Proteomics-based strategy to delineate the molecular mechanisms of RhoGDI2-induced metastasis and drug resistance in gastric cancer

Journal of Proteome Research

Volumn 11, Issue 4, 2012, Pages 2355-2364

  Cho, Hee Jun ^a   Baek, Kyoung Eun ^a   Kim, In Kyu ^a   Park, Sun Mi ^a   Choi, Yeong Lim ^a   Nam, In Koo ^a   Park, Seung Ho ^a   Im, Min Ju ^a   Yoo, Jong Min ^a   Ryu, Ki Jun ^a   Oh, Young Taek ^a   Hong, Soon Chan ^b   Kwon, Oh Hyung ^c   Kim, Jae Won ^a   Lee, Chang Won ^a   Yoo, Jiyun ^a  

^a Gyeongsang National University   (South Korea)

^b Gyeongsang National University School of Medicine   (South Korea)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

cathepsin D; CIAPIN1; cisplatin resistance; gastric cancer; invasion; metastasis; PAK2; RhoGDI2

Indexed keywords

CATHEPSIN D; COFILIN 1; GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR; P21 ACTIVATED KINASE 2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL CULTURE; CELL INVASION; CONTROLLED STUDY; DRUG RESISTANCE; HUMAN; HUMAN CELL; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; STOMACH CANCER; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING;

CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GUANINE NUCLEOTIDE DISSOCIATION INHIBITORS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEOPLASM METASTASIS; P21-ACTIVATED KINASES; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; STOMACH NEOPLASMS; UP-REGULATION;

EID: 84859571571     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2011186     Document Type: Article

References (55)

