SLIT2 inhibits cell migration in colorectal cancer through the AKT-GSK3β signaling pathway

International Journal of Colorectal Disease

Volumn 28, Issue 7, 2013, Pages 933-940

  Chen, Wei Feng ^a   Gao, Wei Dong ^a   Li, Quan Lin ^a   Zhou, Ping Hong ^a   Xu, Mei Dong ^a   Yao, Li Qing ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

AKT GSK3 signaling pathway; Colorectal cancer; Epithelial to mesenchymal transition; Metastasis; SLIT2

Indexed keywords

BETA CATENIN; CELL PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; PROTEIN KINASE B INHIBITOR; PROTEIN ROBO1; SHORT HAIRPIN RNA; SLIT2 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CANCER CELL CULTURE; CELL MIGRATION; CELL MOTILITY; COLON CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; METASTASIS; MOLECULAR BIOLOGY; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SLIT2 GENE; UPREGULATION; WESTERN BLOTTING; WOUND HEALING;

EID: 84880751701     PISSN: 01791958     EISSN: 14321262     Source Type: Journal    
DOI: 10.1007/s00384-013-1641-9     Document Type: Article

References (34)

1. Markowitz SD, Bertagnolli MM (2009) Molecular origins of cancer: molecular basis of colorectal cancer. N Engl J Med 361(25):2449-2460
2. Wang WS, Chen PM, Su Y (2009) Colorectal carcinoma: from tumorigenesis to treatment. Cell Mol Life Sci 63(6):663-671
3. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Murray T, Thun MJ (2008) Cancer statistics, 2008. CA Cancer J Clin 58(2):71-96
4. Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479-507
5. Georgas K, Burridge L, Smith K, Holmes GP, Chenevix-Trench G, Ioannou PA, Little MH (1999) Assignment of the human slit homologue SLIT2 to human chromosome band 4p15.2. Cytogenet Cell Genet 86(3-4):246-247
6. Nguyen-Ba-Charvet KT, Chedotal A (2002) Role of Slit proteins in the vertebrate brain. J Physiol Paris 96(1-2):91-98
7. Wong K, Ren XR, Huang YZ, Xie Y, Liu G, Saito H, Tang H, Wen L, Brady-Kalnay SM, Mei L, Wu JY, Xiong WC, Rao Y (2001) Signal transduction in neuronal migration: roles of GTPase activating proteins and the small GTPase Cdc42 in the Slit-Robo pathway. Cell 107(2):209-221
8. Liao WX, Wing DA, Geng JG, Chen DB (2010) Perspectives of SLIT/ROBO signaling in placental angiogenesis. Histol Histopathol 25(9):1181-1190
9. Liu D, Hou J, Hu X, Wang X, Xiao Y, Mou Y, De Leon H (2006) Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ Res 98(4):480-489
10. Jin J, You H, Yu B, Deng Y, Tang N, Yao G, Shu H, Yang S, Qin W (2009) Epigenetic inactivation of SLIT2 in human hepatocellular carcinomas. Biochem Biophys Res Commun 379(1):86-91
11. Tseng RC, Lee SH, Hsu HS, Chen BH, Tsai WC, Tzao C, Wang YC (2010) SLIT2 attenuation during lung cancer progression deregulates beta-catenin and E-cadherin and associates with poor prognosis. Cancer Res 70(2):543-551
12. Narayan G, Goparaju C, Arias-Pulido H, Kaufmann AM, Schneider A, Dürst M, Mansukhani M, Pothuri B, Murty VV (2006) Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol Cancer 5:16
13. Xu Y, Li WL, Fu L, Gu F, Ma YJ (2010) Slit2/Robo1 signaling in glioma migration and invasion. Neurosci Bull 26(6):474-478
14. Dunwell TL, Dickinson RE, Stankovic T, Dallol A, Weston V, Austen B, Catchpoole D, Maher ER, Latif F (2009) Frequent epigenetic inactivation of the SLIT2 gene in chronic and acute lymphocytic leukemia. Epigenetics 4(4):265-269
