Cationic ceramides and analogues, LCL30 and LCL85, as adjuvants to photodynamic therapy of tumors

Journal of Photochemistry and Photobiology B: Biology

Volumn 126, Issue , 2013, Pages 72-77

  Korbelik, Mladen ^a   Zhang, Wei ^a   Saw, Kyi Min ^a   Szulc, Zdzislaw M ^b   Bielawska, Alicja ^b   Separovic, Duska ^c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c WAYNE STATE UNIVERSITY   (United States)

Author keywords

Dihydroceramide desaturase; Photodynamic therapy; SCCVII; Sphingolipid analogs; Sphingosine kinase; Squamous cell carcinoma

Indexed keywords

ANTINEOPLASTIC AGENT; CATIONIC C16 CERAMIDE LCL30; DEXTRO ERYTHRO 2 N [16' (1'' PYRIDINIUM) HEXADECANOYL] SPHINGOSINE BROMIDE; DEXTRO THREO 2 N [16' (1''' PYRIDINIUM) HEXADECANOYL]AMINO 1 (4''''NITROPHENYL) 1,3 PROPANDIOL BROMIDE; DIHYDROCERAMIDE DESATURASE; HYDROLASE INHIBITOR; LCL 30; LCL 85; OXYGENASE; PHOTOFRIN; PHTHALOCYANINE; SILICON PHTHALOCYANINE; SPHINGOSINE KINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER ADJUVANT THERAPY; CANCER CELL; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; FLOW CYTOMETRY; GENE EXPRESSION; GENETIC CODE; IN VITRO STUDY; MALIGNANT NEOPLASTIC DISEASE; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; SPHINGOLIPID METABOLISM; TISSUE DISTRIBUTION; TUMOR ABLATION; TUMOR GROWTH; TUMOR RECURRENCE; UPREGULATION;

DIHYDROCERAMIDE DESATURASE; PHOTODYNAMIC THERAPY; SPHINGOLIPID ANALOGS; SPHINGOSINE KINASE; SQUAMOUS CELL CARCINOMA SCCVII;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CERAMIDES; CHEMOTHERAPY, ADJUVANT; MICE; OXIDOREDUCTASES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PHOTOCHEMOTHERAPY; PROPANOLAMINES; PYRIDINIUM COMPOUNDS; SPHINGOSINE; TREATMENT OUTCOME; UP-REGULATION;

EID: 84885132906     PISSN: 10111344     EISSN: 18732682     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2013.06.013     Document Type: Article

References (47)

