The proteins DLK1 and DLK2 modulate NOTCH1-dependent proliferation and oncogenic potential of human SK-MEL-2 melanoma cells

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 11, 2014, Pages 2674-2684

  Nueda, María Luisa ^a   Naranjo, Ana Isabel ^b   Baladrón, Victoriano ^b   Laborda, Jorge ^b  

^a Biomedical Research Unit CSIC UCLM   (Spain)

^b Biomedical Research Unit CSIC UCLM   (Spain)

Author keywords

DLK; GSI; Melanoma; NOTCH signaling

Indexed keywords

EID: 84905963021     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.07.015     Document Type: Article

References (58)

1. D'Souza B., Miyamoto A., Weinmaster G. The many facets of Notch ligands. Oncogene 2008, 27:5148-5167.
2. Leong K.G., Karsan A. Recent insights into the role of Notch signaling in tumorigenesis. Blood 2006, 107:2223-2233.
3. Lobry C., Oh P., Aifantis I. Oncogenic and tumor suppressor functions of Notch in cancer: it's NOTCH what you think. J. Exp. Med. 2011, 208:1931-1935.
4. Wang Z., Li Y., Sarkar F.H. Notch signaling proteins: legitimate targets for cancer therapy. Curr. Protein Pept. Sci. 2010, 11:398-408.
5. South A.P., Cho R.J., Aster J.C. The double-edged sword of Notch signaling in cancer. Semin. Cell Dev. Biol. 2012, 23:458-464.
6. Yin L., Velazquez O.C., Liu Z.J. Notch signaling: emerging molecular targets for cancer therapy. Biochem. Pharmacol. 2010, 80:690-701.
7. Mauerer A., Roesch A., Hafner C., Stempfl T., Wild P., Meyer S., Landthaler M., Vogt T. Identification of new genes associated with melanoma. Exp. Dermatol. 2011, 20:502-507.
8. Pinnix C.C., Lee J.T., Liu Z.J., McDaid R., Balint K., Beverly L.J., Brafford P.A., Xiao M., Himes B., Zabierowski S.E., Yashiro-Ohtani Y., Nathanson K.L., Bengston A., Pollock P.M., Weeraratna A.T., Nickoloff B.J., Pear W.S., Capobianco A.J., Herlyn M. Active Notch1 confers a transformed phenotype to primary human melanocytes. Cancer Res. 2009, 69:5312-5320.
9. Balint K., Xiao M., Pinnix C.C., Soma A., Veres I., Juhasz I., Brown E.J., Capobianco A.J., Herlyn M., Liu Z.J. Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J. Clin. Invest. 2005, 115:3166-3176.
10. Liu Z.J., Xiao M., Balint K., Smalley K.S., Brafford P., Qiu R., Pinnix C.C., Li X., Herlyn M. Notch1 signaling promotes primary melanoma progression by activating mitogen-activated protein kinase/phosphatidylinositol 3-kinase-Akt pathways and up-regulating N-cadherin expression. Cancer Res. 2006, 66:4182-4190.
11. Bedogni B., Warneke J.A., Nickoloff B.J., Giaccia A.J., Powell M.B. Notch1 is an effector of Akt and hypoxia in melanoma development. J. Clin. Invest. 2008, 118:3660-3670.
12. Bolos V., Grego-Bessa J., de la Pompa J.L. Notch signaling in development and cancer. Endocr. Rev. 2007, 28:339-363.
13. Groth C., Fortini M.E. Therapeutic approaches to modulating Notch signaling: current challenges and future prospects. Semin. Cell Dev. Biol. 2012, 23:465-472.
14. Mimeault M., Batra S.K. Novel biomarkers and therapeutic targets for optimizing the therapeutic management of melanomas. World J. Clin. Oncol. 2012, 3:32-42.
15. Purow B. Notch inhibition as a promising new approach to cancer therapy. Adv. Exp. Med. Biol. 2012, 727:305-319.
