Acid sphingomyelinase determines melanoma progression and metastatic behaviour via the microphtalmia-associated transcription factor signalling pathway

Cell Death and Differentiation

Volumn 21, Issue 4, 2014, Pages 507-520

  Bizzozero, L ^a   Cazzato, D ^a,b   Cervia, D ^b,c   Assi, E ^b   Simbari, F ^d   Pagni, F ^e   De Palma, C ^b   Monno, A ^f   Verdelli, C ^b   Querini, P R ^f   Russo, V ^f   Clementi, E ^a,b   Perrotta, C ^b  

^a SCIENTIFIC INSTITUTE   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF TUSCIA   (Italy)

^d INSTITUTE OF ADVANCED CHEMISTRY OF CATALONIA IQAC CSIC   (Spain)

^e UNIVERSITY OF MILANO BICOCCA   (Italy)

^f SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

acid sphingomyelinase; melanoma; microphtalmia associated transcription factor; signalling mechanisms

Indexed keywords

CYCLIN DEPENDENT KINASE 2; MICROPHTALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL 2; SPHINGOLIPID; SPHINGOMYELIN PHOSPHODIESTERASE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER STAGING; CANCER SURVIVAL; CELL FUNCTION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MELANOMA CELL; METASTASIS; METASTATIC MELANOMA; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SKIN PIGMENTATION; TUMOR BIOPSY; TUMOR GROWTH; TUMOR INVASION;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE 2; DISEASE PROGRESSION; DOWN-REGULATION; FEMALE; HUMANS; LUNG NEOPLASMS; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; PIGMENTATION; PROTO-ONCOGENE PROTEINS C-BCL-2; PROTO-ONCOGENE PROTEINS C-MET; SIGNAL TRANSDUCTION; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84903372715     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.173     Document Type: Article

References (60)

