CD24 Induces Expression of the Oncomir miR-21 via Src, and CD24 and Src Are Both Post-Transcriptionally Downregulated by the Tumor Suppressor miR-34a

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Muppala, Santoshi ^a   Mudduluru, Giridhar ^a   Leupold, Jörg H ^a   Buergy, Daniel ^a   Sleeman, Jonathan P ^b,c   Allgayer, Heike ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD24 ANTIGEN; MICRORNA 21; MICRORNA 34A; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN C FOS; PROTEIN C JUN; PROTEIN PDCD4; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; SRC KINASE; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CANCER INVASION; CLINICAL ARTICLE; COLON CANCER; CONTROLLED STUDY; CORRELATIONAL STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; MIGRATION INHIBITION; MOLECULAR INTERACTION; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANTIGENS, CD24; CELL LINE, TUMOR; HCT116 CELLS; HT29 CELLS; HUMANS; MICRORNAS; PROTO-ONCOGENE PROTEINS PP60(C-SRC);

EID: 84875316099     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059563     Document Type: Article

References (54)

1. Croce CM, (2008) Oncogenes and cancer. N Engl J Med 358: 502-511.
2. Sleeman JP, (2000) The lymph node as a bridgehead in the metastatic dissemination of tumors. Recent Results Cancer Res 157: 55-81.
3. Sporn MB, (1996) The war on cancer. Lancet 347: 1377-1381.
4. Kristiansen G, Sammar M, Altevogt P, (2004) Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol 35: 255-262.
5. Nestl A, Von Stein OD, Zatloukal K, Thies WG, Herrlich P, et al. (2001) Gene expression patterns associated with the metastatic phenotype in rodent and human tumors. Cancer Res 61: 1569-1577.
6. Pedersen MW, Thykjaer T, Orntoft TF, Damstrup L, Poulsen HS, (2001) Profile of differentially expressed genes mediated by the type III epidermal growth factor receptor mutation expressed in a small-cell lung cancer cell line. Br J Cancer 85: 1211-1218.
7. Baumann P, Cremers N, Kroese F, Orend G, Chiquet-Ehrismann R, et al. (2005) CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 65: 10783-10793.
8. Senner V, Sturm A, Baur I, Schrell UH, Distel L, et al. (1999) CD24 promotes invasion of glioma cells in vivo. J Neuropathol Exp Neurol 58: 795-802.
9. Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, et al. (1998) CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 12: 1241-1251.
10. Celi A, Furie B, Furie BC, (1991) PADGEM: an adhesion receptor for leukocytes on stimulated platelets and endothelial cells. Proc Soc Exp Biol Med 198: 703-709.
11. McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF, (1989) GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest 84: 92-99.
12. Bevilacqua MP, Pober JS, Mendrick DL, Cotran RS, Gimbrone MA Jr, (1987) Identification of an inducible endothelial-leukocyte adhesion molecule. Proc Natl Acad Sci U S A 84: 9238-9242.
13. Schabath H, Runz S, Joumaa S, Altevogt P, (2006) CD24 affects CXCR4 function in pre-B lymphocytes and breast carcinoma cells. J Cell Sci 119: 314-325.
14. Baumann P, Thiele W, Cremers N, Muppala S, Krachulec J, et al. (2011) CD24 interacts with and promotes the activity of c-src within lipid rafts in breast cancer cells, thereby increasing integrin-dependent adhesion. Cell Mol Life Sci.
15. Brunton VG, Frame MC, (2008) Src and focal adhesion kinase as therapeutic targets in cancer. Curr Opin Pharmacol 8: 427-432.
16. Aligayer H, Boyd DD, Heiss MM, Abdalla EK, Curley SA, et al. (2002) Activation of Src kinase in primary colorectal carcinoma: an indicator of poor clinical prognosis. Cancer 94: 344-351.
17. Alvarez RH, Kantarjian HM, Cortes JE, (2006) The role of Src in solid and hematologic malignancies: development of new-generation Src inhibitors. Cancer 107: 1918-1929.
18. Luo Y, Liang F, Zhang ZY, (2009) PRL1 promotes cell migration and invasion by increasing MMP2 and MMP9 expression through Src and ERK1/2 pathways. Biochemistry 48: 1838-1846.
19. Jochum W, Passegue E, Wagner EF, (2001) AP-1 in mouse development and tumorigenesis. Oncogene 20: 2401-2412.
20. Asangani IA, Rasheed SA, Nikolova DA, Leupold JH, Colburn NH, et al. (2008) MicroRNA-21 (miR-21) post-transcriptionally downregulates tumor suppressor Pdcd4 and stimulates invasion, intravasation and metastasis in colorectal cancer. Oncogene 27: 2128-2136.
21. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, et al. (2007) MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133: 647-658.
22. Fujita S, Ito T, Mizutani T, Minoguchi S, Yamamichi N, et al. (2008) miR-21 Gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol 378: 492-504.
23. Mudduluru G, George-William JN, Muppala S, Asangani IA, Kumarswamy R, et al. (2011) Curcumin regulates miR-21 expression and inhibits invasion and metastasis in colorectal cancer. Biosci Rep 31: 185-197.
24. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, et al. (2007) Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26: 745-752.
25. Mudduluru G, Ceppi P, Kumarswamy R, Scagliotti GV, Papotti M, et al. (2011) Regulation of Axl receptor tyrosine kinase expression by miR-34a and miR-199a/b in solid cancer. Oncogene 30: 2888-2899.