16. Nueda M.L., Baladron V., Sanchez-Solana B., Ballesteros M.A., Laborda J. The EGF-like protein dlk1 inhibits notch signaling and potentiates adipogenesis of mesenchymal cells. J. Mol. Biol. 2007, 367:1281-1293.
17. Bray S.J., Takada S., Harrison E., Shen S.C., Ferguson-Smith A.C. The atypical mammalian ligand Delta-like homologue 1 (Dlk1) can regulate Notch signalling in Drosophila. BMC Dev. Biol. 2008, 8:11.
18. Sanchez-Solana B., Nueda M.L., Ruvira M.D., Ruiz-Hidalgo M.J., Monsalve E.M., Rivero S., Garcia-Ramirez J.J., Diaz-Guerra M.J., Baladron V., Laborda J. The EGF-like proteins DLK1 and DLK2 function as inhibitory non-canonical ligands of NOTCH1 receptor that modulate each other's activities. Biochim. Biophys. Acta 2011, 1813:1153-1164.
19. Mirshekar-Syahkal B., Haak E., Kimber G.M., van Leusden K., Harvey K., O'Rourke J., Laborda J., Bauer S.R., de Bruijn M.F., Ferguson-Smith A.C., Dzierzak E., Ottersbach K. Dlk1 is a negative regulator of emerging hematopoietic stem and progenitor cells. Haematologica 2013, 98:163-171.
20. Kawakami T., Chano T., Minami K., Okabe H., Okada Y., Okamoto K. Imprinted DLK1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma. Hum. Mol. Genet. 2006, 15:821-830.
21. Sul H.S. Minireview: Pref-1: role in adipogenesis and mesenchymal cell fate. Mol. Endocrinol. 2009, 23:1717-1725.
22. Chen L., Qanie D., Jafari A., Taipaleenmaki H., Jensen C.H., Saamanen A.M., Sanz M.L., Laborda J., Abdallah B.M., Kassem M. Delta-like 1/fetal antigen-1 (Dlk1/FA1) is a novel regulator of chondrogenic cell differentiation via inhibition of the Akt kinase-dependent pathway. J. Biol. Chem. 2011, 286:32140-32149.
23. Falix F.A., Aronson D.C., Lamers W.H., Gaemers I.C. Possible roles of DLK1 in the Notch pathway during development and disease. Biochim. Biophys. Acta 2012, 1822:988-995.
24. Samulewicz S.J., Seitz A., Clark L., Heber-Katz E. Expression of preadipocyte factor-1(Pref-1), a delta-like protein, in healing mouse ears. Wound Repair Regen. 2002, 10:215-221.
25. Yin D., Xie D., Sakajiri S., Miller C.W., Zhu H., Popoviciu M.L., Said J.W., Black K.L., Koeffler H.P. DLK1: increased expression in gliomas and associated with oncogenic activities. Oncogene 2006, 25:1852-1861.
26. Yanai H., Nakamura K., Hijioka S., Kamei A., Ikari T., Ishikawa Y., Shinozaki E., Mizunuma N., Hatake K., Miyajima A. Dlk-1, a cell surface antigen on foetal hepatic stem/progenitor cells, is expressed in hepatocellular, colon, pancreas and breast carcinomas at a high frequency. J. Biochem. 2008, 148:85-92.
27. Li L., Forman S.J., Bhatia R. Expression of DLK1 in hematopoietic cells results in inhibition of differentiation and proliferation. Oncogene 2005, 24:4472-4476.
28. Friedrichsen B.N., Carlsson C., Moldrup A., Michelsen B., Jensen C.H., Teisner B., Nielsen J.H. Expression, biosynthesis and release of preadipocyte factor-1/delta-like protein/fetal antigen-1 in pancreatic beta-cells: possible physiological implications. J. Endocrinol. 2003, 176:257-266.
29. Qi X., Chen Z., Liu D., Cen J., Gu M. Expression of Dlk1 gene in myelodysplastic syndrome determined by microarray, and its effects on leukemia cells. Int. J. Mol. Med. 2008, 22:61-68.
30. Yu F., Hao X., Zhao H., Ge C., Yao M., Yang S., Li J. Delta-like 1 contributes to cell growth by increasing the interferon-inducible protein 16 expression in hepatocellular carcinoma. Liver Int. 2010, 30:703-714.