1. Nikolaou VA, Stratigos AJ, Flaherty KT, Tsao H. Melanoma: new insights and new therapies. J Invest Dermatol 2012; 132(3 Pt 2): 854-863.
2. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med 2010; 363: 711-723.
3. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011; 364: 2507-2516.
4. Hendrix MJ, Seftor EA, Hess AR, Seftor RE. Molecular plasticity of human melanoma cells. Oncogene 2003; 22: 3070-3075.
5. Marusyk A, Polyak K. Tumor heterogeneity: causes and consequences. Biochim Biophys Acta 2010; 1805: 105-117.
6. Balch CM, Gershenwald JE, Soong SJ, Thompson JF. Update on the melanoma staging system: the importance of sentinel node staging and primary tumor mitotic rate. J Surg Oncol 2011; 104: 379-385.
7. Tremante E, Ginebri A, Lo Monaco E, Frascione P, Di Filippo F, Terrenato I et al. Melanoma molecular classes and prognosis in the postgenomic era. Lancet Oncol 2012; 13: e205-e211.
8. Barsacchi R, Perrotta C, Sestili P, Cantoni O, Moncada S, Clementi E. Cyclic GMP-dependent inhibition of acid sphingomyelinase by nitric oxide: an early step in protection against apoptosis. Cell Death Differ 2002; 9: 1248-1255.
9. Perrotta C, Bizzozero L, Cazzato D, Morlacchi S, Assi E, Simbari F et al. Syntaxin 4 is required for acid sphingomyelinase activity and apoptotic function. J Biol Chem 2010; 285: 40240-40251.
10. Bauer J, Huy C, Brenmoehl J, Obermeier F, Bock J. Matrix metalloproteinase-1 expression induced by IL-1beta requires acid sphingomyelinase. FEBS Lett 2009; 583: 915-920.
11. Edelmann B, Bertsch U, Tchikov V, Winoto-Morbach S, Perrotta C, Jakob M et al. Caspase-8 and caspase-7 sequentially mediate proteolytic activation of acid sphingomyelinase in TNF-R1 receptosomes. EMBO J 2011; 30: 379-394.
12. Perrotta C, Clementi E. Biological roles of Acid and neutral sphingomyelinases and their regulation by nitric oxide. Physiology (Bethesda) 2010; 25: 64-71.
13. Smith EL, Schuchman EH. The unexpected role of acid sphingomyelinase in cell death and the pathophysiology of common diseases. FASEB J 2008; 22: 3419-3431.
14. Langmann T, Buechler C, Ries S, Schaeffler A, Aslanidis C, Schuierer M et al. Transcription factors Sp1 and AP-2 mediate induction of acid sphingomyelinase during monocytic differentiation. J Lipid Res 1999; 40: 870-880.
15. Sakata A, Ochiai T, Shimeno H, Hikishima S, Yokomatsu T, Shibuya S et al. Acid sphingomyelinase inhibition suppresses lipopolysaccharide-mediated release of inflammatory cytokines from macrophages and protects against disease pathology in dextran sulphate sodium-induced colitis in mice. Immunology 2007; 122: 54-64.
16. Perrotta C, Bizzozero L, Falcone S, Rovere-Querini P, Prinetti A, Schuchman EH et al. Nitric oxide boosts chemoimmunotherapy via inhibition of acid sphingomyelinase in a mouse model of melanoma. Cancer Res 2007; 67: 7559-7564.
17. Cronin JC, Wunderlich J, Loftus SK, Prickett TD, Wei X, Ridd K et al. Frequent mutations in the MITF pathway in melanoma. Pigment Cell Melanoma Res 2009; 22: 435-444.
18. Bertolotto C, Lesueur F, Giuliano S, Strub T, de Lichy M, Bille K et al. A SUMOylationdefective MITF germline mutation predisposes to melanoma and renal carcinoma. Nature 2011; 480: 94-98.
19. Yokoyama S, Woods SL, Boyle GM, Aoude LG, MacGregor S, Zismann V et al. A novel recurrent mutation in MITF predisposes to familial and sporadic melanoma. Nature 2011; 480: 99-103.
20. Konsti J, Lundin M, Joensuu H, Lehtimaki T, Sihto H, Holli K et al. Development and evaluation of a virtual microscopy application for automated assessment of Ki-67 expression in breast cancer. BMC Clin Pathol 2011; 11: 3.
21. Kashani-Sabet M, Rangel J, Torabian S, Nosrati M, Simko J, Jablons DM et al. A multi-marker assay to distinguish malignant melanomas from benign nevi. Proc Natl Acad Sci USA 2009; 106: 6268-6272.
