Drosophila PRL-1 Is a Growth Inhibitor That Counteracts the Function of the Src Oncogene

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Pagarigan, Krystle T ^a   Bunn, Bryce W ^a   Goodchild, Jake ^a   Rahe, Travis K ^a,b   Weis, Julie F ^a   Saucedo, Leslie J ^a  

^a UNIVERSITY OF PUGET SOUND   (United States)

^b USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; PHOSPHATASE OF REGENERATING LIVER 1; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG;

ARTICLE; CANCER INHIBITION; CELL MEMBRANE; CONTROLLED STUDY; DROSOPHILA; GENE ACTIVITY; GENE FUNCTION; GENETIC REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOGENE SRC; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; TRANSGENICS;

ANIMALS; CELL MEMBRANE; CYTOPLASM; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, SRC; HUMANS; PROTEIN TRANSPORT; PROTEIN TYROSINE PHOSPHATASES;

EID: 84875990614     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061084     Document Type: Article

References (70)

1. Stephens BJ, Han H, Gokhale V, Von Hoff DD, (2005) PRL phosphatases as potential molecular targets in cancer. Mol Cancer Ther 4: 1653-1661 doi:10.1158/1535-7163.MCT-05-0248.
2. Bessette DC, Qiu D, Pallen CJ, (2008) PRL PTPs: mediators and markers of cancer progression. Cancer Metastasis Rev 27: 231-252 doi:10.1007/s10555-008-9121-3.
3. Al-Aidaroos AQO, Zeng Q, (2010) PRL-3 phosphatase and cancer metastasis. J Cell Biochem 111: 1087-1098 doi:10.1002/jcb.22913.
4. Li Z, Zhan W, Wang Z, Zhu B, He Y, et al. (2006) Inhibition of PRL-3 gene expression in gastric cancer cell line SGC7901 via microRNA suppressed reduces peritoneal metastasis. Biochem Biophys Res Commun 348: 229-237 doi:10.1016/j.bbrc.2006.07.043.
5. Guo K, Tang JP, Tan CPB, Wang H, Zeng Q, (2008) Monoclonal antibodies target intracellular PRL phosphatases to inhibit cancer metastases in mice. Cancer Biol Ther 7: 750-757.
6. Mohn KL, Melby AE, Tewari DS, Laz TM, Taub R, (1991) The gene encoding rat insulinlike growth factor-binding protein 1 is rapidly and highly induced in regenerating liver. Mol Cell Biol 11: 1393-1401.
7. Diamond RH, Cressman DE, Laz TM, Abrams CS, Taub R, (1994) PRL-1, a unique nuclear protein tyrosine phosphatase, affects cell growth. Mol Cell Biol 14: 3752-3762.
8. Zeng Q, Hong W, Tan YH, (1998) Mouse PRL-2 and PRL-3, two potentially prenylated protein tyrosine phosphatases homologous to PRL-1. Biochem Biophys Res Commun 244: 421-427 doi:10.1006/bbrc.1998.8291.
9. Matter WF, Estridge T, Zhang C, Belagaje R, Stancato L, et al. (2001) Role of PRL-3, a human muscle-specific tyrosine phosphatase, in angiotensin-II signaling. Biochem Biophys Res Commun 283: 1061-1068 doi:10.1006/bbrc.2001.4881.
10. Werner SR, Lee PA, DeCamp MW, Crowell DN, Randall SK, et al. (2003) Enhanced cell cycle progression and down regulation of p21(Cip1/Waf1) by PRL tyrosine phosphatases. Cancer Lett 202: 201-211.
11. Liang F, Liang J, Wang W-Q, Sun J-P, Udho E, et al. (2007) PRL3 promotes cell invasion and proliferation by down-regulation of Csk leading to Src activation. J Biol Chem 282: 5413-5419 doi:10.1074/jbc.M608940200.
12. Zeng Q, Dong J-M, Guo K, Li J, Tan H-X, et al. (2003) PRL-3 and PRL-1 promote cell migration, invasion, and metastasis. Cancer Res 63: 2716-2722.
13. Wu X, Zeng H, Zhang X, Zhao Y, Sha H, et al. (2004) Phosphatase of regenerating liver-3 promotes motility and metastasis of mouse melanoma cells. Am J Pathol 164: 2039-2054 doi:10.1016/S0002-9440(10)63763-7.
14. Wang Y, Lazo JS, (2012) Metastasis-associated phosphatase PRL-2 regulates tumor cell migration and invasion. Oncogene 31: 818-827 doi:10.1038/onc.2011.281.
15. Guo K, Li J, Tang JP, Koh V, Gan BQ, et al. (2004) Catalytic domain of PRL-3 plays an essential role in tumor metastasis: formation of PRL-3 tumors inside the blood vessels. Cancer Biol Ther 3: 945-951.
