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Published in: Journal of Translational Medicine 1/2013

Open Access 01-12-2013 | Research

Phosphatase of regenerating liver-3 (PRL-3) is associated with metastasis and poor prognosis in gastric carcinoma

Authors: Xiaofang Xing, Shenyi Lian, Ying Hu, Ziyu Li, Lianhai Zhang, Xianzi Wen, Hong Du, Yongning Jia, Zhixue Zheng, Lin Meng, Chengchao Shou, Jiafu Ji

Published in: Journal of Translational Medicine | Issue 1/2013

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Abstract

Background

PRL-3 is a member of phosphatases of regenerating liver family, characterized by phosphatase active domain and C-terminal prenylation motif. Overexpression of PRL-3 has been implicated in multiple cancers. Here we examined the clinical significance of PRL-3 in gastric cancer together with its metastatic biological functions utilizing different structural mutants.

Methods

PRL-3 expression was analyzed immunohistochemically in 196 gastric cancer patients and 21 cases of liver metastasis. A series of wild type PRL-3 or its mutant plasmids were expressed in BGC823 cells to investigate the relationship between its catalytic activity, cellular localization and metastatic potential in vitro.

Results

Positive staining of PRL-3 was observed in 19.4% (38/196) gastric cancer tissues compared with 76.2% (16/21) in liver metastasis. Statistical analysis revealed that PRL-3 expression correlated with lymph node metastasis and vascular invasion (P < 0.05). Patients with high PRL-3 expression showed poorer 5-year overall survival (P = 0.011). Wild type PRL-3 expressing cells resulted in enhanced migration and invasion ability, which were greatly crippled in form of PRL-3(C104S) or PRL-3(ΔCAAX) mutants accompanied with its alteration in subcellular localization.