1. T.J. Dougherty, C.J. Gomer, B.W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan, Q. Peng, Photodynamic therapy, J. Natl. Cancer Inst. 90 (1998) 889-905. (Pubitemid 28304157)
2. P. Agostinis, K. Berg, K.A. Cengel, T.H. Foster, A.W. Girotti, S.O. Gollnick, S.M. Hahn, M.R. Hamblin, A. Juzeniene, D. Kessel, M. Korbelik, J. Moan, P. Mroz, D. Nowis, J. Piette, B.C. Wilson, J. Golab, Photodynamic therapy of cancer; an update, CA Cancer J. Clin. 61 (2011) 250-281.
3. Y.A. Hannun, L.M. Obeid, The ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind, J. Biol. Chem. 277 (2002) 25847-25850. (Pubitemid 34967060)
4. Y. Barenholz, Sphingomyelin and cholesterol: from membrane biophysics and rafts to potential medical applications, Subcell. Biochem. 37 (2004) 167-215.
5. D. Milhas, C.J. Clarke, Y.A. Hannun, Sphingolipid metabolism at the plasma membrane: implications for bioactive sphingolipids, FEBS Lett. 584 (2010) 1887-1894.
6. Y.A. Hannun, C. Luberto, Ceramide in the eukaryotic stress response, Trends Cell Biol. 10 (2010) 73-80.
7. B. Cinque, L. Di Marzio, C. Centi, C. Di Rocco, C. Riccardi, M.G. Cifone, Sphingolipids and the immune system, Pharmacol. Res. 47 (2003) 421-437. (Pubitemid 36379204)
8. I. Gombos, E. Kiss, C. Detre, G. Laszlo, J. Matko, Cholesterol and sphingolipids as lipid organizers of the immune cells' plasma membrane: their impact on the functions of MHC molecules, effector T-lymphocytes and T-cell death, Immunol. Lett. 104 (2006) 59-69. (Pubitemid 43330710)
9. B. Wispriyono, E. Schmelz, H.l. Pelayo, K. Hanada, D. Separovic, A role for de novo sphingolipids in apoptosis of photosensitized cells, Exp. Cell Res. 279 (2002) 153-165.
10. D. Separovic, J. Bielawski, J.S. Pierce, S. Merchant, A.L. Tarca, B. Ogretman, M. Korbelik, Increased tumor dihydroceramide production after Photofrin-PDT alone and improved tumour response after the combination with the ceramide analogue LCL29. Evidence from mouse squamous cell carcinomas, Br. J. Cancer 100 (2009) 626-632.
11. D. Separovic, J. Bielawski, J.S. Pierce, S. Merchant, A.L. Tarca, G. Bhatti, B. Ogretmen, M. Korbelik, Enhanced tumor cures after Foscan photodynamic therapy combined with the ceramide analog LCL29. Evidence from mouse squamous cell carcinomas for sphingolipids as biomarkers of treatment response, Int. J. Oncol. 38 (2011) 521-527.
12. A.G. Charles, T.Y. Han, Y.Y. Liu, N. Hansen, A.E. Giuliano, M.C. Cabot, Taxol-induced ceramide generation and apoptosis in human breast cancer cells, Cancer Chemother. Pharmacol. 47 (2001) 444-450. (Pubitemid 32397622)
13. V. Dolgachev, M.S. Farooqui, O.I. Kulaeva, M.A. Tainsky, B. Nagy, K. Hanada, D. Separovic, De novo ceramide accumulation due to inhibition of its conversion to complex sphingolipids in apoptotic photosensitized cells, J. Biol. Chem. 279 (2004) 23238-23249. (Pubitemid 38685631)
14. M. Korbelik, W. Zhang, D. Separovic, Amplification of cancer cell apoptosis, in photodynamic therapy-treated tumors by adjuvant ceramide analog LCL29, Lasers Surg. Med. 43 (2011) 614-620.
15. M. Korbelik, W. Zhang, D. Separovic, Monitoring ceramide and sphingosine-1-phosphate levels in cancer cells and macrophages from tumours treated by photodynamic therapy, Photochem. Photobiol. Sci. 11 (2012) 779.
16. M. Selzner, A. Bielawska, M.A. Morse, H.A. Rudiger, D. Sindram, Y.A. Hannun, P.A. Clavien, Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer, Cancer Res. 61 (2001) 1233-1240. (Pubitemid 32174448)
17. M. Kester, R. Kolesnick, Sphingolipids as therapeutics, Pharmacol. Res. 47 (2003) 365-371. (Pubitemid 36379198)
18. Y.H. Zeidan, Y.A. Hannun, Translational aspects of sphingolipid metabolism, Trends Mol. Med. 13 (2007) 327-336. (Pubitemid 47126985)
19. Z.M. Szulc, J. Bielawski, H. Gracz, M. Gustilo, N. Mayroo, Y.A. Hannun, L.M. Obeid, A. Bielawska, Tailoring structure-function and targeting properties of ceramides by site-specific cationization, Bioorg. Med. Chem. 14 (2006) 7083-7104. (Pubitemid 44403118)
20. Z.M. Szulc, N. Mayroo, A. Bai, J. Bielawski, X. Liu, J.S. Norris, Y.A. Hannun, A. Bielawska, Novel analogs of d-e-MAPP and B13. Part 1: synthesis and evaluation as potential anticancer agents, Bioorg. Med. Chem. 16 (2008) 1015-1031. (Pubitemid 351163041)
21. D. Separovic, Z.H. Saad, E.A. Edwin, J. Bielawski, J.S. Pierce, E. Van Buren, A. Bielawska, C16-ceramide analog combined with Pc 4 photodynamic therapy evokes enhanced total ceramide accumulation, promotion of DEVDase activation in the absence of apoptosis, and augmented overall cell killing, J. Lipids (2011), http://dx.doi.org/10.1155/2011/713867.
22. D. Separovic, N. Joseph, P. Breen, J. Bielawski, J.S. Pierce, E. Van Buren, G. Bhatti, Z.H. Saad, A. Bai, A. Bielawska, Combining anticancer agents photodynamic therapy and LCL85 leads to distinct changes in the sphingolipid profile, autophagy, caspase-3 activation in the absence of cell death, and long-term sensitization, Biochem. Biophys. Res. Commun. 409 (2011) 372-377.
