Cancer Letters
Volume 290, Issue 2 , Pages 238-247 , 28 April 2010

Upregulated fascin1 in non-small cell lung cancer promotes the migration and invasiveness, but not proliferation

  • Jinbo Zhao

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
    • These authors contributed equally to this work.
  • ,
  • Yongan Zhou

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
    • These authors contributed equally to this work.
  • ,
  • Zhipei Zhang

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
  • ,
  • Feng Tian

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
  • ,
  • Nan Ma

      Affiliations

    • Department of Ophthalmology, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
  • ,
  • Tonggang Liu

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
  • ,
  • Zhongping Gu

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
  • ,
  • Yunjie Wang

      Affiliations

    • Department of Thoracic Surgery, Tangdu Hospital, Forth Military Medical University, Xi’an 710038, China
    • Corresponding Author InformationCorresponding author. Address: Department of Thoracic Surgery, Tangdu Hospital, 1 Xin Si Road, Xi’an 710038, Shannxi, China. Tel.: +86 29 84777827; fax: +86 29 84777838.

Received 8 July 2009 ,Revised 17 September 2009 ,Accepted 17 September 2009.

References 

  1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, et al. Cancer statistics, 2008. CA Cancer J. Clin. 2008;58:71–96
  2. Scagliotti G. Consensus development conference on the medical treatment of non-small cell lung cancer: treatment of the early stages. Lung Cancer. 2002;38(suppl. 3):S23–S29
  3. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127:679–695
  4. Friedl P, Wolf K. Tumour-cell invasion, migration: diversity and escape mechanisms. Nat. Rev. Cancer. 2003;3:362–374
  5. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell. 2003;112:453–465
  6. Adams JC. Fascin protrusions in cell interactions. Trends Cardiovas. Med. 2004;14:221–226
  7. Adams JC. Roles of fascin in cell adhesion and motility. Curr. Opin. Cell Biol. 2004;16:590–596
  8. Kane RE. Preparation and purification of polymerized actin from sea urchin egg extracts. J. Cell Biol. 1975;66:305–315
  9. Hashimoto Y, Skacel M, Adams JC. Roles of fascin in human carcinoma motility and signaling: prospects for a novel biomarker?. Int. J. Biochem. Cell Biol. 2005;37:1787–1804
  10. Hashimoto Y, Ito T, Inoue H, Okumura T, Tanaka E, Tsunoda S, et al. Prognostic significance of fascin overexpression in human esophageal squamous cell carcinoma. Clin. Cancer Res. 2005;11:2597–2605
  11. Zhang H, Xu L, Xiao D, Xie J, Zeng H, Cai W, et al. Fascin is a potential biomarker for early-stage oesophageal squamous cell carcinoma. J. Clin. Pathol. 2006;59:958–964
  12. Hsu KF, Lin CK, Yu CP, Tzao C, Lee SC, Lee YY, et al. Cortactin, fascin, and survivin expression associated with clinicopathological parameters in esophageal squamous cell carcinoma. Dis. Esophagus. 2009;22:402–408
  13. Hashimoto Y, Shimada Y, Kawamura J, Yamasaki S, Imamura M. The prognostic relevance of fascin expression in human gastric carcinoma. Oncology. 2004;67:262–270
  14. Tsai WC, Jin JS, Chang WK, Chan DC, Yeh MK, Cherng SC, et al. Association of cortactin and fascin-1 expression in gastric adenocarcinoma: correlation with clinicopathological parameters. J. Histochem. Cytochem. 2007;55:955–962
  15. Li X, Zheng H, Hara T, Takahashi H, Masuda S, Wang Z, et al. Aberrant expression of cortactin and fascin are effective markers for pathogenesis, invasion, metastasis and prognosis of gastric carcinomas. Int. J. Oncol. 2008;33:69–79
  16. Jawhari AU, Buda A, Jenkins M, Shehzad K, Sarraf C, Noda M, et al. Fascin, an actin-bundling protein, modulates colonic epithelial cell invasiveness and differentiation in vitro. Am. J. Pathol. 2003;162:69–80
  17. Puppa G, Maisonneuve P, Sonzogni A, Masullo M, Chiappa A, Valerio M, et al. Independent prognostic value of fascin immunoreactivity in stage III–IV colonic adenocarcinoma. Brit. J. Cancer. 2007;96:1118–1126
  18. Maitra A, Iacobuzio-Donahue C, Rahman A, Sohn TA, Argani P, Meyer R, et al. Immunohistochemical validation of a novel epithelial and a novel stromal marker of pancreatic ductal adenocarcinoma identified by global expression microarrays: sea urchin fascin homolog and heat shock protein 47. Am. J. Clin. Pathol. 2002;118:52–59
