Essential role for acid sphingomyelinase-inhibited autophagy in melanoma response to cisplatin

Oncotarget

Volumn 7, Issue 18, 2016, Pages 24995-25009

  Cervia, Davide ^a,b   Assi, Emma ^c,d   De Palma, Clara ^b   Giovarelli, Matteo ^b   Bizzozero, Laura ^c,e   Pambianco, Sarah ^b   Di Renzo, Ilaria ^b   Zecchini, Silvia ^b   Moscheni, Claudia ^b   Vantaggiato, Chiara ^c   Procacci, Patrizia ^f   Clementi, Emilio ^b,c   Perrotta, Cristiana ^b  

^a UNIVERSITY OF TUSCIA   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c SCIENTIFIC INSTITUTE   (Italy)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e UNIVERSITY OF TURIN   (Italy)

^f UNIVERSITY OF MILAN   (Italy)

Author keywords

A SMase; Autophagy; Chemo resistance; Melanoma; mTOR

Indexed keywords

CHLOROQUINE; CISPLATIN; IMMUNOGLOBULIN LIGHT CHAIN; IMMUNOGLOBULIN LIGHT CHAIN 3; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; SPHINGOMYELIN PHOSPHODIESTERASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFICACY; DRUG POTENCY; DRUG POTENTIATION; DRUG SENSITIVITY; DRUG TARGETING; EC50; ENZYME ACTIVITY; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MELANOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL TIME; TREATMENT RESPONSE; UPREGULATION; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; ENZYMOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; AUTOPHAGY; CISPLATIN; DRUG RESISTANCE, NEOPLASM; HUMANS; MELANOMA; MICE; SPHINGOMYELIN PHOSPHODIESTERASE; TOR SERINE-THREONINE KINASES;

EID: 84967261194     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.8735     Document Type: Article

