RUNX2 is overexpressed in melanoma cells and mediates their migration and invasion

Cancer Letters

Volumn 348, Issue 1-2, 2014, Pages 61-70

  Boregowda, Rajeev K ^a   Olabisi, Oyenike O ^a   Abushahba, Walid ^a   Jeong, Byeong Seon ^a   Haenssen, Keneshia K ^a   Chen, Wenjin ^b   Chekmareva, Marina ^c   Lasfar, Ahmed ^d   Foran, David J ^b   Goydos, James S ^a   Cohen Solal, Karine A ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

^c ROBERT WOOD JOHNSON UNIVERSITY HOSPITAL   (United States)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

Cholecalciferol (Vitamin D3); FAK; Melanoma; Migration; RUNX2; Transcription factor

Indexed keywords

COLECALCIFEROL; FOCAL ADHESION KINASE; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; CANCER GROWTH; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; MELANOCYTE; MELANOMA CELL; NEVUS CELL; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TISSUE MICROARRAY; TISSUE SECTION;

CHOLECALCIFEROL (VITAMIN D3); FAK; MELANOMA; MIGRATION; RUNX2; TRANSCRIPTION FACTOR;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CHOLECALCIFEROL; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; MATRIX METALLOPROTEINASE 13; MELANOMA; NEOPLASM INVASIVENESS; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TISSUE ARRAY ANALYSIS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

EID: 84900470421     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.03.011     Document Type: Article

References (55)