  19. Yamaguchi H, Inoue T, Eguchi T, Miyasaka Y, Ohuchida K, Mizumoto K, et al. Fascin overexpression in intraductal papillary mucinous neoplasms (adenomas, borderline neoplasms, and carcinomas) of the pancreas, correlated with increased histological grade. Mod. Pathol. 2007;20:552–561
  20. Yoder BJ, Tso E, Skacel M, Pettay J, Tarr S, Budd T, et al. The expression of fascin, an actin-bundling motility protein, correlates with hormone receptor-negative breast cancer and a more aggressive clinical course. Clin. Cancer Res. 2005;11:186–192
  21. Rodriguez-Pinilla SM, Sarrio D, Honrado E, Hardisson D, Calero F, Benitez J, et al. Prognostic significance of basal-like phenotype and fascin expression in node-negative invasive breast carcinomas. Clin. Cancer Res. 2006;12:1533–1539
  22. Daponte A, Kostopoulou E, Minas M, Koukoulis G, Messinis IE. Prognostic significance of fascin expression in advanced poorly differentiated serous ovarian cancer. Anticancer Res. 2008;28:1905–1910
  23. Wen YH, Yee H, Goswami S, Shukla PS. Fascin expression in serous tumors of ovary correlates with aggressiveness of malignancy. Int. J. Gynecol. Pathol. 2009;28:187–192
  24. Goncharuk VN, Ross JS, Carlson JA. Actin-binding protein fascin expression in skin neoplasia. J. Cutan. Pathol. 2002;29:430–438
  25. Sonderbye L, Meehan S, Palsson R, Ahsan N, Ladefoged J, Langhoff E. Immunohistochemical study of actin binding protein (p55) in the human kidney. Transplantation. 1998;65:1004–1008
  26. Chen G, Zhang FR, Ren J, Tao LH, Shen ZY, Lv Z, et al. Expression of fascin in thyroid neoplasms: a novel diagnostic marker. J. Cancer Res. Clin. Oncol. 2008;134:947–951
  27. Kabukcuoglu S, Ozalp SS, Oner U, Acikalin MF, Yalcin OT, Colak E. Fascin, an actin-bundling protein expression in cervical neoplasms. Eur. J. Gynaecol. Oncol. 2005;26:636–641
  28. Darnel AD, Behmoaram E, Vollmer RT, Corcos J, Bijian K, Sircar K, et al. Fascin regulates prostate cancer cell invasion and is associated with metastasis and biochemical failure in prostate cancer. Clin. Cancer Res. 2009;15:1376–1383
  29. Gunal A, Onguru O, Safali M, Beyzadeoglu M. Fascin expression [corrected] in glial tumors and its prognostic significance in glioblastomas. Neuropathology. 2008;28:382–386
  30. Hwang JH, Smith CA, Salhia B, Rutka JT. The role of fascin in the migration and invasiveness of malignant glioma cells. Neoplasia. 2008;10:149–159
  31. Soukup V, Babjuk M, Duskova J, Pesl M, Szakaczova M, Zamecnik L, et al. Does the expression of fascin-1 and tumor subclassification help to assess the risk of recurrence and progression in t1 urothelial urinary bladder carcinoma?. Urol. Int. 2008;80:413–418
  32. Pelosi G, Pastorino U, Pasini F, Maissoneuve P, Fraggetta F, Iannucci A, et al. Independent prognostic value of fascin immunoreactivity in stage I nonsmall cell lung cancer. Brit. J. Cancer. 2003;88:537–547
  33. Pelosi G, Pasini F, Fraggetta F, Pastorino U, Iannucci A, Maisonneuve P, et al. Independent value of fascin immunoreactivity for predicting lymph node metastases in typical and atypical pulmonary carcinoids. Lung Cancer. 2003;42:203–213
  34. Choi PJ, Yang DK, Son CH, Lee KE, Lee JI, Roh MS. Fascin immunoreactivity for preoperatively predicting lymph node metastases in peripheral adenocarcinoma of the lung 3 cm or less in diameter. Eur. J. Cardio – Thorac. Surg. 2006;30:538–542
  35. Xie JJ, Xu LY, Zhang HH, Cai WJ, Mai RQ, Xie YM, et al. Role of fascin in the proliferation and invasiveness of esophageal carcinoma cells. Biochem. Biophys. Res. Commun. 2005;337:355–362
  36. Adiseshaiah P, Lindner DJ, Kalvakolanu DV, Reddy SP. FRA-1 proto-oncogene induces lung epithelial cell invasion and anchorage-independent growth in vitro, but is insufficient to promote tumor growth in vivo. Cancer Res. 2007;67:6204–6211
  37. Hashimoto Y, Skacel M, Lavery IC, Mukherjee AL, Casey G, Adams JC. Prognostic significance of fascin expression in advanced colorectal cancer: an immunohistochemical study of colorectal adenomas and adenocarcinomas. BMC Cancer. 2006;6:241