16. Saha S, Bardelli A, Buckhaults P, Velculescu VE, Rago C, et al. (2001) A phosphatase associated with metastasis of colorectal cancer. Science 294: 1343-1346 doi:10.1126/science.1065817.
17. Bardelli A, Saha S, Sager JA, Romans KE, Xin B, et al. (2003) PRL-3 expression in metastatic cancers. Clin Cancer Res 9: 5607-5615.
18. Kato H, Semba S, Miskad UA, Seo Y, Kasuga M, et al. (2004) 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 10: 7318-7328 doi:10.1158/1078-0432.CCR-04-0485.
19. Peng L, Ning J, Meng L, Shou C, (2004) The association of the expression level of protein tyrosine phosphatase PRL-3 protein with liver metastasis and prognosis of patients with colorectal cancer. J Cancer Res Clin Oncol 130: 521-526 doi:10.1007/s00432-004-0563-x.
20. Wang Y, Li Z-F, He J, Li Y-L, Zhu G-B, et al. (2007) Expression of the human phosphatases of regenerating liver (PRLs) in colonic adenocarcinoma and its correlation with lymph node metastasis. Int J Colorectal Dis 22: 1179-1184 doi:10.1007/s00384-007-0303-1.
21. Xing X, Peng L, Qu L, Ren T, Dong B, et al. (2009) Prognostic value of PRL-3 overexpression in early stages of colonic cancer. Histopathology 54: 309-318 doi:10.1111/j.1365-2559.2009.03226.x.
22. Zhao W-B, Li Y, Liu X, Zhang L-Y, Wang X, (2008) Evaluation of PRL-3 expression, and its correlation with angiogenesis and invasion in hepatocellular carcinoma. Int J Mol Med 22: 187-192.
23. Xu Y, Zhu M, Zhang S, Liu H, Li T, et al. (2010) Expression and prognostic value of PRL-3 in human intrahepatic cholangiocarcinoma. Pathol Oncol Res 16: 169-175 doi:10.1007/s12253-009-9200-y.
24. Kong L, Li Q, Wang L, Liu Z, Sun T, (2007) The value and correlation between PRL-3 expression and matrix metalloproteinase activity and expression in human gliomas. Neuropathology 27: 516-521 doi:10.1111/j.1440-1789.2007.00818.x.
25. Miskad UA, Semba S, Kato H, Yokozaki H, (2004) Expression of PRL-3 phosphatase in human gastric carcinomas: close correlation with invasion and metastasis. Pathobiology 71: 176-184 doi:10.1159/000078671.
26. Miskad UA, Semba S, Kato H, Matsukawa Y, Kodama Y, et al. (2007) High PRL-3 expression in human gastric cancer is a marker of metastasis and grades of malignancies: an in situ hybridization study. Virchows Arch 450: 303-310 doi:10.1007/s00428-006-0361-8.
27. Ooki A, Yamashita K, Kikuchi S, Sakuramoto S, Katada N, et al. (2009) Phosphatase of regenerating liver-3 as a prognostic biomarker in histologically node-negative gastric cancer. Oncol Rep 21: 1467-1475.
28. Dai N, Lu A-P, Shou C-C, Li J-Y, (2009) Expression of phosphatase regenerating liver 3 is an independent prognostic indicator for gastric cancer. World J Gastroenterol 15: 1499-1505.
29. Radke I, Götte M, Kersting C, Mattsson B, Kiesel L, et al. (2006) Expression and prognostic impact of the protein tyrosine phosphatases PRL-1, PRL-2, and PRL-3 in breast cancer. Br J Cancer 95: 347-354 doi:10.1038/sj.bjc.6603261.
30. Wang L, Peng L, Dong B, Kong L, Meng L, et al. (2006) Overexpression of phosphatase of regenerating liver-3 in breast cancer: association with a poor clinical outcome. Ann Oncol 17: 1517-1522 doi:10.1093/annonc/mdl159.
31. Hao R-T, Zhang X-H, Pan Y-F, Liu H-G, Xiang Y-Q, et al. (2010) Prognostic and metastatic value of phosphatase of regenerating liver-3 in invasive breast cancer. J Cancer Res Clin Oncol 136: 1349-1357 doi:10.1007/s00432-010-0786-y.
32. Polato F, Codegoni A, Fruscio R, Perego P, Mangioni C, et al. (2005) PRL-3 phosphatase is implicated in ovarian cancer growth. Clin Cancer Res 11: 6835-6839 doi:10.1158/1078-0432.CCR-04-2357.
33. Ren T, Jiang B, Xing X, Dong B, Peng L, et al. (2009) Prognostic significance of phosphatase of regenerating liver-3 expression in ovarian cancer. Pathol Oncol Res 15: 555-560 doi:10.1007/s12253-009-9153-1.