1. Hersey P., Gallagher S. A focus on PD-L1 in human melanoma. Clin. Cancer Res. 2013.
2. Lyseng-Williamson K.A., Sanford M. Ipilimumab: a guide to its use in advanced melanoma. Am. J. Clin. Dermatol. 2012, 13:349-354.
3. Chapman P.B., Hauschild A., Robert C., Haanen J.B., Ascierto P., Larkin J., Dummer R., Garbe C., Testori A., Maio M., Hogg D., Lorigan P., Lebbe C., Jouary T., Schadendorf D., Ribas A., O'Day S.J., Sosman J.A., Kirkwood J.M., Eggermont A.M., Dreno B., Nolop K., Li J., Nelson B., Hou J., Lee R.J., Flaherty K.T., McArthur G.A. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N. Engl. J. Med. 2011, 364:2507-2516.
4. Boyle G.M. Therapy for metastatic melanoma: an overview and update. Exp. Rev. Anticancer Ther. 2011, 11:725-737.
5. Siegel R., DeSantis C., Virgo K., Stein K., Mariotto A., Smith T., Cooper D., Gansler T., Lerro C., Fedewa S., Lin C., Leach C., Cannady R.S., Cho H., Scoppa S., Hachey M., Kirch R., Jemal A., Ward E. Cancer treatment and survivorship statistics. CA Cancer J. Clin. 2012, 62:220-241.
6. Ghosh D., Papavassiliou A.G. Transcription factor therapeutics: long-shot or lodestone. Curr. Med. Chem. 2005, 12:691-701.
7. Yan C., Higgins P.J. Drugging the undruggable: Transcription therapy for cancer. Biochim. Biophys. Acta. 1835, 2013:76-85.
8. Tsao H., Chin L., Garraway L.A., Fisher D.E. Melanoma: from mutations to medicine. Genes Dev. 2012, 26:1131-1155.
9. Blyth K., Vaillant F., Jenkins A., McDonald L., Pringle M.A., Huser C., Stein T., Neil J., Cameron E.R. Runx2 in normal tissues and cancer cells: a developing story. Blood Cells Mol. Dis. 2010, 45:117-123.
10. Komori T., Yagi H., Nomura S., Yamaguchi A., Sasaki K., Deguchi K., Shimizu Y., Bronson R.T., Gao Y.H., Inada M., Sato M., Okamoto R., Kitamura Y., Yoshiki S., Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 1997, 89:755-764.
11. Otto F., Thornell A.P., Crompton T., Denzel A., Gilmour K.C., Rosewell I.R., Stamp G.W., Beddington R.S., Mundlos S., Olsen B.R., Selby P.B., Owen M.J. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 1997, 89:765-771.
12. Blyth K., Cameron E.R., Neil J.C. The RUNX genes: gain or loss of function in cancer. Nat. Rev. Cancer 2005, 5:376-387.
13. Chua C.W., Chiu Y.T., Yuen H.F., Chan K.W., Man K., Wang X., Ling M.T., Wong Y.C. Suppression of androgen-independent prostate cancer cell aggressiveness by FTY720: validating Runx2 as a potential antimetastatic drug screening platform. Clin. Cancer Res. 2009, 15:4322-4335.
14. van der Deen M., Akech J., Lapointe D., Gupta S., Young D.W., Montecino M.A., Galindo M., Lian J.B., Stein J.L., Stein G.S., van Wijnen A.J. Genomic promoter occupancy of runt-related transcription factor RUNX2 in Osteosarcoma cells identifies genes involved in cell adhesion and motility. J. Biol. Chem. 2012, 287:4503-4517.
15. Sun L., Vitolo M., Passaniti A. Runt-related gene 2 in endothelial cells: inducible expression and specific regulation of cell migration and invasion. Cancer Res. 2001, 61:4994-5001.
16. Pierce A.D., Anglin I.E., Vitolo M.I., Mochin M.T., Underwood K.F., Goldblum S.E., Kommineni S., Passaniti A. Glucose-activated RUNX2 phosphorylation promotes endothelial cell proliferation and an angiogenic phenotype. J. Cell. Biochem. 2012, 113:282-292.
17. Kwon T.G., Zhao X., Yang Q., Li Y., Ge C., Zhao G., Franceschi R.T. Physical and functional interactions between Runx2 and HIF-1alpha induce vascular endothelial growth factor gene expression. J. Cell. Biochem. 2011, 112:3582-3593.
18. Lee S.H., Che X., Jeong J.H., Choi J.Y., Lee Y.J., Lee Y.H., Bae S.C., Lee Y.M. Runx2 protein stabilizes hypoxia-inducible factor-1alpha through competition with von Hippel-Lindau Protein (pVHL) and stimulates angiogenesis in growth plate hypertrophic chondrocytes. J. Biol. Chem. 2012, 287:14760-14771.
19. Riminucci M., Corsi A., Peris K., Fisher L.W., Chimenti S., Bianco P. Coexpression of bone sialoprotein (BSP) and the pivotal transcriptional regulator of osteogenesis, Cbfa1/Runx2, in malignant melanoma. Calcif. Tissue Int. 2003, 73:281-289.