15. Kim HK, Zhang H, Li H, Wu TT, Swisher S, He D, Wu L, Xu J, Elmets CA, Athar M, Xu XC, Xu H (2008) Slit2 inhibits growth and metastasis of fibrosarcoma and squamous cell carcinoma. Neoplasia 10(12):1411-1420
16. Prasad A, Paruchuri V, Preet A, Latif F, Ganju RK (2008) Slit-2 induces a tumor-suppressive effect by regulating beta-catenin in breast cancer cells. J Biol Chem 283(39):26624-26633
17. Astuti D, Da Silva NF, Dallol A, Gentle D, Martinsson T, Kogner P, Grundy R, Kishida T, Yao M, Latif F, Maher ER (2004) SLIT2 promoter methylation analysis in neuroblastoma, Wilms' tumour and renal cell carcinoma. Br J Cancer 90(2):515-521
18. Dallol A, Da Silva NF, Viacava P, Minna JD, Bieche I, Maher ER, Latif F (2002) SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer Res 62(20):5874-5880
19. Dallol A, Krex D, Hesson L, Eng C, Maher ER, Latif F (2003) Frequent epigenetic inactivation of the SLIT2 gene in gliomas. Oncogene 22(29):4611-4616
20. Dallol A, Morton D, Maher ER, Latif F (2003) SLIT2 axon guidance molecule is frequently inactivated in colorectal cancer and suppresses growth of colorectal carcinoma cells. Cancer Res 63(5):1054-1058
21. Zhou WJ, Geng ZH, Chi S, Zhang W, Niu XF, Lan SJ, Ma L, Yang X, Wang LJ, Ding YQ, Geng JG (2011) Slit-Robo signaling induces malignant transformation through Hakai-mediated E-cadherin degradation during colorectal epithelial cell carcinogenesis. Cell Res 21(4):609-626
22. Chen RH, Ding WV, McCormick F (2000) Wnt signaling to beta-catenin involves two interactive components. Glycogen synthase kinase-3beta inhibition and activation of protein kinase C. J Biol Chem 275(23):17894-17899
23. Schmalhofer O, Brabletz S, Brabletz T (2009) E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev 28(1-2):151-166
24. Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, Cha SY, Ryu JK, Choi YJ, Kim J, Fearon ER, Weiss SJ (2006) A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 8(12):1398-1406
25. Qiao M, Sheng S, Pardee AB (2008) Metastasis and AKT activation. Cell Cycle 7(19):2991-2996
26. Katoh M, Katoh M (2006) Cross-talk of WNT and FGF signaling pathways at GSK3beta to regulate beta-catenin and SNAIL signaling cascades. Cancer Biol Ther 5(9):1059-1064
27. Yook JI, Li XY, Ota I, Fearon ER, Weiss SJ (2005) Wnt-dependent regulation of the E-cadherin repressor snail. J Biol Chem 280(12):11740-11748
28. Kaidanovich O, Eldar-Finkelman H (2002) The role of glycogen synthase kinase-3 in insulin resistance and type 2 diabetes. Expert Opin Ther Targets 6(5):555-561
29. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung MC (2004) Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6(10):931-940
30. Moreno-Bueno G, Portillo F, Cano A (2008) Transcriptional regulation of cell polarity in EMT and cancer. Oncogene 27(55):6958-6969
31. Becker KF, Rosivatz E, Blechschmidt K, Kremmer E, Sarbia M, Höfler H (2007) Analysis of the E-cadherin repressor Snail in primary human cancers. Cells Tissues Organs 185(1-3):204-212
32. Unni D (2010) Role of Slit and Robo in the development of midline glia and corpus callosum. PhD Thesis, Queensland Brain Institute, The University of Queensland
33. Dai CF, Jiang YZ, Li Y, Wang K, Liu PS, Patankar MS, Zheng J (2011) Expression and roles of Slit/Robo in human ovarian cancer. Histochem Cell Biol 135(5):475-485
34. Dickinson RE, Dallol A, Bieche I, Krex D, Morton D, Maher ER, Latif F (2004) Epigenetic inactivation of SLIT3 and SLIT1 genes in human cancers. Br J Cancer 91(12):2071-2078