34. Ma Y, Li B, (2011) Expression of phosphatase of regenerating liver-3 in squamous cell carcinoma of the cervix. Med Oncol 28: 775-780 doi:10.1007/s12032-010-9514-3.
35. Wallin AR, Svanvik J, Adell G, Sun X-F, (2006) Expression of PRL proteins at invasive margin of rectal cancers in relation to preoperative radiotherapy. Int J Radiat Oncol Biol Phys 65: 452-458 doi:10.1016/j.ijrobp.2005.12.043.
36. Zhou J, Wang S, Lu J, Li J, Ding Y, (2009) Over-expression of phosphatase of regenerating liver-3 correlates with tumor progression and poor prognosis in nasopharyngeal carcinoma. Int J Cancer 124: 1879-1886 doi:10.1002/ijc.24096.
37. Liu Y-Q, Li H-X, Lou X, Lei J-Y, (2008) Expression of phosphatase of regenerating liver 1 and 3 mRNA in esophageal squamous cell carcinoma. Arch Pathol Lab Med 132: 1307-1312 doi:10.1043/1543-2165(2008)132[1307:EOPORL]2.0.CO;2.
38. Ooki A, Yamashita K, Kikuchi S, Sakuramoto S, Katada N, et al. (2010) Phosphatase of regenerating liver-3 as a convergent therapeutic target for lymph node metastasis in esophageal squamous cell carcinoma. Int J Cancer 127: 543-554 doi:10.1002/ijc.25082.
39. Hassan NMM, Hamada J, Kameyama T, Tada M, Nakagawa K, et al. (2011) Increased expression of the PRL-3 gene in human oral squamous cell carcinoma and dysplasia tissues. Asian Pac J Cancer Prev 12: 947-951.
40. Reich R, Hadar S, Davidson B, (2011) Expression and clinical role of protein of regenerating liver (PRL) phosphatases in ovarian carcinoma. Int J Mol Sci 12: 1133-1145 doi:10.3390/ijms12021133.
41. Yamashita S, Masuda Y, Matsumoto K, Okumura Y, Matsuzaki H, et al. (2007) Down-regulation of the human PRL-3 gene is associated with the metastasis of primary non-small cell lung cancer. Ann Thorac Cardiovasc Surg 13: 236-239.
42. Hatate K, Yamashita K, Hirai K, Kumamoto H, Sato T, et al. (2008) Liver metastasis of colorectal cancer by protein-tyrosine phosphatase type 4A, 3 (PRL-3) is mediated through lymph node metastasis and elevated serum tumor markers such as CEA and CA19-9. Oncol Rep 20: 737-743.
43. Basak S, Jacobs SBR, Krieg AJ, Pathak N, Zeng Q, et al. (2008) The metastasis-associated gene Prl-3 is a p53 target involved in cell-cycle regulation. Mol Cell 30: 303-314 doi:10.1016/j.molcel.2008.04.002.
44. Diamond RH, Peters C, Jung SP, Greenbaum LE, Haber BA, et al. (1996) Expression of PRL-1 nuclear PTPase is associated with proliferation in liver but with differentiation in intestine. Am J Physiol 271: G121-129.
45. Kong W, Swain GP, Li S, Diamond RH, (2000) PRL-1 PTPase expression is developmentally regulated with tissue-specific patterns in epithelial tissues. Am J Physiol Gastrointest Liver Physiol 279: G613-621.
46. Forte E, Orsatti L, Talamo F, Barbato G, De Francesco R, et al. (2008) Ezrin is a specific and direct target of protein tyrosine phosphatase PRL-3. Biochim Biophys Acta 1783: 334-344 doi:10.1016/j.bbamcr.2007.11.004.
47. Peters CS, Liang X, Li S, Kannan S, Peng Y, et al. (2001) ATF-7, a novel bZIP protein, interacts with the PRL-1 protein-tyrosine phosphatase. J Biol Chem 276: 13718-13726 doi:10.1074/jbc.M011562200.
48. Fiordalisi JJ, Keller PJ, Cox AD, (2006) PRL tyrosine phosphatases regulate rho family GTPases to promote invasion and motility. Cancer Res 66: 3153-3161 doi:10.1158/0008-5472.CAN-05-3116.
49. Zeng Q, Si X, Horstmann H, Xu Y, Hong W, et al. (2000) Prenylation-dependent association of protein-tyrosine phosphatases PRL-1,-2, and-3 with the plasma membrane and the early endosome. J Biol Chem 275: 21444-21452 doi:10.1074/jbc.M000453200.
50. Sun J-P, Luo Y, Yu X, Wang W-Q, Zhou B, et al. (2007) Phosphatase activity, trimerization, and the C-terminal polybasic region are all required for PRL1-mediated cell growth and migration. J Biol Chem 282: 29043-29051 doi:10.1074/jbc.M703537200.
