Slit2/robo1 signaling promotes intestinal tumorigenesis through src-mediated activation of the wnt/β-catenin pathway

Oncotarget

Volumn 6, Issue 5, 2015, Pages 3123-3135

  Zhang, Qian Qian ^a   Zhou, Da Lei ^a   Lei, Yan ^a   Zheng, Li ^a   Chen, Sheng Xia ^a   Gou, Hong Ju ^c   Gu, Qu Liang ^a   He, Xiao Dong ^a   Lan, Tian ^a   Qi, Cui Ling ^a   Li, Jiang Chao ^a   Ding, Yan Qing ^c   Qiao, Liang ^b   Wang, Li Jing ^a  

^a GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

^b UNIVERSITY OF SYDNEY   (Australia)

^c SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

E cadherin; Intestinal tumors; Slit2 Robo1 signaling; Src; Wnt catenin

Indexed keywords

BETA CATENIN; PROTEIN TYROSINE KINASE; ROUNDABOUT RECEPTOR; SLIT2 PROTEIN; WNT PROTEIN; CTNNB1 PROTEIN, HUMAN; CTNNB1 PROTEIN, MOUSE; IMMUNOGLOBULIN RECEPTOR; NERVE PROTEIN; SIGNAL PEPTIDE; SLIT HOMOLOG 2 PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CANCER STAGING; CARCINOGENESIS; CELL GROWTH; CELL MIGRATION; COLORECTAL CARCINOMA; CONTROLLED STUDY; FEMALE; HUMAN; INTESTINE CANCER; INTESTINE MUCOSA; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH; TUMOR INVASION; ADENOMA; ANIMAL; C57BL MOUSE; CARCINOMA; CELL PROLIFERATION; CELL TRANSFORMATION; COLORECTAL TUMOR; DISEASE COURSE; DISEASE MODEL; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HCT 116 CELL LINE; METABOLISM; MIDDLE AGED; PATHOLOGY; RNA INTERFERENCE; TRANSGENIC MOUSE; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; WNT SIGNALING PATHWAY;

ADENOMA; ANIMALS; BETA CATENIN; CARCINOMA; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; COLORECTAL NEOPLASMS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; GENES, APC; HCT116 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTESTINAL MUCOSA; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MIDDLE AGED; NERVE TISSUE PROTEINS; RECEPTORS, IMMUNOLOGIC; RNA INTERFERENCE; SRC-FAMILY KINASES; TRANSFECTION; TUMOR BURDEN; WNT SIGNALING PATHWAY;

EID: 84923280655     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3060     Document Type: Article

References (41)

