Phosphorylation of focal adhesion kinase at Tyr397 in gastric carcinomas and its clinical significance

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 1629-1637

  Lai, I Rue ^a,b   Chu, Pei Yu ^c   Lin, Hsiao Sheng ^c   Liou, Jun Yang ^d   Jan, Yee Jee ^e   Lee, Jen Chieh ^b   Shen, Tang Long ^c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e TAICHUNG VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE;

ADULT; AGED; ARTICLE; CANCER INVASION; CANCER RECURRENCE; CANCER SURVIVAL; CELL MIGRATION; CELL PROLIFERATION; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STOMACH CARCINOGENESIS; STOMACH CARCINOMA; TUMOR VOLUME; WESTERN BLOTTING;

EID: 77957350031     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100172     Document Type: Article

References (50)

1. Catalano V, Labianca R, Beretta GD, Gatta G, de Braud F, Van Cutsem E: Gastric cancer. Crit Rev Oncol Hematol 2009, 71:127-164
2. Wu CW, Lo SS, Shen KH, Hsieh MC, Chen JH, Chiang JH, Lin HJ, Li AF, Lui WY: Incidence and factors associated with recurrence patterns after intended curative surgery for gastric cancer. World J Surg 2003, 27:153-158
3. Yoo CH, Noh SH, Shin DW, Choi SH, Min JS: Recurrence following curative resection for gastric carcinoma. Br J Surg 2000, 87:236-242 (Pubitemid 30088655)
4. Schaller MD: Biochemical signals and biological responses elicited by the focal adhesion kinase. Biochim Biophys Acta 2001, 1540:1-21
5. Guan JL, Shalloway D: Regulation of focal adhesion-associated protein tyrosine kinase by both cellular adhesion and oncogenic transformation. Nature 1992, 358:690-692
6. Hanks SK, Calalb MB, Harper MC, Patel SK: Focal adhesion protein-tyrosine kinase phosphorylated in response to cell attachment to fibronectin. Proc Natl Acad Sci USA 1992, 89:8487-8491
7. Schaller MD, Borgman CA, Cobb BS, Vines RR, Reynolds AB, Parsons JT: pp125FAK a structurally distinctive protein-tyrosine kinase associated with focal adhesions. Proc Natl Acad Sci USA 1992, 89:5192-5196
8. Schlaepfer DD, Mitra SK, Ilic D: Control of motile and invasive cell phenotypes by focal adhesion kinase. Biochim Biophys Acta 2004, 1692:77-102
9. Schwock J, Dhani N, Hedley DW: Targeting focal adhesion kinase signaling in tumor growth and metastasis. Expert Opin Ther Targets 14:77-94
10. Akasaka T, van Leeuwen RL, Yoshinaga IG, Mihm MC Jr, Byers HR: Focal adhesion kinase (p125FAK) expression correlates with motility of human melanoma cell lines. J Invest Dermatol 1995, 105:104-108
11. Weiner TM, Liu ET, Craven RJ, Cance WG: Expression of focal adhesion kinase gene and invasive cancer. Lancet 1993, 342:1024-1025
12. McCormack SJ, Brazinski SE, Moore JL, Jr., Werness BA, Goldstein DJ: Activation of the focal adhesion kinase signal transduction pathway in cervical carcinoma cell lines and human genital epithelial cells immortalized with human papillomavirus type 18. Oncogene 1997, 15:265-274
13. Tremblay L, Hauck W, Aprikian AG, Begin LR, Chapdelaine A, Chevalier S: Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int J Cancer 1996, 68:164-171
14. Owens LV, Xu L, Craven RJ, Dent GA, Weiner TM, Kornberg L, Liu ET, Cance WG: Overexpression of the focal adhesion kinase (p125FAK) in invasive human tumors. Cancer Res 1995, 55:2752-2755
15. Judson PL, He X, Cance WG, Van Le L: Overexpression of focal adhesion kinase, a protein tyrosine kinase, in ovarian carcinoma. Cancer 1999, 86:1551-1556
16. Lark AL, Livasy CA, Calvo B, Caskey L, Moore DT, Yang X, Cance WG: Overexpression of focal adhesion kinase in primary colorectal carcinomas and colorectal liver metastases: immunohistochemistry and real-time PCR analyses. Clin Cancer Res 2003, 9:215-222
