P38 and JNK pathways control E-selectin-dependent extravasation of colon cancer cells by modulating miR-31 transcription

Oncotarget

Volumn 8, Issue 1, 2017, Pages 1678-1687

  Zhong, Liang ^a   Simoneau, Bryan ^a   Huot, Jacques ^a   Simard, Martin J ^a  

^a LAVAL UNIVERSITY   (Canada)

Author keywords

C Fos; C Jun; Endothelial cells; GATA2; IL 1 metastasis

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; INTERLEUKIN 1BETA; MESSENGER RNA; MICRORNA 31; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN C FOS; PROTEIN C JUN; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR GATA 2; GATA2 PROTEIN, HUMAN; IL1B PROTEIN, HUMAN; MICRORNA; MIRN31 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CANCER CELL; CELL ADHESION; CELL MIGRATION; COLON CANCER CELL; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; GENE REPRESSION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA TRANSCRIPTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; COLON TUMOR; GENETICS; HEK293 CELL LINE; HT-29 CELL LINE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR EMBOLISM;

CELL ADHESION; CELL LINE, TUMOR; COLONIC NEOPLASMS; E-SELECTIN; ENDOTHELIAL CELLS; GATA2 TRANSCRIPTION FACTOR; HEK293 CELLS; HT29 CELLS; HUMANS; INTERLEUKIN-1BETA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICRORNAS; NEOPLASTIC CELLS, CIRCULATING; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 85009754925     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.13779     Document Type: Article

References (30)