Conclusions

Metastasis associated protein PRL-3 may serve as a potential prognostic biomarker in human gastric cancer. Both the phosphatase catalytic activity and cellular localization are critical for its function.
Appendix
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Literature
1.
go back to reference Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: GLOBOCAN 2008, Cancer incidence and mortality worldwide. 2010, Lyon, France: International Agency for Research on Cancer Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM: GLOBOCAN 2008, Cancer incidence and mortality worldwide. 2010, Lyon, France: International Agency for Research on Cancer
2.
go back to reference Al-Aidaroos AQ, Zeng Q: PRL-3 phosphatase and cancer metastasis. J Cell Biochem. 2010, 111: 1087-1098. 10.1002/jcb.22913.CrossRefPubMed Al-Aidaroos AQ, Zeng Q: PRL-3 phosphatase and cancer metastasis. J Cell Biochem. 2010, 111: 1087-1098. 10.1002/jcb.22913.CrossRefPubMed
3.
go back to reference Saha S, Bardelli A, Buckhaults P, Velculescu VE, Rago C, St Croix B, Romans KE, Choti MA, Lengauer C, Kinzler KW, Vogelstein B: A phosphatase associated with metastasis of colorectal cancer. Science. 2001, 294: 1343-1346. 10.1126/science.1065817.CrossRefPubMed Saha S, Bardelli A, Buckhaults P, Velculescu VE, Rago C, St Croix B, Romans KE, Choti MA, Lengauer C, Kinzler KW, Vogelstein B: A phosphatase associated with metastasis of colorectal cancer. Science. 2001, 294: 1343-1346. 10.1126/science.1065817.CrossRefPubMed
4.
go back to reference Peng L, Xing X, Li W, Qu L, Meng L, Lian S, Jiang B, Wu J, Shou C: PRL-3 promotes the motility, invasion, and metastasis of LoVo colon cancer cells through PRL-3-integrin beta1-ERK1/2 and-MMP2 signaling. Mol Cancer. 2009, 8: 110-10.1186/1476-4598-8-110.PubMedCentralCrossRefPubMed Peng L, Xing X, Li W, Qu L, Meng L, Lian S, Jiang B, Wu J, Shou C: PRL-3 promotes the motility, invasion, and metastasis of LoVo colon cancer cells through PRL-3-integrin beta1-ERK1/2 and-MMP2 signaling. Mol Cancer. 2009, 8: 110-10.1186/1476-4598-8-110.PubMedCentralCrossRefPubMed
5.
go back to reference Kato H, Semba S, Miskad UA, Seo Y, Kasuga M, Yokozaki H: High expression of PRL-3 promotes cancer cell motility and liver metastasis in human colorectal cancer: a predictive molecular marker of metachronous liver and lung metastases. Clin Cancer Res. 2004, 10: 7318-7328. 10.1158/1078-0432.CCR-04-0485.CrossRefPubMed Kato H, Semba S, Miskad UA, Seo Y, Kasuga M, Yokozaki H: High expression of PRL-3 promotes cancer cell motility and liver metastasis in human colorectal cancer: a predictive molecular marker of metachronous liver and lung metastases. Clin Cancer Res. 2004, 10: 7318-7328. 10.1158/1078-0432.CCR-04-0485.CrossRefPubMed
6.
go back to reference Xing X, Peng L, Qu L, Ren T, Dong B, Su X, Shou C: Prognostic value of PRL-3 overexpression in early stages of colonic cancer. Histopathology. 2009, 54: 309-318. 10.1111/j.1365-2559.2009.03226.x.CrossRefPubMed Xing X, Peng L, Qu L, Ren T, Dong B, Su X, Shou C: Prognostic value of PRL-3 overexpression in early stages of colonic cancer. Histopathology. 2009, 54: 309-318. 10.1111/j.1365-2559.2009.03226.x.CrossRefPubMed
7.
