Ceramide as a target of chemotherapy: Its role in apoptosis and autophagy

Clinical Lipidology

Volumn 7, Issue 1, 2012, Pages 111-119

  De Palma, Clara ^a   Perrotta, Cristiana ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

apoptosis; autophagy; ceramide; chemotherapy

Indexed keywords

BECLIN 1; C6 CERAMIDE; CATHEPSIN D; CERAMIDE; CERAMIDE DERIVATIVE; MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN BCL 2; PROTEIN KINASE B; SPHINGOMYELIN PHOSPHODIESTERASE; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGY; CANCER CELL; CANCER CHEMOTHERAPY; CARCINOGENESIS; CELL FATE; CELL SURVIVAL; DRUG TARGETING; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; EXTRINSIC APOPTOTIC PATHWAY; HUMAN; INTRINSIC APOPTOTIC PATHWAY; LIPID ANALYSIS; LIPOGENESIS; LYSOSOME MEMBRANE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 84856925711     PISSN: 17460875     EISSN: 17584302     Source Type: Journal    
DOI: 10.2217/clp.11.71     Document Type: Review

References (79)

1. Sawai H, Domae N, Okazaki T. Current status and perspectives in ceramide-targeting molecular medicine. Curr. Pharm. Des. 11(19), 2479-2487 (2005). (Pubitemid 40872692)
2. Hannun YA, Luberto C. Lipid metabolism: ceramide transfer protein adds a new dimension. Curr. Biol. 14(4), R163-R165 (2004). (Pubitemid 38300202)
3. Payne SG, Milstien S, Spiegel S. Sphingosine-1-phosphate: dual messenger functions. FEBS Lett. 531(1), 54-57 (2002). (Pubitemid 35232784)
4. Bleicher RJ, Cabot MC. Glucosylceramide synthase and apoptosis. Biochim. Biophys. Acta 1585(2-3), 172-178 (2002). (Pubitemid 36092082)
5. Hannun YA, Obeid LM. Many ceramides. J. Biol. Chem. 286(32), 27855-27862 (2011).
6. Nikolova-Karakashian MN, Rozenova KA. Ceramide in stress response. Adv. Exp. Med. Biol. 688, 86-108 (2010).
7. Bedia C, Levade T, Codogno P. Regulation of autophagy by sphingolipids. Anticancer Agents Med. Chem. 11(9), 844-853 (2011).
8. Kitatani K, Idkowiak-Baldys J, Hannun YA. The sphingolipid salvage pathway in ceramide metabolism and signaling. Cell Signal. 20(6), 1010-1018 (2008).
9. Tchikov V, Bertsch U, Fritsch J, Edelmann B, Schutze S. Subcellular compartmentalization of TNF receptor-1 and CD95 signaling pathways. Eur. J. Cell. Biol. 90(6-7), 467-475 (2011).
10. Edelmann B, Bertsch U, Tchikov V et al. Caspase-8 and caspase-7 sequentially mediate proteolytic activation of acid sphingomyelinase in TNF-R1 receptosomes. EMBO J. 30(2), 379-394 (2011).
11. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat. Med. 6(5), 513-519 (2000). (Pubitemid 30305900)
12. Grassme H, Cremesti A, Kolesnick R, Gulbins E. Ceramide-mediated clustering is required for CD95-DISC formation. Oncogene 22(35), 5457-5470 (2003). (Pubitemid 37072201)
13. Perrotta C, Bizzozero L, Falcone S et al. Nitric oxide boosts chemoimmunotherapy via inhibition of acid sphingomyelinase in a mouse model of melanoma. Cancer Res. 67(16), 7559-7564 (2007). (Pubitemid 47281347)
14. Perrotta C, Bizzozero L, Cazzato D et al. Syntaxin 4 is required for acid sphingomyelinase activity and apoptotic function. J. Biol. Chem. 285(51), 40240-40251 (2010).
15. Horinouchi K, Erlich S, Perl DP et al. Acid sphingomyelinase defcient mice: a model of types A and B Niemann-Pick disease. Nat. Genet. 10(3), 288-293 (1995).
16. Dumitru CA, Gulbins E. TRAIL activates acid sphingomyelinase via a redox mechanism and releases ceramide to trigger apoptosis. Oncogene 25(41), 5612-5625 (2006). (Pubitemid 44387617)
17. Li X, Becker KA, Zhang Y. Ceramide in redox signaling and cardiovascular diseases. Cell. Physiol. Biochem. 26(1), 41-48 (2010).
18. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL. Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47(1), 74-80 (2006). (Pubitemid 43177818)