References (84)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA. 2010; 60:277-300.
2. Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer. 2010; 46:765-781.
3. Leiter U, Eigentler T, Garbe C. Epidemiology of skin cancer. Adv Exp Med Biol. 2014; 810:120-140.
4. Tsao H, Atkins MB, Sober AJ. Management of cutaneous melanoma. N Engl J Med. 2004; 351:998-1012.
5. Gogas HJ, Kirkwood JM, Sondak VK. Chemotherapy for metastatic melanoma: time for a change? Cancer. 2007; 109:455-464.
6. Megahed AI, Koon HB. What is the role of chemotherapy in the treatment of melanoma? Current treatment options in oncology. 2014; 15:321-335.
7. Nikolaou VA, Stratigos AJ, Flaherty KT, Tsao H. Melanoma: new insights and new therapies. J Invest Dermatol. 2012; 132:854-863.
8. Finn L, Markovic SN, Joseph RW. Therapy for metastatic melanoma: the past, present, and future. BMC Med. 2012; 10:23.
9. Tronnier M, Mitteldorf C. Treating advanced melanoma: current insights and opportunities. Cancer management and research. 2014; 6:349-356.
10. Grimaldi AM, Cassidy PB, Leachmann S, Ascierto PA. Novel approaches in melanoma prevention and therapy. Cancer Treat Res. 2014; 159:443-455.
11. Hao M, Song F, Du X, Wang G, Yang Y, Chen K, Yang J. Advances in targeted therapy for unresectable melanoma: new drugs and combinations. Cancer Lett. 2015; 359:1-8.
12. Homet B, Ribas A. New drug targets in metastatic melanoma. J Pathol. 2014; 232:134-141.
13. Michielin O, Hoeller C. Gaining momentum: New options and opportunities for the treatment of advanced melanoma. Cancer Treat Rev. 2015; 41:660-670.
14. Barth S, Glick D, Macleod KF. Autophagy: assays and artifacts. J Pathol. 2010; 221:117-124.
15. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010; 140:313-326.
16. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012; 8:445-544.
17. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, Adhihetty PJ, Adler SG, Agam G, Agarwal R, Aghi MK, Agnello M, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016; 12:1-222.
18. Sui X, Chen R, Wang Z, Huang Z, Kong N, Zhang M, Han W, Lou F, Yang J, Zhang Q, Wang X, He C, Pan H. Autophagy and chemotherapy resistance: a promising therapeutic target for cancer treatment. Cell Death Dis. 2013; 4:e838.
19. Corazzari M, Fimia GM, Lovat P, Piacentini M. Why is autophagy important for melanoma? Molecular mechanisms and therapeutic implications. Semin Cancer Biol. 2013; 23:337-343.
20. Buchser WJ, Laskow TC, Pavlik PJ, Lin HM, Lotze MT. Cell-mediated autophagy promotes cancer cell survival. Cancer Res. 2012; 72:2970-2979.
21. Duffy A, Le J, Sausville E, Emadi A. Autophagy modulation: a target for cancer treatment development. Cancer Chemother Pharmacol. 2015; 75:439-447.
22. Marino ML, Pellegrini P, Di Lernia G, Djavaheri-Mergny M, Brnjic S, Zhang X, Hagg M, Linder S, Fais S, Codogno P, De Milito A. Autophagy is a protective mechanism for human melanoma cells under acidic stress. J Biol Chem. 2012; 287:30664-30676.
23. Wu WK, Coffelt SB, Cho CH, Wang XJ, Lee CW, Chan FK, Yu J, Sung JJ. The autophagic paradox in cancer therapy. Oncogene. 2012; 31:939-953.
24. Lazova R, Klump V, Pawelek J. Autophagy in cutaneous malignant melanoma. Journal of cutaneous pathology. 2010; 37:256-268.
25. Lazova R, Pawelek JM. Why do melanomas get so dark? Experimental Dermatology. 2009; 18:934-938.
26. Siddik ZH. Cisplatin: mode of cytotoxic action and molecular basis of resistance. Oncogene. 2003; 22:7265-7279.
27. 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.
28. Lacour S, Hammann A, Grazide S, Lagadic-Gossmann D, Athias A, Sergent O, Laurent G, Gambert P, Solary E, Dimanche-Boitrel MT. Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res. 2004; 64:3593-3598.
29. Prinetti A, Millimaggi D, D'Ascenzo S, Clarkson M, Bettiga A, Chigorno V, Sonnino S, Pavan A, Dolo V. Lack of ceramide generation and altered sphingolipid composition are associated with drug resistance in human ovarian carcinoma cells. Biochem J. 2006; 395:311-318.