go back to reference Radke I, Gotte M, Kersting C, Mattsson B, Kiesel L, Wulfing P: Expression and prognostic impact of the protein tyrosine phosphatases PRL-1, PRL-2, and PRL-3 in breast cancer. Br J Cancer. 2006, 95: 347-354. 10.1038/sj.bjc.6603261.PubMedCentralCrossRefPubMed Radke I, Gotte M, Kersting C, Mattsson B, Kiesel L, Wulfing P: Expression and prognostic impact of the protein tyrosine phosphatases PRL-1, PRL-2, and PRL-3 in breast cancer. Br J Cancer. 2006, 95: 347-354. 10.1038/sj.bjc.6603261.PubMedCentralCrossRefPubMed
8.
go back to reference Yamashita S, Masuda Y, Matsumoto K, Okumura Y, Matsuzaki H, Kurizaki T, Haga Y, Katafuchi S, Murayama T, Ikei S, Kawahara K: Down-regulation of the human PRL-3 gene is associated with the metastasis of primary non-small cell lung cancer. Ann Thorac Cardiovasc Surg. 2007, 13: 236-239.PubMed Yamashita S, Masuda Y, Matsumoto K, Okumura Y, Matsuzaki H, Kurizaki T, Haga Y, Katafuchi S, Murayama T, Ikei S, Kawahara K: Down-regulation of the human PRL-3 gene is associated with the metastasis of primary non-small cell lung cancer. Ann Thorac Cardiovasc Surg. 2007, 13: 236-239.PubMed
9.
go back to reference Polato F, Codegoni A, Fruscio R, Perego P, Mangioni C, Saha S, Bardelli A, Broggini M: PRL-3 phosphatase is implicated in ovarian cancer growth. Clin Cancer Res. 2005, 11: 6835-6839. 10.1158/1078-0432.CCR-04-2357.CrossRefPubMed Polato F, Codegoni A, Fruscio R, Perego P, Mangioni C, Saha S, Bardelli A, Broggini M: PRL-3 phosphatase is implicated in ovarian cancer growth. Clin Cancer Res. 2005, 11: 6835-6839. 10.1158/1078-0432.CCR-04-2357.CrossRefPubMed
10.
go back to reference Zhao WB, Li Y, Liu X, Zhang LY, Wang X: Evaluation of PRL-3 expression, and its correlation with angiogenesis and invasion in hepatocellular carcinoma. Int J Mol Med. 2008, 22: 187-192.PubMed Zhao WB, Li Y, Liu X, Zhang LY, Wang X: Evaluation of PRL-3 expression, and its correlation with angiogenesis and invasion in hepatocellular carcinoma. Int J Mol Med. 2008, 22: 187-192.PubMed
11.
go back to reference Miskad UA, Semba S, Kato H, Yokozaki H: Expression of PRL-3 phosphatase in human gastric carcinomas: close correlation with invasion and metastasis. Pathobiology. 2004, 71: 176-184. 10.1159/000078671.CrossRefPubMed Miskad UA, Semba S, Kato H, Yokozaki H: Expression of PRL-3 phosphatase in human gastric carcinomas: close correlation with invasion and metastasis. Pathobiology. 2004, 71: 176-184. 10.1159/000078671.CrossRefPubMed
12.
go back to reference Li ZR, Wang Z, Zhu BH, He YL, Peng JS, Cai SR, Ma JP, Zhan WH: Association of tyrosine PRL-3 phosphatase protein expression with peritoneal metastasis of gastric carcinoma and prognosis. Surg Today. 2007, 37: 646-651. 10.1007/s00595-006-3437-9.CrossRefPubMed Li ZR, Wang Z, Zhu BH, He YL, Peng JS, Cai SR, Ma JP, Zhan WH: Association of tyrosine PRL-3 phosphatase protein expression with peritoneal metastasis of gastric carcinoma and prognosis. Surg Today. 2007, 37: 646-651. 10.1007/s00595-006-3437-9.CrossRefPubMed
13.
go back to reference Wang Z, He YL, Cai SR, Zhan WH, Li ZR, Zhu BH, Chen CQ, Ma JP, Chen ZX, Li W, Zhang LJ: Expression and prognostic impact of PRL-3 in lymph node metastasis of gastric cancer: its molecular mechanism was investigated using artificial microRNA interference. Int J Cancer. 2008, 123: 1439-1447. 10.1002/ijc.23643.CrossRefPubMed Wang Z, He YL, Cai SR, Zhan WH, Li ZR, Zhu BH, Chen CQ, Ma JP, Chen ZX, Li W, Zhang LJ: Expression and prognostic impact of PRL-3 in lymph node metastasis of gastric cancer: its molecular mechanism was investigated using artificial microRNA interference. Int J Cancer. 2008, 123: 1439-1447. 10.1002/ijc.23643.CrossRefPubMed