19. Montfort A, Martin PG, Levade T, Benoist H, Segui B. FAN (factor associated with neutral sphingomyelinase activation), a moonlighting protein in TNF-R1 signaling. J. Leukoc. Biol. 88(5), 897-903 (2010).
20. Hannun YA, Obeid LM. Principles of bioactive lipid signalling: lessons from sphingolipids. Nat. Rev. Mol. Cell. Biol. 9(2), 139-150 (2008). (Pubitemid 351158911)
21. Ferri KF, Kroemer G. Organelle-specifc initiation of cell death pathways. Nat. Cell. Biol. 3(11), E255-E263 (2001).
22. Xu C, Bailly-Maitre B, Reed JC. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115(10), 2656-2664 (2005). (Pubitemid 41434389)
23. Kroemer G, Jaattela M. Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5(11), 886-897 (2005). (Pubitemid 41746033)
24. Rao R P, Yuan C, Allegood JC et al. Ceramide transfer protein function is essential for normal oxidative stress response and lifespan. Proc. Natl Acad. Sci. USA 104(27), 11364-11369 (2007). (Pubitemid 47175146)
25. Senkal CE, Ponnusamy S, Bielawski J, Hannun YA, Ogretmen B. Antiapoptotic roles of ceramide-synthase-6-generated C16-ceramide via selective regulation of the ATF6/CHOP arm of ER-stress-response pathways. FASEB J. 24(1), 296-308 (2010).
26. Chen CL, Lin CF, Chang WT, Huang WC, Teng CF, Lin YS. Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin- interacting protein-mediated pathway. Blood 111(8), 4365-4374 (2008).
27. White-Gilbertson S, Mullen T, Senkal C et al. Ceramide synthase 6 modulates TRAIL sensitivity and nuclear translocation of active caspase-3 in colon cancer cells. Oncogene 28(8), 1132-1141 (2009).
28. Heinrich M, Neumeyer J, Jakob M et al. Cathepsin D links TNF-induced acid sphingomyelinase to Bid-mediated caspase-9 and-3 activation. Cell Death Differ. 11(5), 550-563 (2004). (Pubitemid 38660140)
29. Pettus BJ, Chalfant CE, Hannun YA. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585(2-3), 114-125 (2002). (Pubitemid 36092075)
30. Lavieu G, Scarlatti F, Sala G et al. Is autophagy the key mechanism by which the sphingolipid rheostat controls the cell fate decision? Autophagy 3(1), 45-47 (2007). (Pubitemid 46100712)
31. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 90(2), 313-323 (2008). (Pubitemid 351181247)
32. Pankiv S, Clausen TH, Lamark T et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 282(33), 24131-24145 (2007). (Pubitemid 47328003)
33. Schweers RL, Zhang J, Randall MS et al. NIX is required for programmed mitochondrial clearance during reticulocyte maturation. Proc. Natl Acad. Sci. USA 104(49), 19500-19505 (2007).
34. Pattingre S, Bauvy C, Carpentier S, Levade T, Levine B, Codogno P. Role of JNK1-dependent Bcl-2 phosphorylation in ceramide-induced macroautophagy. J. Biol. Chem. 284(5), 2719-2728 (2009).
35. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol. Cell 30(6), 678-688 (2008). (Pubitemid 351818252)
36. Levine B, Sinha S, Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 4(5), 600-606 (2008).
37. Daido S, Kanzawa T, Yamamoto A, Takeuchi H, Kondo Y, Kondo S. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64(12), 4286-4293 (2004). (Pubitemid 38802435)
38. Guenther GG, Peralta ER, Rosales KR, Wong SY, Siskind LJ, Edinger AL. Ceramide starves cells to death by downregulating nutrient transporter proteins. Proc. Natl Acad. Sci. USA 105(45), 17402-17407 (2008).
39. Lavieu G, Scarlatti F, Sala G et al. Regulation of autophagy by sphingosine kinase 1 and its role in cell survival during nutrient starvation. J. Biol. Chem. 281(13), 8518-8527 (2006). (Pubitemid 43847954)
40. Colie S, Van Veldhoven PP, Kedjouar B et al. Disruption of sphingosine 1-phosphate lyase confers resistance to chemotherapy and promotes oncogenesis through Bcl-2/Bcl-xL upregulation. Cancer Res. 69(24), 9346-9353 (2009).