1. Barocas, D. A.; Clark, P. E. Bladder cancer Curr. Opin. Oncol. 2008, 20 (3) 307-14
2. Ferraldeschi, R.; Baka, S.; Jyoti, B.; Faivre-Finn, C.; Thatcher, N.; Lorigan, P. Modern management of small-cell lung cancer Drugs 2007, 67 (15) 2135-52
3. Kelland, L. The resurgence of platinum-based cancer chemotherapy Nat. Rev. Cancer 2007, 7 (8) 573-84
4. Moehler, M.; Galle, P. R.; Gockel, I.; Junginger, T.; Schmidberger, H. The multidisciplinary management of gastrointestinal cancer. Multimodal treatment of gastric cancer Best Pract. Res. Clin. Gastroenterol. 2007, 21 (6) 965-81
5. Yuan, J. N.; Chao, Y.; Lee, W. P.; Li, C. P.; Lee, R. C.; Chang, F. Y.; Yen, S. H.; Lee, S. D.; Whang-Peng, J. Chemotherapy with etoposide, doxorubicin, cisplatin, 5-fluorouracil, and leucovorin for patients with advanced hepatocellular carcinoma Med. Oncol. 2008, 25 (2) 201-6
6. Andrews, P. A.; Jones, J. A.; Varki, N. M.; Howell, S. B. Rapid emergence of acquired cis-diamminedichloroplatinum(II) resistance in an in vivo model of human ovarian carcinoma Cancer Commun. 1990, 2 (2) 93-100
7. Etienne-Manneville, S.; Hall, A. Rho GTPases in cell biology Nature 2002, 420 (6916) 629-35
8. Sahai, E.; Marshall, C. J. RHO-GTPases and cancer Nat. Rev. Cancer 2002, 2 (2) 133-42
9. Lozano, E.; Betson, M.; Braga, V. M. Tumor progression: Small GTPases and loss of cell-cell adhesion Bioessays 2003, 25 (5) 452-63
10. Van Aelst, L.; DSouza-Schorey, C. Rho GTPases and signaling networks Genes Dev. 1997, 11 (18) 2295-322
11. Ueda, T.; Kikuchi, A.; Ohga, N.; Yamamoto, J.; Takai, Y. Purification and characterization from bovine brain cytosol of a novel regulatory protein inhibiting the dissociation of GDP from and the subsequent binding of GTP to rhoB p20, a ras p21-like GTP-binding protein J. Biol. Chem. 1990, 265 (16) 9373-80
12. Fukomoto, Y.; Kaibuchi, K.; Hori, Y.; Fujioka, H.; Araki, S.; Ueda, T.; Kikuchi, A.; Takai, Y. 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 (9) 1321-8
13. Dovas, A.; Couchman, J. R. RhoGDI: Multiple functions in the regulation of Rho family GTPase activities Biochem. J. 2005, 390 (1) 1-9
14. Leonard, D.; Hart, M. J.; Platko, J. V.; Eva, A.; Henzel, W.; Evans, T.; Cerione, R. A. The identification and characterization of a GDP-dissociation inhibitor (GDI) for the CDC42Hs protein J. Biol. Chem. 1992, 267 (32) 22860-8
15. Zalcman, G.; Closson, V.; Camonis, J.; Honoré, N.; Rousseau-Merck, M. F.; Tavitian, A.; Olofsson, B. 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 (48) 30366-74
16. Adra, C. N.; Manor, D.; Ko, J. L.; Zhu, S.; Horiuchi, T.; Van Aelst, L.; Cerione, R. A.; Lim, B. RhoGDIγ: A GDP-dissociation inhibitor for Rho proteins with preferential expression in brain and pancreas Proc. Natl. Acad. Sci. U.S.A. 1997, 94 (9) 4279-84
17. Lelias, J. M.; Adra, C. N.; Wulf, G. M.; Guillemot, J. C.; Khagad, M.; Caput, D; Lim, B. cDNA cloning of a human mRNA preferentially expressed in hematopoietic cells and with homology to a GDP-dissociation inhibitor for the rho GTP-binding proteins Proc. Natl. Acad. Sci. U.S.A. 1993, 90 (4) 1479-83
18. Scherle, P.; Behrens, T.; Staudt, L. M. Ly-GDI, a GDP-dissociation inhibitor of the RhoA GTP-binding protein, is expressed preferentially in lymphocytes Proc. Natl. Acad. Sci. U.S.A. 1993, 90 (16) 7568-72
19. Tapper, J.; Kettunen, E.; El-Rifai, W.; Seppala, M.; Andersson, L. C.; Knuutila, S. Changes in gene expression during progression of ovarian carcinoma Cancer Genet. Cytogenet. 2001, 128 (1) 1-6
20. Zhang, Y.; Zhang, B. D4-GDI, a Rho GTPase regulator, promotes breast cancer cell invasiveness Cancer Res. 2006, 66 (11) 5592-8
21. Cho, H. J.; Baek, K. E.; Park, S. M.; Kim, I. K.; Choi, Y. L.; Cho, H. J.; Nam, I. K.; Hwang, E. M.; Park, J. Y.; Han, J. Y.; Kang, S. S.; Kim, D. C.; Lee, W. S.; Lee, M. N.; Oh, G. T.; Kim, J. W.; Lee, C. W.; Yoo, J. RhoGDI2 expression is associated with tumor growth and malignant progression of gastric cancer Clin. Cancer Res. 2009, 15 (8) 2612-9