22. Nakamura K, Yoshikawa N, Yamaguchi Y, Kagota S, Shinozuka K, Kunitomo M. Characterization of mouse melanoma cell lines by their mortal malignancy using an experimental metastatic model. Life Sci 2002; 70: 791-798.
23. Villablanca EJ, Raccosta L, Zhou D, Fontana R, Maggioni D, Negro A et al. Tumor-mediated liver X receptor-alpha activation inhibits CC chemokine receptor-7 expression on dendritic cells and dampens antitumor responses. Nat Med 2010; 16: 98-105.
24. Kim DS, Kim SY, Chung JH, Kim KH, Eun HC, Park KC. Delayed ERK activation by ceramide reduces melanin synthesis in human melanocytes. Cell Signal 2002; 14: 779-785.
25. Cruz J, Reis-Filho JS, Silva P, Lopes JM. Expression of c-met tyrosine kinase receptor is biologically and prognostically relevant for primary cutaneous malignant melanomas. Oncology 2003; 65: 72-82.
26. McGill GG, Haq R, Nishimura EK, Fisher DE. c-Met expression is regulated by Mitf in the melanocyte lineage. J Biol Chem 2006; 281: 10365-10373.
27. Nakai N, Kishida T, Shin-Ya M, Imanishi J, Ueda Y, Kishimoto S et al. Therapeutic RNA interference of malignant melanoma by electrotransfer of small interfering RNA targeting Mitf. Gene Ther 2007; 14: 357-365.
28. Cheli Y, Giuliano S, Fenouille N, Allegra M, Hofman V, Hofman P et al. Hypoxia and MITF control metastatic behaviour in mouse and human melanoma cells. Oncogene 2012; 31: 2461-2470.
29. Halaban R. Pigmentation in melanomas: changes manifesting underlying oncogenic and metabolic activities. Oncol Res 2002; 13: 3-8.
30. Adler MJ,White CR Jr. Amelanotic malignant melanoma. Semin Cutan Med Surg 1997; 16: 122-130.
31. Jimbow K, Lee SK, King MG, Hara H, Chen H, Dakour J et al. Melanin pigments and melanosomal proteins as differentiation markers unique to normal and neoplastic melanocytes. J Invest Dermatol 1993; 100: 259S-268S.
32. Bennett DC, Dexter TJ, Ormerod EJ, Hart IR. Increased experimental metastatic capacity of a murine melanoma following induction of differentiation. Cancer Res 1986; 46: 3239-3244.
33. Kameyama K, Vieira WD, Tsukamoto K, Law LW, Hearing VJ. Differentiation and the tumorigenic and metastatic phenotype of murine melanoma cells. Int J Cancer 1990; 45: 1151-1158.
34. Gupta PB, Kuperwasser C, Brunet JP, Ramaswamy S, Kuo WL, Gray JW et al. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet 2005; 37: 1047-1054.
35. Kim SH, Choe C, Shin YS, Jeon MJ, Choi SJ, Lee J et al. Human lung cancer-associated fibroblasts enhance motility of non-small cell lung cancer cells in co-culture. Anticancer Res 2013; 33: 2001-2009.
36. Aggarwal R, Lu J, Kanji S, Das M, Joseph M, Lustberg MB et al. Human Vgamma2Vdelta2 T cells limit breast cancer growth by modulating cell survival-, apoptosis-related molecules and microenvironment in tumors. Int J Cancer 2013; 133: 2133-2144.
37. Cheng YJ, Lee CH, Lin YP, Huang JY, Su CC, Chang WT et al. Caspase-3 enhances lung metastasis and cell migration in a protease-independent mechanism through the ERK pathway. Int J Cancer 2008; 123: 1278-1285.
38. Jenkins RW, Clarke CJ, Canals D, Snider AJ, Gault CR, Heffernan-Stroud L et al. Regulation of CC ligand 5/RANTES by acid sphingomyelinase and acid ceramidase. J Biol Chem 2011; 286: 13292-13303.
39. Rozenova KA, Deevska GM, Karakashian AA, Nikolova-Karakashian MN. Studies on the role of acid sphingomyelinase and ceramide in the regulation of tumor necrosis factor alpha (TNFalpha)-converting enzyme activity and TNFalpha secretion in macrophages. J Biol Chem 2010; 285: 21103-21113.
40. Garraway LA, Widlund HR, Rubin MA, Getz G, Berger AJ, Ramaswamy S et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005; 436: 117-122.
41. Damsky WE, Curley DP, Santhanakrishnan M, Rosenbaum LE, Platt JT, Rothberg BEG et al. beta-catenin signaling controls metastasis in Braf-activated Pten-deficient melanomas. Cancer Cell 2011; 20: 741-754.
