 2009, 58(2):271-284. 10.1136/gut.2008.159871, 18852256.
29. Barros JC, Marshall CJ. Activation of either ERK1/2 or ERK5 MAP kinase pathways can lead to disruption of the actin cytoskeleton. J Cell Sci 2005, 118(Pt 8):1663-1671. 10.1242/jcs.02308, 15797923.
30. Yip SC, El-Sibai M, Coniglio SJ, Mouneimne G, Eddy RJ, Drees BE, Neilsen PO, Goswami S, Symons M, Condeelis JS, Backer JM. The distinct roles of Ras and Rac in PI 3-kinase-dependent protrusion during EGF-stimulated cell migration. J Cell Sci 2007, 120(Pt 17):3138-46. 10.1242/jcs.005298, 17698922.
31. Ling ZQ, Mukaisho K, Yamamoto H, Chen KH, Asano S, Araki Y, Sugihara H, Mao WM, Hattori T. Initiation of malignancy by duodenal contents reflux and the role of ezrin in developing esophageal squamous cell carcinoma. Cancer Sci 2010, 101(3):624-30. 10.1111/j.1349-7006.2009.01470.x, 20128822.
32. Turunen O, Wahlström T, Vaheri A. Ezrin has a COOH-terminal actin-binding site that is conserved in the ezrin protein family. J Cell Biol 1994, 126(6):1445-1453. 10.1083/jcb.126.6.1445, 2290954, 8089177.
33. Andréoli C, Martin M, Le Borgne R, Reggio H, Mangeat P. Ezrin has properties to self-associate at the plasma membrane. J Cell Sci 1994, 107(Pt 9):2509-2521.
34. Stylli SS, Kaye AH, Lock P. Invadopodia: at the cutting edge of tumour invasion. J Clin Neurosci 2008, 15(7):725-737. 10.1016/j.jocn.2008.03.003, 18468901.
35. Deryugina EI, Bourdon MA, Reisfeld RA, Strongin A. Remodeling of collagen matrix by human tumor cells requires activation and cell surface association of matrix metalloproteinase-2. Cancer Res 1998, 58(16):3743-3750.
36. Park HR, Jung WW, Bacchini P, Bertoni F, Kim YW, Park YK. Ezrin in osteosarcoma: comparison between conventional high-grade and central low-grade osteosarcoma. Pathol Res Pract 2006, 202(7):509-515. 10.1016/j.prp.2006.01.015, 16677779.
37. Elliott BE, Meens JA, SenGupta SK, Louvard D, Arpin M. The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells. Breast Cancer Res 2005, 7(3):R365-373. 10.1186/bcr1006, 1143558, 15987432.
38. Yeh CN, Pang ST, Chen TW, Wu RC, Weng WH, Chen MF. Expression of ezrin is associated with invasion and dedifferentiation of hepatitis B related hepatocellular carcinoma. BMC Cancer 2009, 9:233. 10.1186/1471-2407-9-233, 2716370, 19604375.
39. Hruban RH, Fukushima N. Pancreatic adenocarcinoma: update on the surgical pathology of carcinomas of ductal origin and PanINs. Mod Pathol 2007, (20 Suppl 1):S61-70. 10.1038/modpathol.3800685, 17486053.
40. Zhang L, Sanderson SO, Lloyd RV, Smyrk TC. Pancreatic intraepithelial neoplasia in heterotopic pancreas: evidence for the progression model of pancreatic ductal adenocarcinoma. Am J Surg Pathol 2007, 31(8):1191-1195. 10.1097/PAS.0b013e31806841e1, 17667542.
41. Rosty C, Geradts J, Sato N, Wilentz RE, Roberts H, Sohn T, Cameron JL, Yeo CJ, Hruban RH, Goggins M. p16 Inactivation in pancreatic intraepithelial neoplasias (PanINs) arising in patients with chronic pancreatitis. Am J Surg Pathol 2003, 27(12):1495-1501. 10.1097/00000478-200312000-00001, 14657708.
42. Ueda S, Fukamachi K, Matsuoka Y, Takasuka N, Takeshita F, Naito A, Iigo M, Alexander DB, Moore MA, Saito I, Ochiya T, Tsuda H. Ductal origin of pancreatic adenocarcinomas induced by conditional activation of a human Ha-ras oncogene in rat pancreas. Carcinogenesis 2006, 27(12):2497-2510. 10.1093/carcin/bgl090, 16774944.
43. Wada R, Ogawa K, Yamaguchi T, Tanizaki T, Matsumoto M. Intercalated duct cell is starting point in development of pancreatic ductal carcinoma?. J Carcinog 2005, 4:9. 10.1186/1477-3163-4-9, 1185555, 16018800.
44. Zhu L, Shi G, Schmidt CM, Hruban RH, Konieczny SF. Acinar cells contribute to the molecular heterogeneity of pancreatic intraepithelial neoplasia. Am J Pathol 2007, 171(1):263-273. 10.2353/ajpath.2007.061176, 1941579, 17591971.