1. Sancho E, Batlle E, Clevers H. Signaling pathways in intestinal development and cancer. Annu Rev Cell Dev Biol. 2004; 20: 695-723.
2. Ansher AF, Lewis JH, Fleischer DE, Cattau EL, Jr., Collen MJ, O'Kieffe DA, Korman LY, Benjamin SB. Hyperplastic colonic polyps as a marker for adenomatous colonic polyps. Am J Gastroenterol. 1989; 84: 113-117.
3. Terzic J, Grivennikov S, Karin E, Karin M. Inflammation and colon cancer. Gastroenterology. 2010; 138: 2101-2114 e2105.
4. Grone J, Doebler O, Loddenkemper C, Hotz B, Buhr HJ, Bhargava S. Robo1/Robo4: differential expression of angiogenic markers in colorectal cancer. Oncol Rep. 2006; 15: 1437-1443.
5. Latil A, Chene L, Cochant-Priollet B, Mangin P, Fournier G, Berthon P, Cussenot O. Quantification of expression of netrins, slits and their receptors in human prostate tumors. Int J Cancer. 2003; 103: 306-315.
6. Zhou WJ, Geng ZH, Chi S, Zhang W, Niu XF, Lan SJ, Ma L, Yang X, Wang LJ, Ding YQ, Geng JG. Slit-Robo signaling induces malignant transformation through Hakai-mediated E-cadherin degradation during colorectal epithelial cell carcinogenesis. Cell research. 2011; 21: 609-626.
7. Wang B, Xiao Y, Ding BB, Zhang N, Yuan X, Gui L, Qian KX, Duan S, Chen Z, Rao Y, Geng JG. Induction of tumor angiogenesis by Slit-Robo signaling and inhibition of cancer growth by blocking Robo activity. Cancer Cell. 2003; 4: 19-29.
8. Kim HK, Zhang H, Li H, Wu TT, Swisher S, He D, Wu L, Xu J, Elmets CA, Athar M, Xu XC, Xu H. Slit2 inhibits growth and metastasis of fibrosarcoma and squamous cell carcinoma. Neoplasia. 2008; 10: 1411-1420.
9. Dunaway CM, Hwang Y, Lindsley CW, Cook RS, Wu JY, Boothby M, Chen J, Brantley-Sieders DM. Cooperative signaling between Slit2 and Ephrin-A1 regulates a balance between angiogenesis and angiostasis. Molecular and cellular biology. 2011; 31: 404-416.
10. Shi R, Liu W, Liu B, Xu Z, Chen L, Zhang Z. Slit2 expression and its correlation with subcellular localization of beta-catenin in gastric cancer. Oncol Rep. 2013; 30: 1883-1889.
11. Kopetz S. Targeting SRC and epidermal growth factor receptor in colorectal cancer: rationale and progress into the clinic. Gastrointest Cancer Res. 2007; 1: S37-41.
12. Bolen JB, Veillette A, Schwartz AM, Deseau V, Rosen N. Analysis of pp60c-src in human colon carcinoma and normal human colon mucosal cells. Oncogene Res. 1987; 1: 149-168.
13. DeSeau V, Rosen N, Bolen JB. Analysis of pp60c-src tyrosine kinase activity and phosphotyrosyl phosphatase activity in human colon carcinoma and normal human colon mucosal cells. J Cell Biochem. 1987; 35: 113-128.
14. Kajla S, Mondol AS, Nagasawa A, Zhang Y, Kato M, Matsuno K, Yabe-Nishimura C, Kamata T. A crucial role for Nox 1 in redox-dependent regulation of Wnt-beta-catenin signaling. FASEB J. 2012; 26: 2049-2059.
15. Yokoyama N, Malbon CC. Dishevelled-2 docks and activates Src in a Wnt-dependent manner. J Cell Sci. 2009; 122: 4439-4451.
16. Avizienyte E, Wyke AW, Jones RJ, McLean GW, Westhoff MA, Brunton VG, Frame MC. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nature cell biology. 2002; 4: 632-638.
17. Rosenberg DW, Giardina C, Tanaka T. Mouse models for the study of colon carcinogenesis. Carcinogenesis. 2009; 30: 183-196.
18. Ou CY, LaBonte MJ, Manegold PC, So AY, Ianculescu I, Gerke DS, Yamamoto KR, Ladner RD, Kahn M, Kim JH, Stallcup MR. A coactivator role of CARM1 in the dysregulation of beta-catenin activity in colorectal cancer cell growth and gene expression. Mol Cancer Res. 2011; 9: 660-670.
19. Martinez-Moreno JM, Munoz-Castaneda JR, Herencia C, Oca AM, Estepa JC, Canalejo R, Rodriguez-Ortiz ME, Perez-Martinez P, Aguilera-Tejero E, Canalejo A, Rodriguez M, Almaden Y. In vascular smooth muscle cells paricalcitol prevents phosphate-induced Wnt/beta-catenin activation. Am J Physiol Renal Physiol. 2012; 303: F1136-1144.
20. Orsulic S, Huber O, Aberle H, Arnold S, Kemler R. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J Cell Sci. 1999; 112 (Pt 8): 1237-1245.