42. Yajima I, Kumasaka MY, Thang ND, Goto Y, Takeda K, Iida M et al. Molecular network associated with MITF in skin melanoma development and progression. J Skin Cancer 2011; 2011: 730170.
43. Carreira S, Goodall J, Aksan I, La Rocca SA, Galibert MD, Denat L et al. Mitf cooperates with Rb1 and activates p21Cip1 expression to regulate cell cycle progression. Nature 2005; 433: 764-769.
44. Luo C, Merz PR, Chen Y, Dickes E, Pscherer A, Schadendorf D et al. MiR-101 inhibits melanoma cell invasion and proliferation by targeting MITF and EZH2. Cancer Lett 2013; 341: 240-247.
45. Borgdorff V, Rix U, Winter GE, Gridling M, Muller AC, Breitwieser FP et al. A chemical biology approach identifies AMPK as a modulator of melanoma oncogene MITF. Oncogene 2013; e-pub ahead of print 3 June 2013; doi:10.1038/onc.2013.185.
46. Vazquez F, Lim JH, Chim H, Bhalla K, Girnun G, Pierce K et al. PGC1alpha expression defines a subset of human melanoma tumors with increased mitochondrial capacity and resistance to oxidative stress. Cancer Cell 2013; 23: 287-301.
47. Yan D, Dong XD, Chen X, Yao S, Wang L, Wang J et al. Role of microRNA-182 in posterior uveal melanoma: regulation of tumor development through MITF, BCL2 and cyclin D2. PLoS One 2012; 7: e40967.
48. Feige E, Yokoyama S, Levy C, Khaled M, Igras V, Lin RJ et al. Hypoxia-induced transcriptional repression of the melanoma-associated oncogene MITF. Proc Natl Acad Sci USA 2011; 108: E924-E933.
49. Carreira S, Goodall J, Denat L, Rodriguez M, Nuciforo P, Hoek KS et al. Mitf regulation of Dia1 controls melanoma proliferation and invasiveness. Genes Dev 2006; 20: 3426-3439.
50. Du J, Widlund HR, Horstmann MA, Ramaswamy S, Ross K, Huber WE et al. Critical role of CDK2 for melanoma growth linked to its melanocyte-specific transcriptional regulation by MITF. Cancer Cell 2004; 6: 565-576.
51. Hertzman Johansson C, Azimi A, Frostvik Stolt M, Shojaee S, Wiberg H, Grafstrom E et al. Association of MITF and other melanosome-related proteins with chemoresistance in melanoma tumors and cell lines. Melanoma Res 2013; e-pub ahead of print 5 August 2013; doi:10.1097/CMR.0b013e328362f9cd.
52. Cheli Y, Giuliano S, Botton T, Rocchi S, Hofman V, Hofman P et al. Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny. Oncogene 2011; 30: 2307-2318.
53. Kenessey I, Keszthelyi M, Kramer Z, Berta J, Adam A, Dobos J et al. Inhibition of c-Met with the specific small molecule tyrosine kinase inhibitor SU11274 decreases growth and metastasis formation of experimental human melanoma. Curr Cancer Drug Targets 2010; 10: 332-342.
54. Bedikian AY, Millward M, Pehamberger H, Conry R, Gore M, Trefzer U et al. Bcl-2 antisense (oblimersen sodium) plus dacarbazine in patients with advanced melanoma: the Oblimersen Melanoma Study Group. J Clin Oncol 2006; 24: 4738-4745.
55. Jiang Y, DiVittore NA, Kaiser JM, Shanmugavelandy SS, Fritz JL, Heakal Y et al. Combinatorial therapies improve the therapeutic efficacy of nanoliposomal ceramide for pancreatic cancer. Cancer Biol Ther 2011; 12: 574-585.
56. Morad SA, Cabot MC. Ceramide-orchestrated signalling in cancer cells. Nat Rev Cancer 2013; 13: 51-65.
57. Passini MA, Bu J, Fidler JA, Ziegler RJ, Foley JW, Dodge JC et al. Combination brain and systemic injections of AAV provide maximal functional and survival benefits in the Niemann-Pick mouse. Proc Natl Acad Sci USA 2007; 104: 9505-9510.
58. Orfanelli U, Wenke AK, Doglioni C, Russo V, Bosserhoff AK, Lavorgna G. Identification of novel sense and antisense transcription at the TRPM2 locus in cancer. Cell Res 2008; 18: 1128-1140.
59. Medic S, Ziman M. PAX3 expression in normal skin melanocytes and melanocytic lesions (naevi and melanomas). PLoS One 2010; 5: e9977.
60. Pavlidis P, Noble WS. Matrix2png: a utility for visualizing matrix data. Bioinformatics 2003; 19: 295-296.