14.
go back to reference Pryczynicz A, Guzinska-Ustymowicz K, Chang XJ, Kisluk J, Kemona A: PTP4A3 (PRL-3) expression correlate with lymphatic metastases in gastric cancer. Folia Histochem Cytobiol. 2010, 48: 632-636.PubMed Pryczynicz A, Guzinska-Ustymowicz K, Chang XJ, Kisluk J, Kemona A: PTP4A3 (PRL-3) expression correlate with lymphatic metastases in gastric cancer. Folia Histochem Cytobiol. 2010, 48: 632-636.PubMed
15.
go back to reference Guzinska-Ustymowicz K, Pryczynicz A: PRL-3, an emerging marker of carcinogenesis, is strongly associated with poor prognosis. Anticancer Agents Med Chem. 2011, 11: 99-108. 10.2174/187152011794941145.CrossRefPubMed Guzinska-Ustymowicz K, Pryczynicz A: PRL-3, an emerging marker of carcinogenesis, is strongly associated with poor prognosis. Anticancer Agents Med Chem. 2011, 11: 99-108. 10.2174/187152011794941145.CrossRefPubMed
16.
go back to reference Kozlov G, Cheng J, Ziomek E, Banville D, Gehring K, Ekiel I: Structural insights into molecular function of the metastasis-associated phosphatase PRL-3. J Biol Chem. 2004, 279: 11882-11889. 10.1074/jbc.M312905200.CrossRefPubMed Kozlov G, Cheng J, Ziomek E, Banville D, Gehring K, Ekiel I: Structural insights into molecular function of the metastasis-associated phosphatase PRL-3. J Biol Chem. 2004, 279: 11882-11889. 10.1074/jbc.M312905200.CrossRefPubMed
17.
go back to reference Peng L, Jin G, Wang L, Guo J, Meng L, Shou C: Identification of integrin alpha1 as an interacting protein of protein tyrosine phosphatase PRL-3. Biochem Biophys Res Commun. 2006, 342: 179-183. 10.1016/j.bbrc.2006.01.102.CrossRefPubMed Peng L, Jin G, Wang L, Guo J, Meng L, Shou C: Identification of integrin alpha1 as an interacting protein of protein tyrosine phosphatase PRL-3. Biochem Biophys Res Commun. 2006, 342: 179-183. 10.1016/j.bbrc.2006.01.102.CrossRefPubMed
18.
go back to reference Forte E, Orsatti L, Talamo F, Barbato G, De Francesco R, Tomei L: Ezrin is a specific and direct target of protein tyrosine phosphatase PRL-3. Biochim Biophys Acta. 2008, 1783: 334-344. 10.1016/j.bbamcr.2007.11.004.CrossRefPubMed Forte E, Orsatti L, Talamo F, Barbato G, De Francesco R, Tomei L: Ezrin is a specific and direct target of protein tyrosine phosphatase PRL-3. Biochim Biophys Acta. 2008, 1783: 334-344. 10.1016/j.bbamcr.2007.11.004.CrossRefPubMed
19.
go back to reference Wang H, Quah SY, Dong JM, Manser E, Tang JP, Zeng Q: PRL-3 down-regulates PTEN expression and signals through PI3K to promote epithelial-mesenchymal transition. Cancer Res. 2007, 67: 2922-2926. 10.1158/0008-5472.CAN-06-3598.CrossRefPubMed Wang H, Quah SY, Dong JM, Manser E, Tang JP, Zeng Q: PRL-3 down-regulates PTEN expression and signals through PI3K to promote epithelial-mesenchymal transition. Cancer Res. 2007, 67: 2922-2926. 10.1158/0008-5472.CAN-06-3598.CrossRefPubMed
20.