31. Dezso K., Halasz J., Bisgaard H.C., Paku S., Turanyi E., Schaff Z., Nagy P. Delta-like protein (DLK) is a novel immunohistochemical marker for human hepatoblastomas. Virchows Arch. 2008, 452:443-448.
32. Nueda M.L., Baladron V., Garcia-Ramirez J.J., Sanchez-Solana B., Ruvira M.D., Rivero S., Ballesteros M.A., Monsalve E.M., Diaz-Guerra M.J., Ruiz-Hidalgo M.J., Laborda J. The novel gene EGFL9/Dlk2, highly homologous to Dlk1, functions as a modulator of adipogenesis. J. Mol. Biol. 2007, 367:1270-1280.
33. Lee Y.L., Helman L., Hoffman T., Laborda J. dlk, pG2 and Pref-1 mRNAs encode similar proteins belonging to the EGF-like superfamily. Identification of polymorphic variants of this RNA. Biochim. Biophys. Acta 1995, 1261:223-232.
34. Baladron V., Ruiz-Hidalgo M.J., Nueda M.L., Diaz-Guerra M.J., Garcia-Ramirez J.J., Bonvini E., Gubina E., Laborda J. dlk acts as a negative regulator of Notch1 activation through interactions with specific EGF-like repeats. Exp. Cell Res. 2005, 303:343-359.
35. Baladron V., Ruiz-Hidalgo M.J., Bonvini E., Gubina E., Notario V., Laborda J. The EGF-like homeotic protein dlk affects cell growth and interacts with growth-modulating molecules in the yeast two-hybrid system. Biochem. Biophys. Res. Commun. 2002, 291:193-204.
36. Choi H.J., Yee S.B., Park S.E., Im E., Jung J.H., Chung H.Y., Choi Y.H., Kim N.D. Petrotetrayndiol A induces cell cycle arrest and apoptosis in SK-MEL-2 human melanoma cells through cytochrome c-mediated activation of caspases. Cancer Lett. 2006, 232:214-225.
37. Giudice S., Benassi L., Bertazzoni G., Veratti E., Morini D., Azzoni P., Costi M.P., Venturelli A., Pirondi S., Seidenari S., Magnoni C. Biological evaluation of MR36, a novel non-polyglutamatable thymidylate synthase inhibitor that blocks cell cycle progression in melanoma cell lines. Investig. New Drugs 2012, 30:1484-1492.
38. Sakajiri S., O'Kelly J., Yin D., Miller C.W., Hofmann W.K., Oshimi K., Shih L.Y., Kim K.H., Sul H.S., Jensen C.H., Teisner B., Kawamata N., Koeffler H.P. Dlk1 in normal and abnormal hematopoiesis. Leukemia 2005, 19:1404-1410.
39. Dong Y.B., Yang H.L., Elliott M.J., McMasters K.M. Adenovirus-mediated E2F-1 gene transfer sensitizes melanoma cells to apoptosis induced by topoisomerase II inhibitors. Cancer Res. 2002, 62:1776-1783.
40. Huang J., Zhang X., Zhang M., Zhu J.D., Zhang Y.L., Lin Y., Wang K.S., Qi X.F., Zhang Q., Liu G.Z., Yu J., Cui Y., Yang P.Y., Wang Z.Q., Han Z.G. Up-regulation of DLK1 as an imprinted gene could contribute to human hepatocellular carcinoma. Carcinogenesis 2007, 28:1094-1103.
41. Kim Y., Lin Q., Zelterman D., Yun Z. Hypoxia-regulated delta-like 1 homologue enhances cancer cell stemness and tumorigenicity. Cancer Res. 2009, 69:9271-9280.
42. Orr B., Grace O.C., Brown P., Riddick A.C., Stewart G.D., Franco O.E., Hayward S.W., Thomson A.A. Reduction of pro-tumorigenic activity of human prostate cancer-associated fibroblasts using Dlk1 or SCUBE1. Dis. Models Mech. 2013, 6:530-536.
43. Hoek K., Rimm D.L., Williams K.R., Zhao H., Ariyan S., Lin A., Kluger H.M., Berger A.J., Cheng E., Trombetta E.S., Wu T., Niinobe M., Yoshikawa K., Hannigan G.E., Halaban R. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res. 2004, 64:5270-5282.