30. Ellegaard AM, Groth-Pedersen L, Oorschot V, Klumperman J, Kirkegaard T, Nylandsted J, Jaattela M. Sunitinib and SU11652 inhibit acid sphingomyelinase, destabilize lysosomes, and inhibit multidrug resistance. Mol Cancer Ther. 2013; 12:2018-2030.
31. Petersen NH, Olsen OD, Groth-Pedersen L, Ellegaard AM, Bilgin M, Redmer S, Ostenfeld MS, Ulanet D, Dovmark TH, Lonborg A, Vindelov SD, Hanahan D, Arenz C, Ejsing CS, Kirkegaard T, Rohde M, et al. Transformation-associated changes in sphingolipid metabolism sensitize cells to lysosomal cell death induced by inhibitors of acid sphingomyelinase. Cancer Cell. 2013; 24:379-393.
32. Savic R, He X, Fiel I, Schuchman EH. Recombinant human acid sphingomyelinase as an adjuvant to sorafenib treatment of experimental liver cancer. PLoS One. 2013; 8:e65620.
33. Dimanche-Boitrel MT, Rebillard A. Sphingolipids and response to chemotherapy. Handb Exp Pharmacol. 2013:73-91.
34. Smith EL, Schuchman EH. Acid sphingomyelinase overexpression enhances the antineoplastic effects of irradiation in vitro and in vivo. Mol Ther. 2008; 16:1565-1571.
35. Perrotta C, Bizzozero L, Falcone S, Rovere-Querini P, Prinetti A, Schuchman EH, Sonnino S, Manfredi AA, Clementi E. Nitric oxide boosts chemoimmunotherapy via inhibition of acid sphingomyelinase in a mouse model of melanoma. Cancer Res. 2007; 67:7559-7564.
36. Perrotta C, Clementi E. Biological roles of Acid and neutral sphingomyelinases and their regulation by nitric oxide. Physiology (Bethesda). 2010; 25:64-71.
37. Assi E, Cervia D, Bizzozero L, Capobianco A, Pambianco S, Morisi F, De Palma C, Moscheni C, Pellegrino P, Clementi E, Perrotta C. Modulation of Acid Sphingomyelinase in Melanoma Reprogrammes the Tumour Immune Microenvironment. Mediators Inflamm. 2015; 2015:370482.
38. Bizzozero L, Cazzato D, Cervia D, Assi E, Simbari F, Pagni F, De Palma C, Monno A, Verdelli C, Querini PR, Russo V, Clementi E, Perrotta C. Acid sphingomyelinase determines melanoma progression and metastatic behaviour via the microphtalmia-associated transcription factor signalling pathway. Cell Death Differ. 2014; 21:507-520.
39. Tommasino C, Marconi M, Ciarlo L, Matarrese P, Malorni W. Autophagic flux and autophagosome morphogenesis require the participation of sphingolipids. Apoptosis. 2015; 20:645-657.
40. Perrotta C, Cervia D, De Palma C, Assi E, Pellegrino P, Bassi MT, Clementi E. The emerging role of acid sphingomyelinase in autophagy. Apoptosis. 2015; 20:635-644.
41. Milhas D, Clarke CJ, Hannun YA. Sphingomyelin metabolism at the plasma membrane: implications for bioactive sphingolipids. FEBS Lett. 2010; 584:1887-1894.
42. Zhang P, Liu B, Jenkins GM, Hannun YA, Obeid LM. Expression of neutral sphingomyelinase identifies a distinct pool of sphingomyelin involved in apoptosis. J Biol Chem. 1997; 272:9609-9612.
43. Arenz C. Small molecule inhibitors of acid sphingomyelinase. Cell Physiol Biochem. 2010; 26:1-8.
44. Jung CH, Ro SH, Cao J, Otto NM, Kim DH. mTOR regulation of autophagy. FEBS Lett. 2010; 584:1287-1295.
45. Egan D, Kim J, Shaw RJ, Guan KL. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy. 2011; 7:643-644.
46. Fader CM, Colombo MI. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 2009; 16:70-78.
47. Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013; 14:759-774.
48. Ge R, Liu L, Dai W, Zhang W, Yang Y, Wang H, Shi Q, Guo S, Yi X, Wang G, Gao T, Luan Q, Li C. XPA promotes autophagy to facilitate cisplatin resistance in melanoma cells through the activation of PARP1. J Invest Dermatol. 2016.
49. Hu YL, DeLay M, Jahangiri A, Molinaro AM, Rose SD, Carbonell WS, Aghi MK. Hypoxia-induced autophagy promotes tumor cell survival and adaptation to antiangiogenic treatment in glioblastoma. Cancer Res. 2012; 72:1773-1783.
50. Lakhter AJ, Sahu RP, Sun Y, Kaufmann WK, Androphy EJ, Travers JB, Naidu SR. Chloroquine promotes apoptosis in melanoma cells by inhibiting BH3 domain-mediated PUMA degradation. J Invest Dermatol. 2013; 133:2247-2254.