41. Degenhardt K, Mathew R, Beaudoin B et al. Autophagy promotes tumor cell survival and restricts necrosis, infammation, and tumorigenesis. Cancer Cell 10(1), 51-64 (2006).
42. Edinger AL, Thompson CB. Defective autophagy leads to cancer. Cancer Cell 4(6), 422-424 (2003). (Pubitemid 38050038)
43. Komatsu M, Waguri S, Koike M et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-defcient mice. Cell 131(6), 1149-1163 (2007). (Pubitemid 350235021)
44. Cuervo AM. Autophagy: in sickness and in health. Trends Cell. Biol. 14(2), 70-77 (2004). (Pubitemid 38186640)
45. Lu Z, Luo RZ, Lu Y et al. The tumor suppressor gene ARHI regulates autophagy and tumor dormancy in human ovarian cancer cells. J. Clin. Invest. 118(12), 3917-3929 (2008).
46. Guo JY, Chen HY, Mathew R et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev. 25(5), 460-470 (2011).
47. Beljanski V, Knaak C, Smith CD. A novel sphingosine kinase inhibitor induces autophagy in tumor cells. J. Pharmacol. Exp. Ther. 333(2), 454-464 (2010).
48. Salazar M, Carracedo A, Salanueva IJ et al. Cannabinoid action induces autophagy-mediated cell death through stimulation of ER stress in human glioma cells. J. Clin. Invest. 119(5), 1359-1372 (2009).
49. Ponnusamy S, Meyers-Needham M, Senkal CE et al. Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol. 6(10), 1603-1624 (2010).
50. Tagaram HR, Divittore NA, Barth BM et al. Nanoliposomal ceramide prevents in vivo growth of hepatocellular carcinoma. Gut 60(5), 695-701 (2011).
51. Tran MA, Smith CD, Kester M, Robertson GP. Combining nanoliposomal ceramide with sorafenib synergistically inhibits melanoma and breast cancer cell survival to decrease tumor development. Clin. Cancer Res. 14(11), 3571-3581 (2008).
52. Jiang Y, Divittore NA, Kaiser JM et al. Combinatorial therapies improve the therapeutic effcacy of nanoliposomal ceramide for pancreatic cancer. Cancer Biol. Ther. 12(7), 574-585 (2011).
53. Futerman AH, Hannun YA. The complex life of simple sphingolipids. EMBO Rep. 5(8), 777-782 (2004). (Pubitemid 39199166)
54. Ogretmen B, Hannun YA. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer 4(8), 604-616 (2004). (Pubitemid 39025055)
55. Vaisman A, Varchenko M, Said I, Chaney SG. Cell cycle changes associated with formation of Pt-DNA adducts in human ovarian carcinoma cells with different cisplatin sensitivity. Cytometry 27(1), 54-64 (1997). (Pubitemid 27059782)
56. Eastman A. Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cis-dichloro(ethylenediamine)platinum(II). Biochemistry 22(16), 3927-3933 (1983). (Pubitemid 13035562)
57. Hueber A, Welsandt G, Jordan JF et al. Characterization of CD95 ligand (CD95L)-induced apoptosis in human tenon fbroblasts. Exp. Eye Res. 75(1), 1-8 (2002). (Pubitemid 34765345)
58. Bezombes C, Grazide S, Garret C et al. Rituximab antiproliferative effect in B-lymphoma cells is associated with acid-sphingomyelinase activation in raft microdomains. Blood 104(4), 1166-1173 (2004). (Pubitemid 39038039)
59. Bezombes C, Laurent G, Jaffrezou JP. Implication of raft microdomains in drug induced apoptosis. Curr. Med. Chem Anticancer Agents 3(4), 263-270 (2003). (Pubitemid 36758301)
60. Lacour S, Hammann A, Grazide S et al. Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res. 64(10), 3593-3598 (2004). (Pubitemid 38657937)
61. Garcia-Barros M, Paris F, Cordon-Cardo C et al. Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300(5622), 1155-1159 (2003). (Pubitemid 36583102)
62. Ito H, Murakami M, Furuhata A et al. Transcriptional regulation of neutral sphingomyelinase 2 gene expression of a human breast cancer cell line, MCF-7, induced by the anti-cancer drug, daunorubicin. Biochim. Biophys. Acta 1789(11-12), 681-690 (2009).