go back to reference Liu Y, Zhou J, Chen J, Gao W, Le Y, Ding Y, Li J: PRL-3 promotes epithelial mesenchymal transition by regulating cadherin directly. Cancer Biol Ther. 2009, 8: 1352-1359. 10.4161/cbt.8.14.8695.CrossRefPubMed Liu Y, Zhou J, Chen J, Gao W, Le Y, Ding Y, Li J: PRL-3 promotes epithelial mesenchymal transition by regulating cadherin directly. Cancer Biol Ther. 2009, 8: 1352-1359. 10.4161/cbt.8.14.8695.CrossRefPubMed
21.
go back to reference Guo K, Li J, Wang H, Osato M, Tang JP, Quah SY, Gan BQ, Zeng Q: PRL-3 initiates tumor angiogenesis by recruiting endothelial cells in vitro and in vivo. Cancer Res. 2006, 66: 9625-9635. 10.1158/0008-5472.CAN-06-0726.CrossRefPubMed Guo K, Li J, Wang H, Osato M, Tang JP, Quah SY, Gan BQ, Zeng Q: PRL-3 initiates tumor angiogenesis by recruiting endothelial cells in vitro and in vivo. Cancer Res. 2006, 66: 9625-9635. 10.1158/0008-5472.CAN-06-0726.CrossRefPubMed
22.
go back to reference Al-Aidaroos AQ, Yuen HF, Guo K, Zhang SD, Chung TH, Chng WJ, Zeng Q: Metastasis-associated PRL-3 induces EGFR activation and addiction in cancer cells. J Clin Invest. 2013, 123: 3459-3471. 10.1172/JCI66824.PubMedCentralCrossRefPubMed Al-Aidaroos AQ, Yuen HF, Guo K, Zhang SD, Chung TH, Chng WJ, Zeng Q: Metastasis-associated PRL-3 induces EGFR activation and addiction in cancer cells. J Clin Invest. 2013, 123: 3459-3471. 10.1172/JCI66824.PubMedCentralCrossRefPubMed
23.
go back to reference Kim KA, Song JS, Jee J, Sheen MR, Lee C, Lee TG, Ro S, Cho JM, Lee W, Yamazaki T: Structure of human PRL-3, the phosphatase associated with cancer metastasis. FEBS Lett. 2004, 565: 181-187. 10.1016/j.febslet.2004.03.062.CrossRefPubMed Kim KA, Song JS, Jee J, Sheen MR, Lee C, Lee TG, Ro S, Cho JM, Lee W, Yamazaki T: Structure of human PRL-3, the phosphatase associated with cancer metastasis. FEBS Lett. 2004, 565: 181-187. 10.1016/j.febslet.2004.03.062.CrossRefPubMed
24.
go back to reference Zeng Q, Dong JM, Guo K, Li J, Tan HX, Koh V, Pallen CJ, Manser E, Hong W: PRL-3 and PRL-1 promote cell migration, invasion, and metastasis. Cancer Res. 2003, 63: 2716-2722.PubMed Zeng Q, Dong JM, Guo K, Li J, Tan HX, Koh V, Pallen CJ, Manser E, Hong W: PRL-3 and PRL-1 promote cell migration, invasion, and metastasis. Cancer Res. 2003, 63: 2716-2722.PubMed
25.
go back to reference Peng L, Li Y, Meng L, Shou C: Preparation and characterization of monoclonal antibody against protein tyrosine phosphatase PRL-3. Hybrid Hybridomics. 2004, 23: 23-27. 10.1089/153685904322771999.CrossRefPubMed Peng L, Li Y, Meng L, Shou C: Preparation and characterization of monoclonal antibody against protein tyrosine phosphatase PRL-3. Hybrid Hybridomics. 2004, 23: 23-27. 10.1089/153685904322771999.CrossRefPubMed
26.
go back to reference Mayinuer A, Yasen M, Mogushi K, Obulhasim G, Xieraili M, Aihara A, Tanaka S, Mizushima H, Tanaka H, Arii S: Upregulation of protein tyrosine phosphatase type IVA member 3 (PTP4A3/PRL-3) is associated with tumor differentiation and a poor prognosis in human hepatocellular carcinoma. Ann Surg Oncol. 2013, 20: 305-317. 10.1245/s10434-012-2395-2.PubMedCentralCrossRefPubMed Mayinuer A, Yasen M, Mogushi K, Obulhasim G, Xieraili M, Aihara A, Tanaka S, Mizushima H, Tanaka H, Arii S: Upregulation of protein tyrosine phosphatase type IVA member 3 (PTP4A3/PRL-3) is associated with tumor differentiation and a poor prognosis in human hepatocellular carcinoma. Ann Surg Oncol. 2013, 20: 305-317. 10.1245/s10434-012-2395-2.PubMedCentralCrossRefPubMed
