VEGF-C mediates RhoGDI2-induced gastric cancer cell metastasis and cisplatin resistance

International Journal of Cancer

Volumn 135, Issue 7, 2014, Pages 1553-1563

  Jun Cho, Hee ^a   Kim, In Kyu ^a   Park, Sun Mi ^a   Eun Baek, Kyoung ^a   Nam, In Koo ^a   Park, Seung Ho ^a   Ryu, Ki Jun ^a   Choi, Jungil ^a   Ryu, Jinhyun ^a   Hong, Soon Chan ^a   Jeong, Sang Ho ^a   Lee, Young Joon ^a   Ko, Gyung Hyuck ^a   Won Kim, Jae ^a   Won Lee, Chang ^a   Soo Kang, Sang ^a   Yoo, Jiyun ^a  

^a Gyeongsang National University   (South Korea)

Author keywords

chemoresistance; gastric cancer; metastasis; RhoGDI2; VEGF C

Indexed keywords

ANTINEOPLASTIC AGENT; CISPLATIN; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; VASCULOTROPIN C;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOGENICITY; CELL INVASION; CONTROLLED STUDY; DRUG EFFICACY; DRUG SENSITIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STOMACH; STOMACH CANCER; TISSUE MICROARRAY; TUMOR GROWTH;

CHEMORESISTANCE; GASTRIC CANCER; METASTASIS; RHOGDI2; VEGF-C;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL PROLIFERATION; CHROMATIN IMMUNOPRECIPITATION; CISPLATIN; DRUG RESISTANCE, NEOPLASM; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOENZYME TECHNIQUES; LUNG NEOPLASMS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR BETA; RNA, MESSENGER; RNA, SMALL INTERFERING; STOMACH NEOPLASMS; TISSUE ARRAY ANALYSIS; TUMOR CELLS, CULTURED; VASCULAR ENDOTHELIAL GROWTH FACTOR C; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904461602     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28801     Document Type: Article

References (44)

