The MiR-1-NOTCH3-Asef Pathway is Important for Colorectal Tumor Cell Migration

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2013 Nov 19

PMID 24244701

Citations 22

Authors

Shiori Furukawa

Yoshihiro Kawasaki

Masaya Miyamoto

Masaya Hiyoshi

Joji Kitayama

Tetsu Akiyama

Affiliations

Soon will be listed here.

Abstract

The tumor suppressor adenomatous polyposis coli (APC) is mutated in sporadic and familial colorectal tumors. APC stimulates the activity of the Cdc42- and Rac1-specific guanine nucleotide exchange factor Asef and promotes the migration and invasion of colorectal tumor cells. Furthermore, Asef is overexpressed in colorectal tumors and is required for colorectal tumorigenesis. It is also known that NOTCH signaling plays critical roles in colorectal tumorigenesis and fate determination of intestinal progenitor cells. Here we show that NOTCH3 up-regulates Asef expression by activating the Asef promoter in colorectal tumor cells. Moreover, we demonstrate that microRNA-1 (miR-1) is down-regulated in colorectal tumors and that miR-1 has the potential to suppress NOTCH3 expression through direct binding to its 3'-UTR region. These results suggest that the miR-1-NOTCH3-Asef pathway is important for colorectal tumor cell migration and may be a promising molecular target for the treatment of colorectal tumors.

Citing Articles

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Propofol regulates miR-1-3p/IGF1 axis to inhibit the proliferation and accelerates apoptosis of colorectal cancer cells.

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Xiu M, Wang Y, Li B, Wang X, Xiao F, Chen S Front Mol Biosci. 2021; 8:694141.

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References

Nasser M, Datta J, Nuovo G, Kutay H, Motiwala T, Majumder S . Down-regulation of micro-RNA-1 (miR-1) in lung cancer. Suppression of tumorigenic property of lung cancer cells and their sensitization to doxorubicin-induced apoptosis by miR-1. J Biol Chem. 2008; 283(48):33394-405. PMC: 2586284. DOI: 10.1074/jbc.M804788200. View

Baron M . An overview of the Notch signalling pathway. Semin Cell Dev Biol. 2003; 14(2):113-9. DOI: 10.1016/s1084-9521(02)00179-9. View

Hamann M, Lubking C, Luchini D, Billadeau D . Asef2 functions as a Cdc42 exchange factor and is stimulated by the release of an autoinhibitory module from a concealed C-terminal activation element. Mol Cell Biol. 2006; 27(4):1380-93. PMC: 1800726. DOI: 10.1128/MCB.01608-06. View

Akiyoshi T, Nakamura M, Yanai K, Nagai S, Wada J, Koga K . Gamma-secretase inhibitors enhance taxane-induced mitotic arrest and apoptosis in colon cancer cells. Gastroenterology. 2008; 134(1):131-44. DOI: 10.1053/j.gastro.2007.10.008. View

Huang F, Tang L, Fang Z, Hu X, Pan J, Zhou S . miR-1-mediated induction of cardiogenesis in mesenchymal stem cells via downregulation of Hes-1. Biomed Res Int. 2013; 2013:216286. PMC: 3591156. DOI: 10.1155/2013/216286. View

Indraccolo S, Minuzzo S, Masiero M, Pusceddu I, Persano L, Moserle L . Cross-talk between tumor and endothelial cells involving the Notch3-Dll4 interaction marks escape from tumor dormancy. Cancer Res. 2009; 69(4):1314-23. DOI: 10.1158/0008-5472.CAN-08-2791. View

Kawasaki Y, Sato R, Akiyama T . Mutated APC and Asef are involved in the migration of colorectal tumour cells. Nat Cell Biol. 2003; 5(3):211-5. DOI: 10.1038/ncb937. View

Rodilla V, Villanueva A, Obrador-Hevia A, Robert-Moreno A, Fernandez-Majada V, Grilli A . Jagged1 is the pathological link between Wnt and Notch pathways in colorectal cancer. Proc Natl Acad Sci U S A. 2009; 106(15):6315-20. PMC: 2669348. DOI: 10.1073/pnas.0813221106. View

Cadigan K, Nusse R . Wnt signaling: a common theme in animal development. Genes Dev. 1998; 11(24):3286-305. DOI: 10.1101/gad.11.24.3286. View

10.

Anton R, Chatterjee S, Simundza J, Cowin P, DasGupta R . A systematic screen for micro-RNAs regulating the canonical Wnt pathway. PLoS One. 2011; 6(10):e26257. PMC: 3197157. DOI: 10.1371/journal.pone.0026257. View

11.

Nickoloff B, Osborne B, Miele L . Notch signaling as a therapeutic target in cancer: a new approach to the development of cell fate modifying agents. Oncogene. 2003; 22(42):6598-608. DOI: 10.1038/sj.onc.1206758. View

12.

GREENWALD I . LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 1998; 12(12):1751-62. DOI: 10.1101/gad.12.12.1751. View

13.

Kwon C, Han Z, Olson E, Srivastava D . MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc Natl Acad Sci U S A. 2005; 102(52):18986-91. PMC: 1315275. DOI: 10.1073/pnas.0509535102. View

14.

Song G, Zhang Y, Wang L . MicroRNA-206 targets notch3, activates apoptosis, and inhibits tumor cell migration and focus formation. J Biol Chem. 2009; 284(46):31921-7. PMC: 2797263. DOI: 10.1074/jbc.M109.046862. View

15.

Kinzler K, Vogelstein B . Lessons from hereditary colorectal cancer. Cell. 1996; 87(2):159-70. DOI: 10.1016/s0092-8674(00)81333-1. View

16.

Sonoshita M, Aoki M, Fuwa H, Aoki K, Hosogi H, Sakai Y . Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell. 2011; 19(1):125-37. DOI: 10.1016/j.ccr.2010.11.008. View

17.

Bienz M, Clevers H . Linking colorectal cancer to Wnt signaling. Cell. 2000; 103(2):311-20. DOI: 10.1016/s0092-8674(00)00122-7. View

18.

Peifer M, Polakis P . Wnt signaling in oncogenesis and embryogenesis--a look outside the nucleus. Science. 2000; 287(5458):1606-9. DOI: 10.1126/science.287.5458.1606. View

19.

Sarver A, French A, Borralho P, Thayanithy V, Oberg A, Silverstein K . Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer. 2009; 9:401. PMC: 2787532. DOI: 10.1186/1471-2407-9-401. View

20.

Kawasaki Y, Sagara M, Shibata Y, Shirouzu M, Yokoyama S, Akiyama T . Identification and characterization of Asef2, a guanine-nucleotide exchange factor specific for Rac1 and Cdc42. Oncogene. 2007; 26(55):7620-267. DOI: 10.1038/sj.onc.1210574. View