20. Lasfar A., Cohen-Solal K.A. Resistance to transforming growth factor beta-mediated tumor suppression in melanoma: are multiple mechanisms in place?. Carcinogenesis 2010, 31:1710-1717.
21. Mohammad K.S., Javelaud D., Fournier P.G., Niewolna M., McKenna C.R., Peng X.H., Duong V., Dunn L.K., Mauviel A., Guise T.A. TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res. 2011, 71:175-184.
22. Packer L.M., Pavey S.J., Boyle G.M., Stark M.S., Ayub A.L., Rizos H., Hayward N.K. Gene expression profiling in melanoma identifies novel downstream effectors of p14ARF. Int. J. Cancer 2007, 121:784-790.
23. Underwood K.F., D'Souza D.R., Mochin-Peters M., Pierce A.D., Kommineni S., Choe M., Bennett J., Gnatt A., Habtemariam B., MacKerell A.D., Passaniti A. Regulation of RUNX2 transcription factor-DNA interactions and cell proliferation by vitamin D3 (cholecalciferol) prohormone activity. J. Bone Miner. Res. 2012, 27:913-925.
24. Satyamoorthy K., Li G., Gerrero M.R., Brose M.S., Volpe P., Weber B.L., Van Belle P., Elder D.E., Herlyn M. Constitutive mitogen-activated protein kinase activation in melanoma is mediated by both BRAF mutations and autocrine growth factor stimulation. Cancer Res. 2003, 63:756-759.
25. Welch D.R., Bisi J.E., Miller B.E., Conaway D., Seftor E.A., Yohem K.H., Gilmore L.B., Seftor R.E., Nakajima M., Hendrix M.J. Characterization of a highly invasive and spontaneously metastatic human malignant melanoma cell line. Int. J. Cancer 1991, 47:227-237.
26. Bittner M., Meltzer P., Chen Y., Jiang Y., Seftor E., Hendrix M., Radmacher M., Simon R., Yakhini Z., Ben-Dor A., Sampas N., Dougherty E., Wang E., Marincola F., Gooden C., Lueders J., Glatfelter A., Pollock P., Carpten J., Gillanders E., Leja D., Dietrich K., Beaudry C., Berens M., Alberts D., Sondak V. Molecular classification of cutaneous malignant melanoma by gene expression profiling. Nature 2000, 406:536-540.
27. Le M.N., Chan J.L., Rosenberg S.A., Nabatian A.S., Merrigan K.T., Cohen-Solal K.A., Goydos J.S. The glutamate release inhibitor Riluzole decreases migration, invasion, and proliferation of melanoma cells. J. Invest. Dermatol. 2010, 130:2240-2249.
28. Garraway L.A., Widlund H.R., Rubin M.A., Getz G., Berger A.J., Ramaswamy S., Beroukhim R., Milner D.A., Granter S.R., Du J., Lee C., Wagner S.N., Li C., Golub T.R., Rimm D.L., Meyerson M.L., Fisher D.E., Sellers W.R. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005, 436:117-122.
29. Abushahba W., Olabisi O.O., Jeong B.S., Boregowda R.K., Wen Y., Liu F., Goydos J.S., Lasfar A., Cohen-Solal K.A. Non-canonical smads phosphorylation induced by the glutamate release inhibitor, riluzole, through GSK3 activation in melanoma. PLoS One 2012, 7:e47312.
30. Chen W., Reiss M., Foran D.J. A prototype for unsupervised analysis of tissue microarrays for cancer research and diagnostics. IEEE Trans. Inf. Technol. Biomed. 2004, 8:89-96.
31. Lee M., Partridge N.C. Parathyroid hormone activation of matrix metalloproteinase-13 transcription requires the histone acetyltransferase activity of p300 and PCAF and p300-dependent acetylation of PCAF. J. Biol. Chem. 2010, 285:38014-38022.
32. Selvamurugan N., Jefcoat S.C., Kwok S., Kowalewski R., Tamasi J.A., Partridge N.C. Overexpression of Runx2 directed by the matrix metalloproteinase-13 promoter containing the AP-1 and Runx/RD/Cbfa sites alters bone remodeling in vivo. J. Cell. Biochem. 2006, 99:545-557.
33. Fujita T., Azuma Y., Fukuyama R., Hattori Y., Yoshida C., Koida M., Ogita K., Komori T. Runx2 induces osteoblast and chondrocyte differentiation and enhances their migration by coupling with PI3K-Akt signaling. J. Cell. Biol. 2004, 166:85-95.
34. Chimge N.O., Frenkel B. The RUNX family in breast cancer: relationships with estrogen signaling. Oncogene 2013, 32:2121-2130.
35. Li S., Hua Z.C. FAK expression regulation and therapeutic potential. Adv. Cancer Res. 2008, 101:45-61.
36. Pockwinse S.M., Rajgopal A., Young D.W., Mujeeb K.A., Nickerson J., Javed A., Redick S., Lian J.B., van Wijnen A.J., Stein J.L., Stein G.S., Doxsey S.J. Microtubule-dependent nuclear-cytoplasmic shuttling of Runx2. J. Cell. Physiol. 2006, 206:354-362.