17. Kornberg LJ: Focal adhesion kinase and its potential involvement in tumor invasion and metastasis. Head Neck 1998, 20:745-752
18. Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark GM, Edge SB, Hayes DF, Hughes LL, Hutter RV, Morrow M, Page DL, Recht A, Theriault RL, Thor A, Weaver DL, Wieand HS, Greene FL: Staging system for breast cancer: revisions for the ed 6 of the AJCC Cancer Staging Manual. Surg Clin North Am 2003, 83:803-819
19. Jan YJ, Ko BS, Hsu C, Chang TC, Chen SC, Wang J, Liou JY: Overexpressed focal adhesion kinase predicts a higher incidence of extrahepatic metastasis and worse survival in hepatocellular carcinoma. Hum Pathol 2009, 40:1384-1390
20. Shen TL, Park AY, Alcaraz A, Peng X, Jang I, Koni P, Flavell RA, Gu H, Guan JL: Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J Cell Biol 2005, 169:941-952
21. Chu PY, Huang LY, Hsu CH, Liang CC, Guan JL, Hung TH, Shen TL: Tyrosine phosphorylation of growth factor receptor-bound protein-7 by focal adhesion kinase in the regulation of cell migration, proliferation, and tumorigenesis. J Biol Chem 2009, 284:20215-20226
22. Overall CM, Dean RA: Degradomics: systems biology of the protease web. Pleiotropic roles of MMPs in cancer. Cancer Metastasis Rev 2006, 25:69-75
23. Iiizumi M, Bandyopadhyay S, Pai SK, Watabe M, Hirota S, Hosobe S, Tsukada T, Miura K, Saito K, Furuta E, Liu W, Xing F, Okuda H, Kobayashi A, Watabe K: RhoC promotes metastasis via activation of the Pyk2 pathway in prostate cancer. Cancer Res 2008, 68:7613-7620
24. Itoh S, Maeda T, Shimada M, Aishima S, Shirabe K, Tanaka S, Maehara Y: Role of expression of focal adhesion kinase in progression of hepatocellular carcinoma. Clin Cancer Res 2004, 10:2812-2817
25. Imaizumi M, Nishimura M, Takeuchi S, Murase M, Hamaguchi M: Role of tyrosine specific phosphorylation of cellular proteins, especially EGF receptor and p125FAK in human lung cancer cells. Lung Cancer 1997, 17:69-84
26. Fujii T, Koshikawa K, Nomoto S, Okochi O, Kaneko T, Inoue S, Yatabe Y, Takeda S, Nakao A: Focal adhesion kinase is overexpressed in hepatocellular carcinoma and can be served as an independent prognostic factor. J Hepatol 2004, 41:104-111
27. Theocharis SE, Kouraklis GP, Kakisis JD, Kanelli HG, Apostolakou FE, Karatzas GM, Koutselinis AS: Focal adhesion kinase expression is not a prognostic predictor in colon adenocarcinoma patients. Eur J Surg Oncol 2003, 29:571-574
28. Gabriel B, zur Hausen A, Stickeler E, Dietz C, Gitsch G, Fischer DC, Bouda J, Tempfer C, Hasenburg A: Weak expression of focal adhesion kinase (pp125FAK) in patients with cervical cancer is associated with poor disease outcome. Clin Cancer Res 2006, 12:2476-2483
29. Chatzizacharias NA, Kouraklis GP, Theocharis SE: Clinical significance of FAK expression in human neoplasia. Histol Histopathol 2008, 23:629-650 (Pubitemid 351552349)
30. Yu HG, Tong SL, Ding YM, Ding J, Fang XM, Zhang XF, Liu ZJ, Zhou YH, Liu QS, Luo HS, Yu JP: Enhanced expression of cholecystokinin-2 receptor promotes the progression of colon cancer through activation of focal adhesion kinase. Int J Cancer 2006, 119:2724-2732 (Pubitemid 44846222)
31. Kassis J, Maeda A, Teramoto N, Takada K, Wu C, Klein G, Wells A: EBV-expressing AGS gastric carcinoma cell sublines present increased motility and invasiveness. Int J Cancer 2002, 99:644-651 (Pubitemid 34538742)
32. Peng L, Ran YL, Hu H, Yu L, Liu Q, Zhou Z, Sun YM, Sun LC, Pan J, Sun LX, Zhao P, Yang ZH: Secreted LOXL2 is a novel therapeutic target that promotes gastric cancer metastasis via the Src/FAK pathway. Carcinogenesis 2009, 30:1660-1669
33. Sieg DJ, Hauck CR, Ilic D, Klingbeil CK, Schaefer E, Damsky CH, Schlaepfer DD: FAK integrates growth-factor and integrin signals to promote cell migration. Nat Cell Biol 2000, 2:249-256