27.
go back to reference De Palma M, Hanahan D: The biology of personalized cancer medicine: facing individual complexities underlying hallmark capabilities. Mol Oncol. 2012, 6: 111-127. 10.1016/j.molonc.2012.01.011.CrossRefPubMed De Palma M, Hanahan D: The biology of personalized cancer medicine: facing individual complexities underlying hallmark capabilities. Mol Oncol. 2012, 6: 111-127. 10.1016/j.molonc.2012.01.011.CrossRefPubMed
28.
go back to reference Peng LR, Shou CC: Phosphatase of regenerating liver-3 (PRL-3) and tumor metastasis. Zhonghua Zhong Liu Za Zhi. 2007, 29: 1-3.PubMed Peng LR, Shou CC: Phosphatase of regenerating liver-3 (PRL-3) and tumor metastasis. Zhonghua Zhong Liu Za Zhi. 2007, 29: 1-3.PubMed
29.
go back to reference Guo K, Li J, Tang JP, Koh V, Gan BQ, Zeng Q: Catalytic domain of PRL-3 plays an essential role in tumor metastasis: formation of PRL-3 tumors inside the blood vessels. Cancer Biol Ther. 2004, 3: 945-951. 10.4161/cbt.3.10.1111.CrossRefPubMed Guo K, Li J, Tang JP, Koh V, Gan BQ, Zeng Q: Catalytic domain of PRL-3 plays an essential role in tumor metastasis: formation of PRL-3 tumors inside the blood vessels. Cancer Biol Ther. 2004, 3: 945-951. 10.4161/cbt.3.10.1111.CrossRefPubMed
30.
go back to reference Cates CA, Michael RL, Stayrook KR, Harvey KA, Burke YD, Randall SK, Crowell PL, Crowell DN: Prenylation of oncogenic human PTP(CAAX) protein tyrosine phosphatases. Cancer Lett. 1996, 110: 49-55. 10.1016/S0304-3835(96)04459-X.CrossRefPubMed Cates CA, Michael RL, Stayrook KR, Harvey KA, Burke YD, Randall SK, Crowell PL, Crowell DN: Prenylation of oncogenic human PTP(CAAX) protein tyrosine phosphatases. Cancer Lett. 1996, 110: 49-55. 10.1016/S0304-3835(96)04459-X.CrossRefPubMed
31.
go back to reference Zeng Q, Si X, Horstmann H, Xu Y, Hong W, Pallen CJ: Prenylation-dependent association of protein-tyrosine phosphatases PRL-1, -2, and −3 with the plasma membrane and the early endosome. J Biol Chem. 2000, 275: 21444-21452. 10.1074/jbc.M000453200.CrossRefPubMed Zeng Q, Si X, Horstmann H, Xu Y, Hong W, Pallen CJ: Prenylation-dependent association of protein-tyrosine phosphatases PRL-1, -2, and −3 with the plasma membrane and the early endosome. J Biol Chem. 2000, 275: 21444-21452. 10.1074/jbc.M000453200.CrossRefPubMed
32.
go back to reference Bessette DC, Wong PC, Pallen CJ: PRL-3: a metastasis-associated phosphatase in search of a function. Cells Tissues Organs. 2007, 185: 232-236. 10.1159/000101324.CrossRefPubMed Bessette DC, Wong PC, Pallen CJ: PRL-3: a metastasis-associated phosphatase in search of a function. Cells Tissues Organs. 2007, 185: 232-236. 10.1159/000101324.CrossRefPubMed
33.
go back to reference Zeng Q, Hong W, Tan YH: Mouse PRL-2 and PRL-3, two potentially prenylated protein tyrosine phosphatases homologous to PRL-1. Biochem Biophys Res Commun. 1998, 244: 421-427. 10.1006/bbrc.1998.8291.CrossRefPubMed Zeng Q, Hong W, Tan YH: Mouse PRL-2 and PRL-3, two potentially prenylated protein tyrosine phosphatases homologous to PRL-1. Biochem Biophys Res Commun. 1998, 244: 421-427. 10.1006/bbrc.1998.8291.CrossRefPubMed
34.