22. Cho, H. J.; Baek, K. E.; Park, S. M.; Kim, I. K.; Nam, I. K.; Choi, Y. L.; Park, S. H.; Im, M. J.; Choi, J.; Ryu, J.; Kim, J. W.; Lee, C. W.; Kang, S. S.; Yoo, J. RhoGDI2 confers gastric cancer cells resistance against cisplatin-induced apoptosis by upregulation of Bcl-2 expression Cancer Lett. 2011, 311 (1) 48-56
23. Kim, J.; Kim, S. H.; Lee, S. U.; Ha, G. H.; Kang, D. G.; Ha, N. Y.; Ahn, J. S.; Cho, H. Y.; Kang, S. J.; Lee, Y. J.; Hong, S. C.; Ha, W. S.; Bae, J. M.; Lee, C. W.; Kim, J. W. Proteome analysis of human liver tumor tissue by two-dimensional gel electrophoresis and matrix assisted laser desorption/ionization-mass spectrometry for identification of disease-related proteins Electrophoresis 2002, 23 (24) 4142-56
24. Neuhoff, V.; Arold, N.; Taube, D.; Ehrhardt, W. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250 Electrophoresis 1988, 9 (6) 255-62
25. Ha, G. H.; Lee, S. U.; Kang, D. G.; Ha, N. Y.; Kim, S. H.; Kim, J.; Bae, J. M.; Kim, J. W.; Lee, C. W. Proteome analysis of human stomach tissue: Separation of soluble proteins by two-dimensional polyacrylamide gel electrophoresis and identification by mass spectrometry Electrophoresis 2002, 23 (15) 2513-24
26. Landry, F.; Lombardo, C. R.; Smith, J. W. A method for application of samples to matrix-assisted laser desorption ionization time-of-flight targets that enhances peptide detection Anal. Biochem. 2000, 279 (1) 1-8
27. Peri, S.; Navarro, J. D.; Amanchy, R.; Kristiansen, T. Z.; Jonnalagadda, C. K.; Surendranath, V.; Niranjan, V.; Muthusamy, B.; Gandhi, T. K.; Gronborg, M.; Ibarrola, N.; Deshpande, N.; Shanker, K.; Shivashankar, H. N.; Rashmi, B. P.; Ramya, M. A.; Zhao, Z.; Chandrika, K. N.; Padma, N.; Harsha, H. C.; Yatish, A. J.; Kavitha, M. P.; Menezes, M.; Choudhury, D. R.; Suresh, S.; Ghosh, N.; Saravana, R.; Chandran, S.; Krishna, S.; Joy, M.; Anand, S. K.; Madavan., V.; Joseph, A.; Wong, G. W.; Schiemann, W. P.; Constantinescu, S. N.; Huang, L.; Khosravi-Far, R.; Steen, H.; Tewari, M.; Ghaffari, S.; Blobe, G. C.; Dang, C. V.; Garcia, J. G.; Pevsner, J.; Jensen, O. N.; Roepstorff, P.; Deshpande, K. S.; Chinnaiyan, A. M.; Hamosh, A.; Chakravarti, A.; Pandey, A. Development of human protein reference database as an initial platform for approaching systems biology in humans Genome Res. 2003, 13 (10) 2363-71
28. Hall, A. Rho GTPases and the actin cytoskeleton Science 1998, 279 (5350) 509-14
29. Bokoch, G. M. Biology of the p21-activated kinases Annu. Rev. Biochem. 2003, 72, 743-81
30. Vadlamudi, R. K.; Kumar, R. p21-activated kinases in human cancer Cancer Metastasis Rev. 2003, 22 (4) 385-93
31. Kumar, R.; Hung, M. C. Signaling intricacies take center stage in cancer cells Cancer Res. 2005, 65 (7) 2511-5
32. Kumar, R.; Gururaj, A. E.; Barnes, C. J. p21-activated kinases in cancer Nat. Rev. Cancer 2006, 6 (6) 459-71
33. Mira, J. P.; Benard, V.; Groffen, J.; Sanders, L. C.; Knaus, U. G. Endogenous, hyperactive Rac3 controls proliferation of breast cancer cells by a p21-activated kinases-dependent pathway Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (1) 185-9
34. Stofega, M. R.; Sanders, L. C.; Gardiner, E. M.; Bokoch, G. M. Constitutive p21-activated kinases (PAK) activation in breast cancer cells as a results of mislocalization of PAK to focal adhesions Mol. Biol. Cell 2004, 15 (6) 2965-77
35. Vadlamudi, R. K.; Adam, L.; Wang, R. A.; Mandal, M.; Nguyen, D.; Sahin, A.; Chernoff, J.; Hung, M. C.; Kumar, R. Regulatable expression of p21-activated kinases-1 promotes anchorage-independent growth and abnormal organization of mitotic spindles in human epithelial breast cancer cells J. Biol. Chem. 2000, 275 (46) 36238-44
36. Marlin, J. W.; Eaton, A.; Montano, G. T.; Chang, Y-W. E.; Jakobi, R. Elevated p21-activated kinase 2 activity results in anchorage-independent growth and resistance to anticancer drug-induced cell death Neoplasia 2009, 11 (3) 286-97
37. Shibayama, H.; Takai, E.; Matsumura, I.; Kouno, M.; Morii, E.; Kitamura, Y.; Takeda, J.; Kanakura, Y. Identification of a cytokine-induced antiapoptotic molecule anamorsin essential for definitive hematopoiesis J. Exp. Med. 2004, 199 (4) 581-92