34. van Nimwegen MJ, van de Water B: Focal adhesion kinase: a potential target in cancer therapy. Biochem Pharmacol 2007, 73:597-609 (Pubitemid 46161372)
35. Su JM, Gui L, Zhou YP, Zha XL: Expression of focal adhesion kinase and alpha5 and beta1 integrins in carcinomas and its clinical significance. World J Gastroenterol 2002, 8:613-618 (Pubitemid 34918651)
36. Giaginis CT, Vgenopoulou S, Tsourouflis GS, Politi EN, Kouraklis GP, Theocharis SE: Expression and clinical significance of focal adhesion kinase in the two distinct histological types, intestinal and diffuse, of human gastric adenocarcinoma. Pathol Oncol Res 2009, 15:173-181
37. Murata T, Naomoto Y, Yamatsuji T, Okawa T, Shirakawa Y, Gunduz M, Nobuhisa T, Takaoka M, Sirmali M, Nakajima M, Ohno Y, Tanaka N: Localization of FAK is related with colorectal carcinogenesis. Int J Oncol 2008, 32:791-796 (Pubitemid 351780589)
38. Schlaepfer DD, Hauck CR, Sieg DJ: Signaling through focal adhesion kinase. Prog Biophys Mol Biol 1999, 71:435-478
39. Zhao J, Guan JL: Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 2009, 28:35-49
40. Tsutsumi R, Takahashi A, Azuma T, Higashi H, Hatakeyama M: Focal adhesion kinase is a substrate and downstream effector of SHP-2 complexed with Helicobacter pylori CagA. Mol Cell Biol 2006, 26:261-276
41. Tamura M, Gu J, Tran H, Yamada KM: PTEN gene and integrin signaling in cancer. J Natl Cancer Inst 1999, 91:1820-1828
42. Rigacci S, Rovida E, Sbarba PD, Berti A: Low Mr phosphotyrosine protein phosphatase associates and dephosphorylates p125 focal adhesion kinase, interfering with cell motility and spreading. J Biol Chem 2002, 277:41631-41636 (Pubitemid 35257468)
43. Zheng Y, Xia Y, Hawke D, Halle M, Tremblay ML, Gao X, Zhou XZ, Aldape K, Cobb MH, Xie K, He J, Lu Z: FAK phosphorylation by ERK primes ras-induced tyrosine dephosphorylation of FAK mediated by PIN1 and PTP-PEST. Mol Cell 2009, 35:11-25
44. Zeng L, Si X, Yu WP, Le HT, Ng KP, Teng RM, Ryan K, Wang DZ, Ponniah S, Pallen CJ: PTP alpha regulates integrin-stimulated FAK autophosphorylation and cytoskeletal rearrangement in cell spreading and migration. J Cell Biol 2003, 160:137-146 (Pubitemid 36091723)
45. Sieg DJ, Ilic D, Jones KC, Damsky CH, Hunter T, Schlaepfer DD: Pyk2 and Src-family protein-tyrosine kinases compensate for the loss of FAK in fibronectin-stimulated signaling events but Pyk2 does not fully function to enhance FAK- cell migration. EMBO J 1998, 17:5933-5947 (Pubitemid 28474788)
46. Weis SM, Lim ST, Lutu-Fuga KM, Barnes LA, Chen XL, Gothert JR, Shen TL, Guan JL, Schlaepfer DD, Cheresh DA: Compensatory role for Pyk2 during angiogenesis in adult mice lacking endothelial cell FAK. J Cell Biol 2008, 181:43-50
47. Behmoaram E, Bijian K, Jie S, Xu Y, Darnel A, Bismar TA, Alaoui-Jamali MA: Focal adhesion kinase-related proline-rich tyrosine kinase 2 and focal adhesion kinase are co-overexpressed in early-stage and invasive ErbB-2-positive breast cancer and cooperate for breast cancer cell tumorigenesis and invasiveness. Am J Pathol 2008, 173:1540-1550
48. Ayaki M, Komatsu K, Mukai M, Murata K, Kameyama M, Ishiguro S, Miyoshi J, Tatsuta M, Nakamura H: Reduced expression of focal adhesion kinase in liver metastases compared with matched primary human colorectal adenocarcinomas. Clin Cancer Res 2001, 7:3106-3112 (Pubitemid 32963831)
49. Lu Z, Jiang G, Blume-Jensen P, Hunter T: Epidermal growth factor-induced tumor cell invasion and metastasis initiated by dephosphorylation and downregulation of focal adhesion kinase. Mol Cell Biol 2001, 21:4016-4031 (Pubitemid 32476463)
50. Zheng Y, Lu Z: Paradoxical roles of FAK in tumor cell migration and metastasis. Cell Cycle 2009, 8:3474-3479