go back to reference Dumaual CM, Sandusky GE, Soo HW, Werner SR, Crowell PL, Randall SK: Tissue-specific alterations of PRL-1 and PRL-2 expression in cancer. Am J Transl Res. 2012, 4: 83-101.PubMedCentralPubMed Dumaual CM, Sandusky GE, Soo HW, Werner SR, Crowell PL, Randall SK: Tissue-specific alterations of PRL-1 and PRL-2 expression in cancer. Am J Transl Res. 2012, 4: 83-101.PubMedCentralPubMed
35.
go back to reference Achiwa H, Lazo JS: PRL-1 tyrosine phosphatase regulates c-Src levels, adherence, and invasion in human lung cancer cells. Cancer Res. 2007, 67: 643-650. 10.1158/0008-5472.CAN-06-2436.CrossRefPubMed Achiwa H, Lazo JS: PRL-1 tyrosine phosphatase regulates c-Src levels, adherence, and invasion in human lung cancer cells. Cancer Res. 2007, 67: 643-650. 10.1158/0008-5472.CAN-06-2436.CrossRefPubMed
36.
go back to reference Winter-Vann AM, Casey PJ: Post-prenylation-processing enzymes as new targets in oncogenesis. Nat Rev Cancer. 2005, 5: 405-412. 10.1038/nrc1612.CrossRefPubMed Winter-Vann AM, Casey PJ: Post-prenylation-processing enzymes as new targets in oncogenesis. Nat Rev Cancer. 2005, 5: 405-412. 10.1038/nrc1612.CrossRefPubMed
37.
go back to reference Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL, Cox AD, Philips MR: Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol. 2002, 4: 343-350.PubMed Chiu VK, Bivona T, Hach A, Sajous JB, Silletti J, Wiener H, Johnson RL, Cox AD, Philips MR: Ras signalling on the endoplasmic reticulum and the Golgi. Nat Cell Biol. 2002, 4: 343-350.PubMed
38.
go back to reference Di Paolo A, Danesi R, Caputo S, Macchia M, Lastella M, Boggi U, Mosca F, Marchetti A, Del Tacca M: Inhibition of protein farnesylation enhances the chemotherapeutic efficacy of the novel geranylgeranyltransferase inhibitor BAL9611 in human colon cancer cells. Br J Cancer. 2001, 84: 1535-1543. 10.1054/bjoc.2001.1820.CrossRefPubMed Di Paolo A, Danesi R, Caputo S, Macchia M, Lastella M, Boggi U, Mosca F, Marchetti A, Del Tacca M: Inhibition of protein farnesylation enhances the chemotherapeutic efficacy of the novel geranylgeranyltransferase inhibitor BAL9611 in human colon cancer cells. Br J Cancer. 2001, 84: 1535-1543. 10.1054/bjoc.2001.1820.CrossRefPubMed
39.
go back to reference Dowlati A, Kluge A, Nethery D, Halmos B, Kern JA: SCH66336, inhibitor of protein farnesylation, blocks signal transducer and activators of transcription 3 signaling in lung cancer and interacts with a small molecule inhibitor of epidermal growth factor receptor/human epidermal growth factor receptor 2. Anticancer Drugs. 2008, 19: 9-16. 10.1097/CAD.0b013e3282f1a908.CrossRefPubMed Dowlati A, Kluge A, Nethery D, Halmos B, Kern JA: SCH66336, inhibitor of protein farnesylation, blocks signal transducer and activators of transcription 3 signaling in lung cancer and interacts with a small molecule inhibitor of epidermal growth factor receptor/human epidermal growth factor receptor 2. Anticancer Drugs. 2008, 19: 9-16. 10.1097/CAD.0b013e3282f1a908.CrossRefPubMed
Metadata
Title
Phosphatase of regenerating liver-3 (PRL-3) is associated with metastasis and poor prognosis in gastric carcinoma
Authors
Xiaofang Xing
Shenyi Lian
Ying Hu
Ziyu Li
Lianhai Zhang
Xianzi Wen
Hong Du
Yongning Jia
Zhixue Zheng
Lin Meng
Chengchao Shou
Jiafu Ji
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2013
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/1479-5876-11-309

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