1. Gout, S., Huot, J. Role of cancer microenvironmentin metastasis: Focus on colon cancer. Cancer Microenvironment. 2008; 1:69-83.
2. Gout, S., Tremblay, P.L., Huot, J. Selectins and selectin ligands in extravasation of cancer cells and organ selectivity of metastasis. Clin Exp Metastasis. 2008; 25:335-344.
3. Vestweber, D., Blanks, J.E. Mechanisms that regulate the function of the selectins and their ligands. Physiol Rev. 1999; 79:181-213.
4. Laferriere, J., Houle, F., Huot, J. Adhesion of HT-29 colon carcinoma cells to endothelial cells requires sequential events involving E-selectin and integrin beta4. Clin Exp Metastasis. 2004; 21:257-264.
5. Sawada, R., Tsuboi, S., Fukuda, M. Differential E-selectindependent adhesion efficiency in sublines of a human colon cancer exhibiting distinct metastatic potentials. The Journal of biological chemistry. 1994; 269:1425-1431.
6. Brodt, P., Fallavollita, L., Bresalier, R.S., Meterissian, S., Norton, C.R., Wolitzky, B.A. Liver endothelial E-selectin mediates carcinoma cell adhesion and promotes liver metastasis. Int J Cancer. 1997; 71:612-619.
7. Reymond, N., d'Agua, B.B., Ridley, A.J. Crossing the endothelial barrier during metastasis. Nature reviews Cancer. 2013; 13: 858-870.
8. Subramaniam, M., Koedam, J.A., Wagner, D.D. Divergent fates of P-and E-selectins after their expression on the plasma membrane. Molecular biology of the cell. 1993; 4:791-801.
9. Suarez, Y., Wang, C., Manes, T.D., Pober, J.S. Cutting edge: TNF-induced microRNAs regulate TNF-induced expression of E-selectin and intercellular adhesion molecule-1 on human endothelial cells: feedback control of inflammation. J Immunol. 2010; 184:21-25.
10. Laferriere, J., Houle, F., Taher, M.M., Valerie, K., Huot, J. Transendothelial migration of colon carcinoma cells requires expression of E-selectin by endothelial cells and activation of stress-activated protein kinase-2 (SAPK2/p38) in the tumor cells. The Journal of biological chemistry. 2001; 276:33762-33772.
11. Meziane, O., Piquet, S., Bosse, G.D., Gagne, D., Paquet, E., Robert, C., Tones, M.A., Simard, M.J. The human decapping scavenger enzyme DcpS modulates microRNA turnover. Sci Rep. 2015; 5:16688.
12. Lin PC, Chiu YL, Banerjee S, Park K, Mosquera JM, Giannopoulou E, Alves P, Tewari AK, Gerstein MB, Beltran H, Melnick AM, Elemento O, Demichelis F, et al. Epigenetic repression of miR-31 disrupts androgen receptor homeostasis and contributes to prostate cancer progression. Cancer research. 2013; 73:1232-1244.
13. Laferriere, J., Houle, F., Huot, J. Regulation of the metastatic process by E-selectin and stress-activated protein kinase-2/p38. Ann N Y Acad Sci. 2002; 973:562-572.
14. Prasad, R., Giri, S., Nath, N., Singh, I., Singh, A.K. Inhibition of phosphoinositide 3 kinase-Akt (protein kinase B)-nuclear factor-kappa B pathway by lovastatin limits endothelial-monocyte cell interaction. J Neurochem. 2005; 94: 204-214.
15. Tanigawa N, Hagiwara M, Tada H, Komatsu T, Sugiura S, Kobayashi K, Kato Y, Ishida N, Nishida K, Ninomiya M, Koketsu M, Matsushita K. Acacetin inhibits expression of E-selectin on endothelial cells through regulation of the MAP kinase signaling pathway and activation of NF-kappaB. Immunopharmacol Immunotoxicol. 2013; 35:471-477.
16. Minden, A., Lin, A., Smeal, T., Derijard, B., Cobb, M., Davis, R., Karin, M. c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Molecular and cellular biology. 1994; 14:6683-6688.
17. Baumgartner, C., Baccarini, M. p38 links RAS to GATA2. EMBO Rep. 2014; 15:912-913.
18. Chen, S., Qiong, Y., Gardner, D.G. A role for p38 mitogenactivated protein kinase and c-myc in endothelin-dependent rat aortic smooth muscle cell proliferation. Hypertension. 2006; 47:252-258.
19. Tanos, T., Marinissen, M.J., Leskow, F.C., Hochbaum, D., Martinetto, H., Gutkind, J.S., Coso, O.A. Phosphorylation of c-Fos by members of the p38 MAPK family. Role in the AP-1 response to UV light. The Journal of biological chemistry. 2005; 280:18842-18852.
20. Zarubin, T., Han, J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005; 15:11-18.
21. Faryammanesh, R., Lange, T., Magbanua, E., Haas, S., Meyer, C., Wicklein, D., Schumacher, U., Hahn, U. SDA, a DNA aptamer inhibiting E-and P-selectin mediated adhesion of cancer and leukemia cells, the first and pivotal step in transendothelial migration during metastasis formation. PloS one. 2014; 9:e93173.
22. Gout, S., Morin, C., Houle, F., Huot, J. Death receptor-3, a new E-Selectin counter-receptor that confers migration and survival advantages to colon carcinoma cells by triggering p38 and ERK MAPK activation. Cancer research. 2006; 66:9117-9124.
23. Kawana, M., Lee, M.E., Quertermous, E.E., Quertermous, T. Cooperative interaction of GATA-2 and AP1 regulates transcription of the endothelin-1 gene. Molecular and cellular biology. 1995; 15:4225-4231.
24. Schmiedel, J.M., Klemm, S.L., Zheng, Y., Sahay, A., Bluthgen, N., Marks, D.S., van Oudenaarden, A. Gene expression. MicroRNA control of protein expression noise. Science. 2015; 348:128-132.
25. Rasheed, S.A., Teo, C.R., Beillard, E.J., Voorhoeve, P.M., Zhou, W., Ghosh, S., Casey, P.J. MicroRNA-31 controls G protein alpha-13 (GNA13) expression and cell invasion in breast cancer cells. Mol Cancer. 2015; 14:67.
26. Sossey-Alaoui, K., Downs-Kelly, E., Das, M., Izem, L., Tubbs, R., Plow, E.F. WAVE3, an actin remodeling protein, is regulated by the metastasis suppressor microRNA, miR-31, during the invasion-metastasis cascade. Int J Cancer. 2011; 129:1331-1343.
27. Ruoming, W., Zhen, Y., Tengteng, Z., Jisheng, H. Tumor suppressor microRNA-31 inhibits gastric carcinogenesis by targeting Smad4 and SGPP2. Cancer Gene Ther. 2015; 22:564-572.
28. Zhang, X.B., Song, L., Wen, H.J., Bai, X.X., Li, Z.J., Ma, L.J. Upregulation of microRNA-31 targeting integrin alpha5 suppresses tumor cell invasion and metastasis by indirectly regulating PI3K/AKT pathway in human gastric cancer SGC7901 cells. Tumour Biol. 2016; 37:8317.
29. Huot, J., Houle, F., Marceau, F., Landry, J. Oxidative stressinduced actin reorganization mediated by the p38 mitogenactivated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res. 1997; 80:383-392.
30. Hutvagner, G., Simard, M.J., Mello, C.C., Zamore, P.D. Sequence-specific inhibition of small RNA function. PLoS Biol. 2004; 2:E98.