51. Kim EL, Wustenberg R, Rubsam A, Schmitz-Salue C, Warnecke G, Bucker EM, Pettkus N, Speidel D, Rohde V, Schulz-Schaeffer W, Deppert W, Giese A. Chloroquine activates the p53 pathway and induces apoptosis in human glioma cells. Neuro Oncol. 2010; 12:389-400.
52. De Palma C, Morisi F, Cheli S, Pambianco S, Cappello V, Vezzoli M, Rovere-Querini P, Moggio M, Ripolone M, Francolini M, Sandri M, Clementi E. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis. 2012; 3:e418.
53. Kimura T, Takabatake Y, Takahashi A, Isaka Y. Chloroquine in cancer therapy: a double-edged sword of autophagy. Cancer Res. 2013; 73:3-7.
54. Perrotta C, De Palma C, Clementi E. Nitric oxide and sphingolipids: mechanisms of interaction and role in cellular pathophysiology. Biol Chem. 2008; 389:1391-1397.
55. Lee JK, Jin HK, Park MH, Kim BR, Lee PH, Nakauchi H, Carter JE, He X, Schuchman EH, Bae JS. Acid sphingomyelinase modulates the autophagic process by controlling lysosomal biogenesis in Alzheimer's disease. J Exp Med. 2014; 211:1551-1570.
56. Patschan S, Chen J, Polotskaia A, Mendelev N, Cheng J, Patschan D, Goligorsky MS. Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells. Am J Physiol Heart Circ Physiol. 2008; 294:H1119-1129.
57. Toops KA, Tan LX, Jiang Z, Radu RA, Lakkaraju A. Cholesterol-mediated activation of acid sphingomyelinase disrupts autophagy in the retinal pigment epithelium. Mol Biol Cell. 2015; 26:1-14.
58. Gabande-Rodriguez E, Boya P, Labrador V, Dotti CG, Ledesma MD. High sphingomyelin levels induce lysosomal damage and autophagy dysfunction in Niemann Pick disease type A. Cell Death Differ. 2014; 21:864-875.
59. Li X, Xu M, Pitzer AL, Xia M, Boini KM, Li PL, Zhang Y. Control of autophagy maturation by acid sphingomyelinase in mouse coronary arterial smooth muscle cells: protective role in atherosclerosis. J Mol Med (Berl). 2014; 92:473-485.
60. Fucho R, Martinez L, Baulies A, Torres S, Tarrats N, Fernandez A, Ribas V, Astudillo AM, Balsinde J, Garcia-Roves P, Elena M, Bergheim I, Lotersztajn S, Trautwein C, Appelqvist H, Paton AW, et al. ASMase regulates autophagy and lysosomal membrane permeabilization and its inhibition prevents early stage non-alcoholic steatohepatitis. J Hepatol. 2014; 61:1126-1134.
61. Lavieu G, Scarlatti F, Sala G, Levade T, Ghidoni R, Botti J, Codogno P. Is autophagy the key mechanism by which the sphingolipid rheostat controls the cell fate decision? Autophagy. 2007; 3:45-47.
62. Cervia D, Perrotta C, Moscheni C, De Palma C, Clementi E. Nitric oxide and sphingolipids control apoptosis and autophagy with a significant impact on Alzheimer's disease. J Biol Regul Homeost Agents. 2013; 27:11-22.
63. Li Y, Li S, Qin X, Hou W, Dong H, Yao L, Xiong L. The pleiotropic roles of sphingolipid signaling in autophagy. Cell Death Dis. 2014; 5:e1245.
64. Taniguchi M, Kitatani K, Kondo T, Hashimoto-Nishimura M, Asano S, Hayashi A, Mitsutake S, Igarashi Y, Umehara H, Takeya H, Kigawa J, Okazaki T. Regulation of autophagy and its associated cell death by "sphingolipid rheostat": reciprocal role of ceramide and sphingosine 1-phosphate in the mammalian target of rapamycin pathway. J Biol Chem. 2012; 287:39898-39910.
65. De Palma C, Perrotta C. Ceramide as a target of chemotherapy: Its role in apoptosis and autophagy. Clin Lipidol. 2012; 7:111-119.
66. Vollrath JT, Sechi A, Dreser A, Katona I, Wiemuth D, Vervoorts J, Dohmen M, Chandrasekar A, Prause J, Brauers E, Jesse CM, Weis J, Goswami A. Loss of function of the ALS protein SigR1 leads to ER pathology associated with defective autophagy and lipid raft disturbances. Cell Death Dis. 2014; 5:e1290.
67. Hu YL, Jahangiri A, Delay M, Aghi MK. Tumor cell autophagy as an adaptive response mediating resistance to treatments such as antiangiogenic therapy. Cancer Res. 2012; 72:4294-4299.
68. Rangwala R, Leone R, Chang YC, Fecher LA, Schuchter LM, Kramer A, Tan KS, Heitjan DF, Rodgers G, Gallagher M, Piao S, Troxel AB, Evans TL, DeMichele AM, Nathanson KL, O'Dwyer PJ, et al. Phase I trial of hydroxychloroquine with dose-intense temozolomide in patients with advanced solid tumors and melanoma. Autophagy. 2014; 10:1369-1379.