  38. Kabukcuoglu S, Oner U, Ozalp SS, Dundar E, Yalcin OT, Colak E. Prognostic significance of fascin expression in endometrioid carcinoma. Eur. J. Gynaecol. Oncol. 2006;27:481–486
  39. Kureishy N, Sapountzi V, Prag S, Anilkumar N, Adams JC. Fascins, and their roles in cell structure and function. Bioessays. 2002;24:350–361
  40. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG. Role of fascin in filopodial protrusion. J. Cell Biol. 2006;174:863–875
  41. Aratyn YS, Schaus TE, Taylor EW, Borisy GG. Intrinsic dynamic behavior of fascin in filopodia. Mol. Biol. Cell. 2007;18:3928–3940
  42. Vignjevic D, Schoumacher M, Gavert N, Janssen KP, Jih G, Lae M, et al. Fascin, a novel target of beta-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res. 2007;67:6844–6853
  43. Grothey A, Hashizume R, Ji H, Tubb BE, Patrick CW, Yu D, et al. C-erbB-2/HER-2 upregulates fascin, an actin-bundling protein associated with cell motility, in human breast cancer cell lines. Oncogene. 2000;19:4864–4875
  44. Guvakova MA, Boettiger D, Adams JC. Induction of fascin spikes in breast cancer cells by activation of the insulin-like growth factor-I receptor. Int. J. Biochem. Cell Biol. 2002;34:685–698
  45. Shonukan O, Bagayogo I, McCrea P, Chao M, Hempstead B. Neurotrophin-induced melanoma cell migration is mediated through the actin-bundling protein fascin. Oncogene. 2003;22:3616–3623
  46. Ramires M, David L, Leitao D, Seixas M, Sansonetty F, Sobrinho-Simoes M. Ki67 labelling index in gastric carcinomas. An immunohistochemical study using double staining for the evaluation of the proliferative activity of diffuse-type carcinomas. J. Pathol. 1997;182:62–67
  47. Jung A, Schrauder M, Oswald U, Knoll C, Sellberg P, Palmqvist R, et al. The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation. Am. J. Pathol. 2001;159:1613–1617
  48. Hou Y, Yang L, Mou M, Hou Y, Zhang A, Pan N, et al. Annexin A2 regulates the levels of plasmin, S100A10 and fascin in L5178Y cells. Cancer Invest. 2008;26:809–815
  49. Wong V, Ching D, McCrea PD, Firestone GL. Glucocorticoid down-regulation of fascin protein expression is required for the steroid-induced formation of tight junctions and cell–cell interactions in rat mammary epithelial tumor cells. J. Biol. Chem. 1999;274:5443–5453
  50. Guan Y, Woo PL, Rubenstein NM, Firestone GL. Transforming growth factor-alpha abrogates the glucocorticoid stimulation of tight junction formation and reverses the steroid-induced down-regulation of fascin in rat mammary epithelial tumor cells by a Ras-dependent pathway. Exp. Cell Res. 2002;273:1–11
  51. Zhang S, Lin QD, DI W. Suppression of human ovarian carcinoma metastasis by the metastasis-suppressor gene, BRMS1. Int. J. Gynecol. Cancer. 2006;16:522–531
  52. Hashimoto Y, Loftis DW, Adams JC. Fascin-1 promoter activity is regulated by CREB and the aryl hydrocarbon receptor in human carcinoma cells. PLoS ONE. 2009;4:e5130
  53. Anilkumar N, Parsons M, Monk R, Ng T, Adams JC. Interaction of fascin and protein kinase C alpha: a novel intersection in cell adhesion and motility. EMBO J. 2003;22:5390–5402
  54. Ono S, Yamakita Y, Yamashiro S, Matsudaira PT, Gnarra JR, Obinata T, et al. Identification of an actin binding region and a protein kinase C phosphorylation site on human fascin. J. Biol. Chem. 1997;272:2527–2533
  55. Hashimoto Y, Parsons M, Adams JC. Dual actin-bundling and protein kinase C-binding activities of fascin regulate carcinoma cell migration downstream of Rac and contribute to metastasis. Mol. Biol. Cell. 2007;18:4591–4602
  56. Adams JC, Schwartz MA. Stimulation of fascin spikes by thrombospondin-1 is mediated by the GTPases Rac and Cdc42. J. Cell Biol. 2000;150:807–822
  57. Parsons M, Adams JC. Rac regulates the interaction of fascin with protein kinase C in cell migration. J. Cell Sci. 2008;121:2805–2813
  58. Adams JC, Clelland JD, Collett GD, Matsumura F, Yamashiro S, Zhang L. Cell–matrix adhesions differentially regulate fascin phosphorylation. Mol. Biol. Cell. 1999;10:4177–4190
  59. Ishikawa R, Yamashiro S, Kohama K, Matsumura F. Regulation of actin binding and actin bundling activities of fascin by caldesmon coupled with tropomyosin. J. Biol. Chem. 1998;273:26991–26997

PII: S0304-3835(09)00601-6

doi: 10.1016/j.canlet.2009.09.013

Cancer Letters
Volume 290, Issue 2 , Pages 238-247 , 28 April 2010