37. Bonner M.K., Poole D.S., Xu T., Sarkeshik A., Yates J.R., Skop A.R. Mitotic spindle proteomics in Chinese hamster ovary cells. PLoS One 2011, 6:e20489.
38. Chuang L.S., Lai S.K., Murata-Hori M., Yamada A., Li H.Y., Gunaratne J., Ito Y. RUNX3 interactome reveals novel centrosomal targeting of RUNX family of transcription factors. Cell Cycle 2012, 11:1938-1947.
39. Kim S., Koga T., Isobe M., Kern B.E., Yokochi T., Chin Y.E., Karsenty G., Taniguchi T., Takayanagi H. Stat1 functions as a cytoplasmic attenuator of Runx2 in the transcriptional program of osteoblast differentiation. Genes Dev. 2003, 17:1979-1991.
40. Deepak V., Zhang Z., Meng L., Zeng X., Liu W. Reduced activity and cytoplasmic localization of Runx2 is observed in C3h10t1/2 cells overexpressing Tbx3. Cell. Biochem. Funct. 2011, 29:348-350.
41. Kuilman T., Michaloglou C., Mooi W.J., Peeper D.S. The essence of senescence. Genes Dev. 2010, 24:2463-2479.
42. Pollock P.M., Harper U.L., Hansen K.S., Yudt L.M., Stark M., Robbins C.M., Moses T.Y., Hostetter G., Wagner U., Kakareka J., Salem G., Pohida T., Heenan P., Duray P., Kallioniemi O., Hayward N.K., Trent J.M., Meltzer P.S. High frequency of BRAF mutations in nevi. Nat. Genet. 2003, 33:19-20.
43. Dankort D., Curley D.P., Cartlidge R.A., Nelson B., Karnezis A.N., Damsky W.E., You M.J., DePinho R.A., McMahon M., Bosenberg M. Braf(V600E) cooperates with Pten loss to induce metastatic melanoma. Nat. Genet. 2009, 41:544-552.
44. Dhomen N., Reis-Filho J.S., da Rocha Dias S., Hayward R., Savage K., Delmas V., Larue L., Pritchard C., Marais R. Oncogenic Braf induces melanocyte senescence and melanoma in mice. Cancer Cell 2009, 15:294-303.
45. Michaloglou C., Vredeveld L.C., Soengas M.S., Denoyelle C., Kuilman T., van der Horst C.M., Majoor D.M., Shay J.W., Mooi W.J., Peeper D.S. BRAFE600-associated senescence-like cell cycle arrest of human naevi. Nature 2005, 436:720-724.
46. Chuang L.S., Ito K., Ito Y. RUNX family: Regulation and diversification of roles through interacting proteins. Int. J. Cancer 2013, 132:1260-1271.
47. Zaidi S.K., Pande S., Pratap J., Gaur T., Grigoriu S., Ali S.A., Stein J.L., Lian J.B., van Wijnen A.J., Stein G.S. Runx2 deficiency and defective subnuclear targeting bypass senescence to promote immortalization and tumorigenic potential. Proc. Natl. Acad. Sci. USA 2007, 104:19861-19866.
48. Akech J., Wixted J.J., Bedard K., van der Deen M., Hussain S., Guise T.A., van Wijnen A.J., Stein J.L., Languino L.R., Altieri D.C., Pratap J., Keller E., Stein G.S., Lian J.B. Runx2 association with progression of prostate cancer in patients: mechanisms mediating bone osteolysis and osteoblastic metastatic lesions. Oncogene 2010, 29:811-821.
49. Baniwal S.K., Khalid O., Gabet Y., Shah R.R., Purcell D.J., Mav D., Kohn-Gabet A.E., Shi Y., Coetzee G.A., Frenkel B. Runx2 transcriptome of prostate cancer cells: insights into invasiveness and bone metastasis. Mol. Cancer 2010, 9:258.
50. Sheng S., Qiao M., Pardee A.B. Metastasis and AKT activation. J. Cell. Physiol. 2009, 218:451-454.
51. Lake S.L., Jmor F., Dopierala J., Taktak A.F., Coupland S.E., Damato B.E. Multiplex ligation-dependent probe amplification of conjunctival melanoma reveals common BRAF V600E gene mutation and gene copy number changes. Invest. Ophthalmol. Vis. Sci. 2011, 52:5598-5604.
52. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat. Rev. Mol. Cell. Biol. 2005, 6:56-68.
53. Boukerche H., Su Z.Z., Emdad L., Baril P., Balme B., Thomas L., Randolph A., Valerie K., Sarkar D., Fisher P.B. Mda-9/Syntenin: a positive regulator of melanoma metastasis. Cancer Res. 2005, 65:10901-10911.
54. Das S.K., Bhutia S.K., Kegelman T.P., Peachy L., Oyesanya R.A., Dasgupta S., Sokhi U.K., Azab B., Dash R., Quinn B.A., Kim K., Barral P.M., Su Z.Z., Boukerche H., Sarkar D., Fisher P.B. MDA-9/syntenin: a positive gatekeeper of melanoma metastasis. Front. Biosci. 2012, 17:1-15.
55. Kaneda T., Sonoda Y., Ando K., Suzuki T., Sasaki Y., Oshio T., Tago M., Kasahara T. Mutation of Y925F in focal adhesion kinase (FAK) suppresses melanoma cell proliferation and metastasis. Cancer Lett. 2008, 270:354-361.