69. Rangwala R, Chang YC, Hu J, Algazy KM, Evans TL, Fecher LA, Schuchter LM, Torigian DA, Panosian JT, Troxel AB, Tan KS, Heitjan DF, DeMichele AM, Vaughn DJ, Redlinger M, Alavi A, et al. Combined MTOR and autophagy inhibition: phase I trial of hydroxychloroquine and temsirolimus in patients with advanced solid tumors and melanoma. Autophagy. 2014; 10:1391-1402.
70. Ma XH, Piao S, Wang D, McAfee QW, Nathanson KL, Lum JJ, Li LZ, Amaravadi RK. Measurements of tumor cell autophagy predict invasiveness, resistance to chemotherapy, and survival in melanoma. Clin Cancer Res. 2011; 17:3478-3489.
71. Martin S, Dudek-Peric AM, Maes H, Garg AD, Gabrysiak M, Demirsoy S, Swinnen JV, Agostinis P. Concurrent MEK and autophagy inhibition is required to restore cell death associated danger-signalling in Vemurafenib-resistant melanoma cells. Biochem Pharmacol. 2015; 93:290-304.
72. Goodall ML, Wang T, Martin KR, Kortus MG, Kauffman AL, Trent JM, Gately S, MacKeigan JP. Development of potent autophagy inhibitors that sensitize oncogenic BRAF V600E mutant melanoma tumor cells to vemurafenib. Autophagy. 2014; 10:1120-1136.
73. Rebecca VW, Massaro RR, Fedorenko IV, Sondak VK, Anderson AR, Kim E, Amaravadi RK, Maria-Engler SS, Messina JL, Gibney GT, Kudchadkar RR, Smalley KS. Inhibition of autophagy enhances the effects of the AKT inhibitor MK-2206 when combined with paclitaxel and carboplatin in BRAF wild-type melanoma. Pigment Cell Melanoma Res. 2014; 27:465-478.
74. Galluzzi L, Senovilla L, Vitale I, Michels J, Martins I, Kepp O, Castedo M, Kroemer G. Molecular mechanisms of cisplatin resistance. Oncogene. 2012; 31:1869-1883.
75. Young MM, Kester M, Wang HG. Sphingolipids: regulators of crosstalk between apoptosis and autophagy. J Lipid Res. 2013; 54:5-19.
76. Noack J, Choi J, Richter K, Kopp-Schneider A, Regnier-Vigouroux A. A sphingosine kinase inhibitor combined with temozolomide induces glioblastoma cell death through accumulation of dihydrosphingosine and dihydroceramide, endoplasmic reticulum stress and autophagy. Cell Death Dis. 2014; 5:e1425.
77. Gramatzki D, Herrmann C, Happold C, Becker KA, Gulbins E, Weller M, Tabatabai G. Glioma cell death induced by irradiation or alkylating agent chemotherapy is independent of the intrinsic ceramide pathway. PLoS One. 2013; 8:e63527.
78. Perrotta C, Bizzozero L, Cazzato D, Morlacchi S, Assi E, Simbari F, Zhang Y, Gulbins E, Bassi MT, Rosa P, Clementi E. Syntaxin 4 is required for acid sphingomyelinase activity and apoptotic function. J Biol Chem. 2010; 285:40240-40251.
79. Cazzato D, Assi E, Moscheni C, Brunelli S, De Palma C, Cervia D, Perrotta C, Clementi E. Nitric oxide drives embryonic myogenesis in chicken through the upregulation of myogenic differentiation factors. Exp Cell Res. 2014; 320:269-280.
80. Perrotta C, Buldorini M, Assi E, Cazzato D, De Palma C, Clementi E, Cervia D. The thyroid hormone triiodothyronine controls macrophage maturation and functions: protective role during inflammation. Am J Pathol. 2014; 184:230-247.
81. De Palma C, Di Paola R, Perrotta C, Mazzon E, Cattaneo D, Trabucchi E, Cuzzocrea S, Clementi E. Ibuprofen-arginine generates nitric oxide and has enhanced anti-inflammatory effects. Pharmacol Res. 2009; 60:221-228.
82. Armani C, Catalani E, Balbarini A, Bagnoli P, Cervia D. Expression, pharmacology, and functional role of somatostatin receptor subtypes 1 and 2 in human macrophages. J Leukoc Biol. 2007; 81:845-855.
83. Cervia D, Martini D, Garcia-Gil M, Di Giuseppe G, Guella G, Dini F, Bagnoli P. Cytotoxic effects and apoptotic signalling mechanisms of the sesquiterpenoid euplotin C, a secondary metabolite of the marine ciliate Euplotes crassus, in tumour cells. Apoptosis. 2006; 11:829-843.
84. Cervia D, Garcia-Gil M, Simonetti E, Di Giuseppe G, Guella G, Bagnoli P, Dini F. Molecular mechanisms of euplotin C-induced apoptosis: involvement of mitochondrial dysfunction, oxidative stress and proteases. Apoptosis. 2007; 12:1349-1363.