21. Singh RK, Indra D, Mitra S, Mondal RK, Basu PS, Roy A, Roychowdhury S, Panda CK. Deletions in chromosome 4 differentially associated with the development of cervical cancer: evidence of slit2 as a candidate tumor suppressor gene. Human genetics. 2007; 122: 71-81.
22. Narayan G, Goparaju C, Arias-Pulido H, Kaufmann AM, Schneider A, Durst M, Mansukhani M, Pothuri B, Murty VV. Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Molecular cancer. 2006; 5: 16.
23. Dallol A, Da Silva NF, Viacava P, Minna JD, Bieche I, Maher ER, Latif F. SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer research. 2002; 62: 5874-5880.
24. Chen WF, Gao WD, Li QL, Zhou PH, Xu MD, Yao LQ. SLIT2 inhibits cell migration in colorectal cancer through the AKT-GSK3beta signaling pathway. Int J Colorectal Dis. 2013; 28: 933-940.
25. Dallol A, Morton D, Maher ER, Latif F. SLIT2 axon guidance molecule is frequently inactivated in colorectal cancer and suppresses growth of colorectal carcinoma cells. Cancer research. 2003; 63: 1054-1058.
26. Yiin JJ, Hu B, Jarzynka MJ, Feng H, Liu KW, Wu JY, Ma HI, Cheng SY. Slit2 inhibits glioma cell invasion in the brain by suppression of Cdc42 activity. Neuro Oncol. 2009; 11: 779-789.
27. Qi C, Lan H, Ye J, Li W, Wei P, Yang Y, Guo S, Lan T, Li J, Zhang Q, He X, Wang L. Slit2 promotes tumor growth and invasion in chemically induced skin carcinogenesis. Lab Invest. 2014: DOI: 10.1038/labinvest.2014.1070.
28. Zhou WJ, Geng ZH, Spence JR, Geng JG. Induction of intestinal stem cells by R-spondin 1 and Slit2 augments chemoradioprotection. Nature. 2013; 501: 107-111.
29. Roncucci L, Medline A, Bruce WR. Classification of aberrant crypt foci and microadenomas in human colon. Cancer Epidemiol Biomarkers Prev. 1991; 1: 57-60.
30. Nascimbeni R, Donato F, Ghirardi M, Mariani P, Villanacci V, Salerni B. Constipation, anthranoid laxatives, melanosis coli, and colon cancer: a risk assessment using aberrant crypt foci. Cancer Epidemiol Biomarkers Prev. 2002; 11: 753-757.
31. Zoghbi S, Drouin E, Claustre J, Bara J, Scoazec JY, Plaisancie P. Intestinal MUC2 and gastric M1/MUC5AC in preneoplastic lesions induced by 1,2-dimethylhydrazine in rat: a sequential analysis. Int J Oncol. 2007; 30: 489-497.
32. Cartwright CA, Meisler AI, Eckhart W. Activation of the pp60c-src protein kinase is an early event in colonic carcinogenesis. Proc Natl Acad Sci U S A. 1990; 87: 558-562.
33. Levitzki A. SRC as a target for anti-cancer drugs. Anticancer Drug Des. 1996; 11: 175-182.
34. Irby R, Mao W, Coppola D, Jove R, Gamero A, Cuthbertson D, Fujita DJ, Yeatman TJ. Overexpression of normal c-Src in poorly metastatic human colon cancer cells enhances primary tumor growth but not metastatic potential. Cell Growth Differ. 1997; 8: 1287-1295.
35. Mao W, Irby R, Coppola D, Fu L, Wloch M, Turner J, Yu H, Garcia R, Jove R, Yeatman TJ. Activation of c-Src by receptor tyrosine kinases in human colon cancer cells with high metastatic potential. Oncogene. 1997; 15: 3083-3090.
36. Courtneidge SA, Fumagalli S, Koegl M, Superti-Furga G, Twamley-Stein GM. The Src family of protein tyrosine kinases: regulation and functions. Dev Suppl. 1993: 57-64.
37. LaVallee TM, Prudovsky IA, McMahon GA, Hu X, Maciag T. Activation of the MAP kinase pathway by FGF-1 correlates with cell proliferation induction while activation of the Src pathway correlates with migration. J Cell Biol. 1998; 141: 1647-1658.
38. Luttrell DK, Lee A, Lansing TJ, Crosby RM, Jung KD, Willard D, Luther M, Rodriguez M, Berman J, Gilmer TM. Involvement of pp60c-src with two major signaling pathways in human breast cancer. Proc Natl Acad Sci U S A. 1994; 91: 83-87.
39. Rahimi N, Hung W, Tremblay E, Saulnier R, Elliott B. c-Src kinase activity is required for hepatocyte growth factor-induced motility and anchorage-independent growth of mammary carcinoma cells. J Biol Chem. 1998; 273: 33714-33721.
40. Yang XM, Han HX, Sui F, Dai YM, Chen M, Geng JG. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem Biophys Res Commun. 2010; 396: 571-577.
41. Xu H, He JH, Xiao ZD, Zhang QQ, Chen YQ, Zhou H, Qu LH. Liver-Enriched Transcription Factors Regulate MicroRNA-122 That Targets CUTL1 During Liver Development. Hepatology. 2010; 52: 1431-1442.