26. Chantret I, Barbat A, Dussaulx E, Brattain MG, Zweibaum A, (1988) Epithelial polarity, villin expression, and enterocytic differentiation of cultured human colon carcinoma cells: a survey of twenty cell lines. Cancer Res 48: 1936-1942.
27. Sagiv E, Starr A, Rozovski U, Khosravi R, Altevogt P, et al. (2008) Targeting CD24 for treatment of colorectal and pancreatic cancer by monoclonal antibodies or small interfering RNA. Cancer Res 68: 2803-2812.
28. Kim NH, Kim HS, Kim NG, Lee I, Choi HS, et al. (2011) p53 and microRNA-34 are suppressors of canonical Wnt signaling. Sci Signal 4: ra71.
29. Yamamura S, Saini S, Majid S, Hirata H, Ueno K, et al. (2012) MicroRNA-34a modulates c-Myc transcriptional complexes to suppress malignancy in human prostate cancer cells. PLoS One 7: e29722.
30. Mudduluru G, Leupold JH, Stroebel P, Allgayer H, (2011) PMA up-regulates the transcription of Axl by AP-1 transcription factor binding to TRE sequences via the MAPK cascade in leukaemia cells. Biol Cell 103: 21-33.
31. Leupold JH, Asangani I, Maurer GD, Lengyel E, Post S, et al. (2007) Src induces urokinase receptor gene expression and invasion/intravasation via activator protein-1/p-c-Jun in colorectal cancer. Mol Cancer Res 5: 485-496.
32. Guarino M, (2010) Src signaling in cancer invasion. J Cell Physiol 223: 14-26.
33. Krichevsky AM, Gabriely G, (2009) miR-21: a small multi-faceted RNA. J Cell Mol Med 13: 39-53.
34. Selcuklu SD, Donoghue MT, Spillane C, (2009) miR-21 as a key regulator of oncogenic processes. Biochem Soc Trans 37: 918-925.
35. Chan JA, Krichevsky AM, Kosik KS, (2005) MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res 65: 6029-6033.
36. Sathyan P, Golden HB, Miranda RC, (2007) Competing interactions between micro-RNAs determine neural progenitor survival and proliferation after ethanol exposure: evidence from an ex vivo model of the fetal cerebral cortical neuroepithelium. J Neurosci 27: 8546-8557.
37. Si ML, Zhu S, Wu H, Lu Z, Wu F, et al. (2007) miR-21-mediated tumor growth. Oncogene 26: 2799-2803.
38. Papagiannakopoulos T, Shapiro A, Kosik KS, (2008) MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res 68: 8164-8172.
39. Schramedei K, Morbt N, Pfeifer G, Lauter J, Rosolowski M, et al. (2011) MicroRNA-21 targets tumor suppressor genes ANP32A and SMARCA4. Oncogene 30: 2975-2985.
40. Yang XR, Xu Y, Yu B, Zhou J, Li JC, et al. (2009) CD24 is a novel predictor for poor prognosis of hepatocellular carcinoma after surgery. Clin Cancer Res 15: 5518-5527.
41. Wilson GR, Cramer A, Welman A, Knox F, Swindell R, et al. (2006) Activated c-SRC in ductal carcinoma in situ correlates with high tumour grade, high proliferation and HER2 positivity. Br J Cancer 95: 1410-1414.
42. Zhang J, Kalyankrishna S, Wislez M, Thilaganathan N, Saigal B, et al. (2007) SRC-family kinases are activated in non-small cell lung cancer and promote the survival of epidermal growth factor receptor-dependent cell lines. Am J Pathol 170: 366-376.
43. Kim LC, Song L, Haura EB, (2009) Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 6: 587-595.
44. Hermeking H, (2010) The miR-34 family in cancer and apoptosis. Cell Death Differ 17: 193-199.
45. de Antonellis P, Medaglia C, Cusanelli E, Andolfo I, Liguori L, et al. (2011) MiR-34a targeting of Notch ligand delta-like 1 impairs CD15+/CD133+ tumor-propagating cells and supports neural differentiation in medulloblastoma. PLoS One 6: e24584.
46. Lee JH, Voortman J, Dingemans AM, Voeller DM, Pham T, et al. (2011) MicroRNA expression and clinical outcome of small cell lung cancer. PLoS One 6: e21300.
47. Pang RT, Leung CO, Ye TM, Liu W, Chiu PC, et al. (2010) MicroRNA-34a suppresses invasion through downregulation of Notch1 and Jagged1 in cervical carcinoma and choriocarcinoma cells. Carcinogenesis 31: 1037-1044.
48. Sun F, Fu H, Liu Q, Tie Y, Zhu J, et al. (2008) Downregulation of CCND1 and CDK6 by miR-34a induces cell cycle arrest. FEBS Lett 582: 1564-1568.
49. Wei JS, Song YK, Durinck S, Chen QR, Cheuk AT, et al. (2008) The MYCN oncogene is a direct target of miR-34a. Oncogene 27: 5204-5213.
50. Chen QR, Yu LR, Tsang P, Wei JS, Song YK, et al. (2011) Systematic proteome analysis identifies transcription factor YY1 as a direct target of miR-34a. J Proteome Res 10: 479-487.
51. Yamakuchi M, Ferlito M, Lowenstein CJ, (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A 105: 13421-13426.
52. Majid S, Saini S, Dar AA, Hirata H, Shahryari V, et al. (2011) MicroRNA-205 inhibits Src-mediated oncogenic pathways in renal cancer. Cancer Res 71: 2611-2621.
53. Saini S, Arora S, Majid S, Shahryari V, Chen Y, et al. (2011) Curcumin modulates microRNA-203-mediated regulation of the Src-Akt axis in bladder cancer. Cancer Prev Res (Phila) 4: 1698-1709.
54. Kong D, Heath E, Chen W, Cher M, Powell I, et al. (2012) Epigenetic silencing of miR-34a in human prostate cancer cells and tumor tissue specimens can be reversed by BR-DIM treatment. Am J Transl Res 4: 14-23.