38. Hao, Z.; Li, X.; Qiao, T.; Du, R.; Hong, L.; Fan, D. CIAPIN1 confers multidrug resistance by upregulating the expression of MDR-1 and MRP-1 in gastric cancer cells Cancer Biol. Ther. 2006, 5 (3) 261-6
39. Li, X.; Hong, L.; Zhao, Y.; Jin, H.; Fan, R.; Du, R.; Xia, L.; Luo, G.; Fan, D. A new apoptosis inhibitor, CIAPIN1 (cytokine induced apoptosis inhibitor 1), mediates multidrug resistance in leukemia cells by regulating MDR-1, Bcl-2, and Bax Biochem. Cell Biol. 2007, 85 (6) 741-50
40. Li, X.; Fan, R.; Zou, X.; Hong, L.; Gao, L.; Jin, H.; Du, R.; He, L.; Xia, L.; Fan, D. Reversal of multidrug resistance of gastric cancer cells by down-regulation of CIAPIN1 with CIAPIN1 siRNA Mol. Biol. (Mosk) 2008, 42 (1) 102-9
41. Li, X.; Wu, K.; Fan, D. CIAPIN1 as therapeutic target in cancer Expert Opin. Ther. Targets 2010, 14 (6) 603-10
42. Li, X.; Pan, Y.; Fan, R.; Jin, H.; Han, S.; Liu, J.; Wu, K.; Fan, D. Adenovirus-delivered CIAPIN1 small interfering RNA inhibits HCC growth in vitro and in vivo Carcinogenesis 2008, 29 (8) 1587-93
43. Garman, K. S.; Acharya, C. R.; Edelman, E.; Grade, M.; Gaedcke, J.; Sud, S.; Barry, W.; Diehl, A. M.; Provenzale, D.; Ginsburg, G. S.; Ghadimi, B. M.; Ried, T.; Nevins, J. R.; Mukherjee, S.; Hsu, D.; Potti, A. A genomic approach to colon cancer risk stratification yields biologic insights into therapeutic opportunities Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (49) 19432-7
44. Vincent-Salomon, A.; Lucchesi, C.; Gruel, N.; Raynal, V.; Pierron, G.; Goudefroye, R.; Reyal, F.; Radvanyi, F.; Salmon, R.; Thiery, J. P.; Sastre-Garau, X.; Sigal-Zafrani, B.; Fourquet, A.; Delattre, O. Integrated genomic and transcriptomic analysis of ductal carcinoma in situ of the breast Cancer Res. 2008, 14 (7) 1956-65
45. Yan, K.; He, L. J.; Cheng, W.; Ji, Z. Z.; Zhao, B. X.; Hui, X. L.; Cao, S. S.; Chen, B.; He, L.; Liang, S. H.; Miao, Y. Inhibiting gastric cancer-associated angiogenesis by CIAPIN1 siRNA Cancer Biol. Ther. 2009, 8 (11) 1058-63
46. de Duve, C. Lysosomes revisited Eur. J. Biochem. 1983, 137 (3) 391-7
47. Laurent-Matha, V.; Maruani-Herrmann, S.; Prebois, C.; Beaujouin, M.; Glondu, M.; Noel, A.; Alvarez-Gonzalez, M. L.; Blacher, S.; Coopman, P.; Baghdiguian, S.; Gilles, C.; Loncarek, J.; Freiss, G.; Vignon, F.; Liaudet-Coopman, E. Catalytically inactive human cathepsin D triggers fibroblast invasive growth J. Cell. Biol. 2005, 168 (3) 489-99
48. Koblinski, J. E.; Ahram, M.; Sloane, B. F. Unraveling the role of proteases in cancer Clin. Chim. Acta 2000, 291 (2) 113-35
49. Fehrenbacher, N.; Jaattela, M. Lysosomes as targets for cancer therapy Cancer Res. 2005, 65 (8) 2993-5
50. Talieri, M.; Papadopoulou, S.; Scorilas, A.; Xynopoulos, D.; Arnogianaki, N.; Plataniotis, G.; Yotis, J.; Agnanti, N. Cathepsin B and cathepsin D expression in the progression of colorectal adenoma to carcinoma Cancer Lett. 2004, 205 (1) 97-106
51. Foekens, J. A.; Look, M. P.; Bolt-de Vries, J.; Meijer-van Gelder, M. E.; van Putten, W. L.; Klijn, J. G. Cathepsin-D in primary breast cancer: Prognostic evaluation involving 2810 patients Br. J. Cancer 1999, 79 (2) 300-7
52. Fukuda, M. E.; Iwadate, Y.; Machida, T.; Hiwasa, T.; Nimura, Y.; Nagai, Y.; Takiguchi, M.; Tanzawa, H.; Yamaura, A.; Seki, N. Cathepsin D is a potential serum marker for poor prognosis in glioma patients Cancer Res. 2005, 65 (12) 5190-4
53. Baekelandt, M.; Holm, R.; Trope, C. G.; Nesland, J. M.; Kristensen, G. B. The significance of metastasis-related factors cathepsin-D and nm23 in advanced ovarian cancer Ann. Oncol. 1999, 10 (11) 1335-41
54. Berchem, G.; Glondu, M.; Gleizes, M.; Brouillet, J. P.; Vignon, F.; Garcia, M.; Liaudet-Coopman, E. Cathepsin-D affects multiple tumor progression steps in vivo: proliferation, angiogenesis and apoptosis Oncogene 2002, 21 (38) 5951-5
55. Cho, H. J.; Baek, K. E.; Nam, I. K.; Park, S. M.; Kim, I. K.; Park, S. H.; Im, M. J.; Ryu, K. J.; Yoo, J. M.; Hong, S. C.; Kim, J. W.; Lee, C. W.; Yoo, J. PLCγ is required for RhoGDI2-mediated cisplatin resistance in gastric cancer Biochem. Biophys. Res. Commun. 2011, 414 (3) 575-80