1. Jemal A, Bray F, Center MM, et al. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Schmidt A, Hall A,. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev 2002; 16: 1587-609.
3. Moon SY, Zheng Y,. Rho GTPase-activation proteins in cell regulation. Trends Cell Biol 2003; 13: 13-22.
4. Fukomoto Y, Kaibuchi K, Hori Y, et al. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the Rho proteins, ras p21-like small GTP-binding proteins. Oncogene 1990; 5: 1321-8.
5. Scherle P, Behrens T, Staudt LM,. Ly-GDI, a GDP-dissociation inhibitor of the RhoA GTP-binding protein, is expressed preferentially in lymphocytes. Proc Natl Acad Sci USA 1993; 90: 7568-72.
6. Zalcman G, Closson V, Camonis J, et al. RhoGDI-3 is a new GDP dissociation inhibitor (GDI). Identification of a non-cytosolic GDI protein interacting with the small GTP-binding proteins RhoB and RhoG. J Biol Chem 1996; 271: 30366-74.
7. Gildea JJ, Seraj MJ, Oxford G, et al. RhoGDI2 is an invasion and metastasis suppressor gene in human cancer. Cancer Res 2002; 62: 6418-23.
8. Theodorescu D, Sapinoso LM, Conaway MR, et al. Reduced expression of metastasis suppressor RhoGDI2 is associated with decreased survival for patients with bladder cancer. Clin Cancer Res 2004; 10: 3800-6.
9. Tapper J, Kettunen E, El-Rifai W, et al. Changes in gene expression during progression of ovarian carcinoma. Cancer Genet Cytogenet 2001; 128: 1-6.
10. Zhang Y, Zhang B,. D4-GDI, a Rho GTPase regulator, promotes breast cancer cell invasiveness. Cancer Res 2006; 66: 5592-8.
11. Cho HJ, Baek KE, Yoo J,. RhoGDI2 as a therapeutic target in cancer. Expert Opin Ther Targets 2010; 14: 67-75.
12. Cho HJ, Baek KY, Park SM, et al. RhoGDI2 expression is associated with tumor growth and malignant progression of gastric cancer. Clin Cancer Res 2009; 15: 2612-9.
13. Cho HJ, Baek KE, Park SM, et al. RhoGDI2 confers gastric cancer cells resistance against cisplatin-induced apoptosis by upregulation of Bcl-2 expression. Cancer Lett 2011; 311: 48-56.
14. Zheng Z, He XY, Li JF, et al. RhoGDI2 confers resistance to 5-fluorouracil in human gastric cancer cells. Oncol Lett 2013; 5: 255-60.
15. Cao Y, Linden P, Farnebo J, et al. Vascular endothelial growth factor C induces angiogenesis in vivo. Proc Natl Acad Sci USA 1998; 95: 14389-94.
16. Jeltsch M, Kaipainen A, Joukov V, et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science 1997; 276: 1423-5.
17. Su JL, Yang PC, Shih JY, et al. The VEGF-C/Flt-4 promotes invasion and metastasis of cancer cells. Cancer Cell 2006; 9: 209-23.
18. Dias S, Choy M, Alitalo K, et al. Vascular endothelial growth factor (VEGF)-C signaling through FLT-4 (VEGFR-3) mediates leukemic cell proliferation, survival, and resistance to chemotherapy. Blood 2002; 99: 2179-84.
19. Su JL, Yen CJ, Chen PS, et al. The role of the VEGF-C/VEGFR-3 axis in cancer progression. Br J Cancer 2007; 96: 541-5.
20. Ferrara N, Davis-Smyth T,. The biology of vascular endothelial growth factor. Endocr Rev 1997; 18: 4-25.
21. Timoshenko AV, Rastogi S, Lala PK,. Migration-promoting role of VEGF-C and VEGF-C binding receptors in human breast cancer cells. Br J Cancer 2007; 97: 1090-8.
22. DerMardirossian C, Bokoch GM,. GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol 2005; 15: 356-63.
23. Zhang Y, Rivera Rosado LA, Moon SY, et al. Silencing of D4-GDI inhibits growth and invasive behavior in MDA-MB-231 cells by activation of Rac-dependent p38 and JNK signalling. J Biol Chem 2009; 284: 12956-65.
24. Moissoglu K, McRoberts KS, Meier JA, et al. Rho GDP dissociation inhibitor 2 suppresses metastasis via unconventional regulation of Rho GTPases. Cancer Res 2009; 69: 2838-44.
25. Tsai PW, Shiah SG, Lin MT, et al. Up-regulation of vascular endothelial growth factor C in breast cancer cells by heregulin-beta 1. A critical role of p38/nuclear factor-kappaB signaling pathway. J Biol Chem 2003; 278: 5750-9.
26. Catalano V, Labianca R, Beretta GD, et al. Gastric cancer. Crit Rev Oncol Hematol 2009; 19: 19.
27. Leonard D, Hart M, Platko J, et al. The identification and characterization of a GDP-dissociation inhibitor (GDI) for the Cdc42Hs protein. J Biol Chem 1992; 267: 22860-8.
28. Katzav S, Martin-Zanca D, Barbacid M,. vav, a novel human oncogene derived from a locus ubiquitously expressed in hematopoietic cells. EMBO J 1989; 8: 2283-90.
29. Bustelo XR,. Regulatory and signaling properties of the Vav family. Mol Cell Biol 2000; 20: 1461-77.
30. Groysman M, Hornstein I, Alcover A, et al. Vav1 and Ly-GDI two regulators of Rho GTPases, function cooperatively as signal transducers in T cell antigen receptor-induced pathways. J Biol Chem 2002; 277: 50121-30.
31. Watanabe T, Urano E, Miyauchi K, et al. The hematopoietic cell-specific Rho GTPase inhibitor ARHGDIB/D4GDI limits HIV type 1 replication. AIDS Res Hum Retroviruses 2012; 28: 913-22.
32. Mehta P, Wavreille AS, Justiniano SE, et al. LyGDI, a novel SHIP-interacting protein, is a negative regulator of FcγR-mediated phagocytosis. PLoS One 2011; 6: e21175.
33. Huang CY, Yang LC, Liu KY, et al. ZAK negatively regulates RhoGDIbeta-induced Rac1-mediated hypertrophic growth and cell migration. J Biomed Sci 2009; 16: 56.
34. Tsurusaki T, Kanda S, Sakai H, et al. Vascular endothelial growth factor-C expression in human prostatic carcinoma and its relationship to lymph node metastasis. Br J Cancer 1999; 80: 309-13.
35. Yonemura Y, Endo Y, Fujita H, et al. Role of vascular endothelial growth factor C expression in the development of lymph node metastasis in gastric cancer. Clin Cancer Res 1999; 5: 1823-9.
36. Akagi K, Ikeda Y, Miyazaki M, et al. Vascular endothelial growth factor-C (VEGF-C) expression in human colorectal cancer tissues. Br J Cancer 2000; 83: 887-91.
37. Kajita T, Ohta Y, Kimura K, et al. The expression of vascular endothelial growth factor C and its receptors in non-small cell lung cancer. Br J Cancer 2001; 85: 255-60.
38. Schunke D, Span P, Ronneburg H, et al. Cyclooxygenase-2 is a target gene of Rho GDP dissociation inhibitor beta in breast cancer cells. Cancer Res 2007; 67: 10694-702.
39. Su JL, Shih JY, Yen ML, et al. Cyclooxygenase-2 induces EP1- and HER-2/Neu-dependent vascular endothelial growth factor-C up-regulation: a novel mechanism of lymphangiogenesis in lung adenocarcinoma. Cancer Res 2004; 64: 554-64.
40. Lemoine NR, Jain S, Silvestre F, et al. Amplification and overexpression of the EGF receptor and c-erbB-2 proto-oncogenes in human stomach cancer. Br J Cancer 1991; 64: 79-83.
41. Kimura M, Tsuda H, Morita D, et al. Usefulness and limitation of multiple endoscopic biopsy sampling for epidermal growth factor receptor and c-erbB-2 testing in patients with gastric adenocarcinoma. Jpn J Clin Oncol 2005; 35: 324-31.
42. Kimura M, Tsuda H, Morita D, et al. A proposal for diagnostically meaningful criteria to classify increased epidermal growth factor receptor and c-erbB-2 gene copy numbers in gastric carcinoma, based on correlation of fluorescence in situ hybridization and immunohistochemical measurements. Virchows Arch 2004; 445: 255-62.
43. Kim MA, Lee HS, Lee HE, et al. EGFR in gastric carcinomas: prognostic significance of protein overexpression and high gene copy number. Histopathology 2008; 52: 738-46.
44. Bang YJ, Van Cutsem E, Feyereislova A, et al. Trastuzumab in combination with chemotherapy versus chemotherapy alone for treatment of HER2-positive advanced gastric or gastro-oesophageal junction cancer (ToGA): a phase 3, open-label, randomized controlled trial. Lancet 2010; 376: 687-97.