44. Mazzone M., Selfors L.M., Albeck J., Overholtzer M., Sale S., Carroll D.L., Pandya D., Lu Y., Mills G.B., Aster J.C., Artavanis-Tsakonas S., Brugge J.S. Dose-dependent induction of distinct phenotypic responses to Notch pathway activation in mammary epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:5012-5017.
45. Kim Y. The effects of nutrient depleted microenvironments and delta-like 1 homologue (DLK1) on apoptosis in neuroblastoma. Nutr. Res. Pract. 2011, 4:455-461.
46. Jang M.S., Miao H., Carlesso N., Shelly L., Zlobin A., Darack N., Qin J.Z., Nickoloff B.J., Miele L. Notch-1 regulates cell death independently of differentiation in murine erythroleukemia cells through multiple apoptosis and cell cycle pathways. J. Cell. Physiol. 2004, 199:418-433.
47. Qi R., An H., Yu Y., Zhang M., Liu S., Xu H., Guo Z., Cheng T., Cao X. Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis. Cancer Res. 2003, 63:8323-8329.
48. Guo D., Ye J., Dai J., Li L., Chen F., Ma D., Ji C. Notch-1 regulates Akt signaling pathway and the expression of cell cycle regulatory proteins cyclin D1, CDK2 and p21 in T-ALL cell lines. Leuk. Res. 2009, 33:678-685.
49. Miyamoto S., Nakanishi M., Rosenberg D.W. Suppression of colon carcinogenesis by targeting Notch signaling. Carcinogenesis 2013, 34:2415-2423.
50. Wang Z., Zhang Y., Li Y., Banerjee S., Liao J., Sarkar F.H. Down-regulation of Notch-1 contributes to cell growth inhibition and apoptosis in pancreatic cancer cells. Mol. Cancer Ther. 2006, 5:483-493.
51. Sun Q., Wang R., Wang Y., Luo J., Wang P., Cheng B. Notch1 is a potential therapeutic target for the treatment of human hepatitis B virus X protein-associated hepatocellular carcinoma. Oncol. Rep. 2014, 31:933-939.
52. Zhang S., Yang Y., Liang Z., Duan W., Yang J., Yan J., Wang N., Feng W., Ding M., Nie Y., Jin Z. Silybin-mediated inhibition of Notch signaling exerts antitumor activity in human hepatocellular carcinoma cells. PLoS ONE 2013, 8:e83699.
53. Takebe N., Nguyen D., Yang S.X. Targeting Notch signaling pathway in cancer: clinical development advances challenges. Pharmacol. Ther. 2014, 141:140-149.
54. Gordon W.R., Arnett K.L., Blacklow S.C. The molecular logic of Notch signaling - a structural and biochemical perspective. J. Cell Sci. 2008, 121:3109-3119.
55. Han J., Ma I., Hendzel M.J., Allalunis-Turner J. The cytotoxicity of gamma-secretase inhibitor I to breast cancer cells is mediated by proteasome inhibition, not by gamma-secretase inhibition. Breast Cancer Res. 2009, 11:R57.
56. Dikic I., Schmidt M.H. Notch: implications of endogenous inhibitors for therapy. Bioessays 2010, 32:481-487.
57. Krop I., Demuth T., Guthrie T., Wen P.Y., Mason W.P., Chinnaiyan P., Butowski N., Groves M.D., Kesari S., Freedman S.J., Blackman S., Watters J., Loboda A., Podtelezhnikov A., Lunceford J., Chen C., Giannotti M., Hing J., Beckman R., Lorusso P. Phase I pharmacologic and pharmacodynamic study of the gamma secretase (Notch) inhibitor MK-0752 in adult patients with advanced solid tumors. J. Clin. Oncol. 2012, 30:2307-2313.
58. Wang Z., Li Y., Ahmad A., Azmi A.S., Banerjee S., Kong D., Sarkar F.H. Targeting Notch signaling pathway to overcome drug resistance for cancer therapy. Biochim. Biophys. Acta 2010, 1806:258-267.