63. Uchida Y, Itoh M, Taguchi Y et al. Ceramide reduction and transcriptional up-regulation of glucosylceramide synthase through doxorubicin-activated Sp1 in drug-resistant HL-60/ADR cells. Cancer Res. 64(17), 6271-6279 (2004). (Pubitemid 39129431)
64. Dumitru CA, Carpinteiro A, Trarbach T, Hengge UR, Gulbins E. Doxorubicin enhances TRAIL-induced cell death via ceramide-enriched membrane platforms. Apoptosis 12(8), 1533-1541 (2007). (Pubitemid 46988288)
65. Rath G, Schneider C, Langlois B et al. De novo ceramide synthesis is responsible for the anti-tumor properties of camptothecin and doxorubicin in follicular thyroid carcinoma. Int. J. Biochem. Cell. Biol. 41(5), 1165-1172 (2009).
66. Min J, Mesika A, Sivaguru M et al. (Dihydro) ceramide synthase 1 regulated sensitivity to cisplatin is associated with the activation of p38 mitogen-activated protein kinase and is abrogated by sphingosine kinase 1. Mol. Cancer Res. 5(8), 801-812 (2007). (Pubitemid 47294808)
67. Senkal CE, Ponnusamy S, Rossi MJ et al. Role of human longevity assurance gene 1 and C18-ceramide in chemotherapy-induced cell death in human head and neck squamous cell carcinomas. Mol. Cancer Ther. 6(2), 712-722 (2007). (Pubitemid 46332472)
68. Morales A, Paris R, Villanueva A, Llacuna L, Garcia-Ruiz C, Fernandez-Checa JC. Pharmacological inhibition or small interfering RNA targeting acid ceramidase sensitizes hepatoma cells to chemotherapy and reduces tumor growth in vivo. Oncogene 26(6), 905-916 (2007).
69. Bielawska A, Bielawski J, Szulc ZM et al. Novel analogs of D-e-MAPP and B13. Part 2: signature effects on bioactive sphingolipids. Bioorg. Med. Chem. 16(2), 1032-1045 (2008). (Pubitemid 351163040)
70. Bedia C, Casas J, Andrieu-Abadie N, Fabrias G, Levade T. Acid ceramidase expression modulates the sensitivity of A375 melanoma cells to dacarbazine. J. Biol. Chem. 286(32), 28200-28209 (2011).
71. Scarlatti F, Sala G, Ricci C et al. Resveratrol sensitization of DU145 prostate cancer cells to ionizing radiation is associated to ceramide increase. Cancer Lett. 253(1), 124-130 (2007). (Pubitemid 46874732)
72. Delmas D, Solary E, Latruffe N. Resveratrol, a phytochemical inducer of multiple cell death pathways: apoptosis, autophagy and mitotic catastrophe. Curr. Med. Chem. 18(8), 1100-1121 (2011).
73. Sanchez AM, Malagarie-Cazenave S, Olea N, Vara D, Chiloeches A, Diaz-Laviada I. Apoptosis induced by capsaicin in prostate PC-3 cells involves ceramide accumulation, neutral sphingomyelinase, and JNK activation. Apoptosis 12(11), 2013-2024 (2007). (Pubitemid 47498227)
74. Mondal S, Mandal C, Sangwan R, Chandra S. Withanolide D induces apoptosis in leukemia by targeting the activation of neutral sphingomyelinase-ceramide cascade mediated by synergistic activation of c-Jun N-terminal kinase and p38 mitogen-activated protein kinase. Mol. Cancer 9, 239 (2010).
75. Canals D, Mormeneo D, Fabrias G, Llebaria A, Casas J, Delgado A. Synthesis and biological properties of Pachastrissamine (jaspine B) and diastereoisomeric jaspines. Bioorg. Med. Chem. 17(1), 235-241 (2009).
76. Ogretmen B, Hannun YA. Updates on functions of ceramide in chemotherapy-induced cell death and in multidrug resistance. Drug Resist. Updat. 4(6), 368-377 (2001). (Pubitemid 34746871)
77. Senchenkov A, Han TY, Wang H et al. Enhanced ceramide generation and induction of apoptosis in human leukemia cells exposed to DT(388)-granulocyte- macrophage colony-stimulating factor (GM-CSF), a truncated diphtheria toxin fused to human GM-CSF. Blood 98(6), 1927-1934 (2001).
78. Radin NS. The development of aggressive cancer: a possible role for sphingolipids. Cancer Invest. 20(5-6), 779-786 (2002). (Pubitemid 37210051)
79. Hinrichs J W, Klappe K, Kok J W. Rafts as missing link between multidrug resistance and sphingolipid metabolism. J. Membr. Biol. 203(2), 57-64 (2005). (Pubitemid 40976368)