51. Song R, Qian F, Li Y-P, Sheng X, Cao S-X, et al. (2009) Phosphatase of regenerating liver-3 localizes to cyto-membrane and is required for B16F1 melanoma cell metastasis in vitro and in vivo. PLoS ONE 4: e4450 doi:10.1371/journal.pone.0004450.
52. Achiwa H, Lazo JS, (2007) PRL-1 tyrosine phosphatase regulates c-Src levels, adherence, and invasion in human lung cancer cells. Cancer Res 67: 643-650 doi:10.1158/0008-5472.CAN-06-2436.
53. Luo Y, Liang F, Zhang Z-Y, (2009) PRL1 promotes cell migration and invasion by increasing MMP2 and MMP9 expression through Src and ERK1/2 pathways. Biochemistry 48: 1838-1846 doi:10.1021/bi8020789.
54. Liang F, Luo Y, Dong Y, Walls CD, Liang J, et al. (2008) Translational control of C-terminal Src kinase (Csk) expression by PRL3 phosphatase. J Biol Chem 283: 10339-10346 doi:10.1074/jbc.M708285200.
55. Wang H, Quah SY, Dong JM, Manser E, Tang JP, et al. (2007) PRL-3 down-regulates PTEN expression and signals through PI3K to promote epithelial-mesenchymal transition. Cancer Res 67: 2922-2926 doi:10.1158/0008-5472.CAN-06-3598.
56. Parcellier A, Tintignac LA, Zhuravleva E, Hemmings BA, (2008) PKB and the mitochondria: AKTing on apoptosis. Cell Signal 20: 21-30 doi:10.1016/j.cellsig.2007.07.010.
57. Stambolic V, Woodgett JR, (2006) Functional distinctions of protein kinase B/Akt isoforms defined by their influence on cell migration. Trends Cell Biol 16: 461-466 doi:10.1016/j.tcb.2006.07.001.
58. Xu T, Rubin GM, (1993) Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237.
59. Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA, (1998) Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183-1193.
60. Jeong DG, Kim SJ, Kim JH, Son JH, Park MR, et al. (2005) Trimeric structure of PRL-1 phosphatase reveals an active enzyme conformation and regulation mechanisms. J Mol Biol 345: 401-413 doi:10.1016/j.jmb.2004.10.061.
61. Vidal M, Warner S, Read R, Cagan RL, (2007) Differing Src signaling levels have distinct outcomes in Drosophila. Cancer Res 67: 10278-10285 doi:10.1158/0008-5472.CAN-07-1376.
62. Kozlov G, Cheng J, Ziomek E, Banville D, Gehring K, et al. (2004) Structural Insights into Molecular Function of the Metastasis-associated Phosphatase PRL-3. J Biol Chem 279: 11882-11889 doi:10.1074/jbc.M312905200.
63. Sun J-P, Wang W-Q, Yang H, Liu S, Liang F, et al. (2005) Structure and biochemical properties of PRL-1, a phosphatase implicated in cell growth, differentiation, and tumor invasion. Biochemistry 44: 12009-12021 doi:10.1021/bi0509191.
64. Yu L, Kelly U, Ebright JN, Malek G, Saloupis P, et al. (2007) Oxidative stress-induced expression and modulation of Phosphatase of Regenerating Liver-1 (PRL-1) in mammalian retina. Biochim Biophys Acta 1773: 1473-1482 doi:10.1016/j.bbamcr.2007.06.005.
65. Skinner AL, Vartia AA, Williams TD, Laurence JS, (2009) Enzyme activity of phosphatase of regenerating liver is controlled by the redox environment and its C-terminal residues. Biochemistry 48: 4262-4272 doi:10.1021/bi900241k.
66. Min S-H, Kim DM, Heo Y-S, Kim Y-I, Kim HM, et al. (2009) New p53 target, phosphatase of regenerating liver 1 (PRL-1) downregulates p53. Oncogene 28: 545-554 doi:10.1038/onc.2008.409.
67. Min S-H, Kim DM, Heo Y-S, Kim HM, Kim I-C, et al. (2010) Downregulation of p53 by phosphatase of regenerating liver 3 is mediated by MDM2 and PIRH2. Life Sci 86: 66-72 doi:10.1016/j.lfs.2009.11.010.
68. Rudrapatna VA, Cagan RL, Das TK, (2012) Drosophila cancer models. Dev Dyn 241: 107-118 doi:10.1002/dvdy.22771.
69. Sanson B, White P, Vincent JP, (1996) Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383: 627-630 doi:10.1038/383627a0.
70. O'Reilly AM, Ballew AC, Miyazawa B, Stocker H, Hafen E, et al. (2006) Csk differentially regulates Src64 during distinct morphological events in Drosophila germ cells. Development 133: 2627-2638 doi:10.1242/dev.02423.