23. F. Dahm, A. Bielawska, A. Nocito, P. Georgiew, Z.M. Szulc, J. Bielawski, W. Jochum, D. Dindo, Y.A. Hannun, P.-A. Clavien, Mitochondrially targeted ceramide LCL-30 inhibits colorectal cancer in mice, Br. J. Cancer 98 (2008) 98-105.
24. A. Bielawska, J. Bielawski, Z.M. Szulc, N. Mayroo, X. Liu, A. Bai, S. Elojeimy, B. Rembiesa, J. Pierce, J.S. Norris, Y.A. Hannun, Novel analogs of D-e-MAPP and B13. Part 2. Signature effects on bioactive sphingolipids, Bioorg. Med. Chem. 16 (2008) 1032-1045. (Pubitemid 351163040)
25. D. Khurana, E.A. Martin, J.L. Kasperbauer, B.W. O'Malley Jr., D.R. Salomao, L. Chen, S.E. Strome, Characterization of a spontaneously arising murine squamous cell carcinoma (SCC VII) as a prerequisite for head and neck cancer immunotherapy, Head Neck 23 (2001) 899-906. (Pubitemid 32862295)
26. K. Endo, Y. Matsuda, S. Kobayashi, Mdes, a mouse homolog of the of the Drosophila degenerative spermatocyte gene is expressed during mouse spermatogenesis, Dev. Growth Differ. 39 (1997) 399-404.
27. P. Ternes, S. Franke, U. Zahringer, P. Sperling, E. Heinz, Identification and characterization of a sphingolipid delta 4-desaturase family, J. Biol. Chem. 277 (2002) 25512-25518. (Pubitemid 34951866)
28. M. Maceyka, S.G. Payne, S. Milstein, S. Spiegel, Sphingosine kinase, sphingosine-1-phosphate, and apoptosis, Biochim. Biophys. Acta 1585 (2002) 193-201. (Pubitemid 36096858)
29. M. Korbelik, I. Cecic, S. Merchant, J. Sun, Acute phase response induction by cancer treatment with photodynamic therapy, Int. J. Cancer 122 (2008) 1411-1417. (Pubitemid 351287243)
30. S. Merchant, N. Huang, M. Korbelik, Expression of complement and pentraxin proteins in acute phase response elicited by tumor photodynamic therapy: the engagement of adrenal hormones, Int. Immunopharmacol. 10 (2010) 1595-1601.
31. X. Wang, Y. Guo, S. Yang, C. Wang, X. Fu, J. Wang, Y. Mao, J. Zhang, Y. Li, Cellular and molecular mechanisms of photodynamic hypericin therapy for nasopharyngeal carcinoma cells, J. Pharmacol. Exp. Ther. 334 (2010) 847-853.
32. F. Omae, M. Miyazaki, A. Enomoto, M. Suzuki, Y. Suzuki, A. Suzuki, DES2 protein is responsible for phytoceramide biosynthesis in the mouse small intestine, Biochem. J. 379 (2004) 687-695. (Pubitemid 38703653)
33. J. Idkowiak-Balys, A. Apraiz, L. Li, M. Rahmaniyan, C.J. Clarke, J.M. Kraveka, A. Asumendi, Y.A. Hannun, Dihidroceramide desaturase activity is modulated by oxidative stress, Biochem. J. 427 (2010) 265-274.
34. B.M. Buehrer, R.M. Bell, Sphingosine kinase: properties and cellular functions, Adv. Lipid Res. 26 (1993) 59-67.
35. T. Nishiuma, Y. Nishimura, T. Okada, E. Kuramoto, Y. Kotani, S. Jahangeer, S.-I. Nakamura, Inhalation of sphingosine kinase inhibitor attenuates airway inflammation in asthmatic mouse model, Am. J. Physiol. Lung Cell. Mol. Physiol. 294 (2008) L1085-L1093.
36. S. Merchant, M. Korbelik, Upregulation of genes for C-reactive protein and related pentraxin/complement proteins in photodynamic therapy-treated human tumor cells: enrolment of PI3K/Akt and AP-1, Immunobiology 218 (2013) 869-874.
37. R. Kammerer, A. Buchner, P. Palluch, T. Pongratz, K. Oboukhovskij, W. Beyer, A. Johansson, H. Stepp, R. Baumgartner, W. Zimmermann, Induction of immune mediators in glioma and prostate cancer cells by non-lethal photodynamic therapy, PLoS ONE 6 (2011) e21834.
38. A.B. Uzdensky, Signal transduction and photodynamic therapy, Curr. Sig. Trans. Ther. 3 (2008) 55-74. (Pubitemid 351267020)
39. S. Zhuang, I.E. Kochevar, Singlet oxygen-induced activation of Akt/Protein Kinase B is independent of growth factor receptors, Photochem. Photobiol. 78 (2003) 361-371.
40. J.-Y. Matroule, C. Volanti, J. Piette, NF-jB in photodynamic therapy: discrepancies of a master regulator, Photochem. Photobiol. 82 (2006) 1241-1246. (Pubitemid 44702003)
41. W.L. Holland, B.T. Bikman, L.P. Wang, G. Yuguang, K.M. Sargent, S. Bulchand, T.A. Knotts, G. Shui, D.J. Clegg, M.R. Wenk, M.J. Pagliassotti, P.E. Scherer, S.A. Summers, Lipid-induced insulin resistance mediated by the proinflammatory receptor TLR4 requires saturated fatty acid-induced ceramide biosynthesis in mice, J. Clin. Invest. 121 (2011) 1858-1870.
42. C. Senkal, S. Ponnusamy, M. Rossi, K. Sundaraj, Z.M. Szulc, J. Bielawski, A. Bielawska, M. Meyer, B. Cobanoglu, S. Koybasi, D. Sinha, T. Day, L.M. Obeid, Y.A. Hannun, B. Ogretmen, Potent anti-tumor activity of a novel cationic pyridinium-ceramide alone or in combination with gemcitabine against human head and neck squamous cell carcinomas in vitro and in vivo, J. Pharmacol. Exp. Ther. 317 (2006) 1188-1199. (Pubitemid 43764124)
43. T. Beckham, P. Lu, E. Jones, T.S. Marrison, C.S. Lewis, J. Cheng, V. Ramshesh, G. Beeson, C. Beeson, R. Drake, A. Bielawska, J. Bielawski, Z.M. Szulc, B. Ogretmen, J. Norris, X. Liu, LCL124, a cationic analog of ceramide, selectively induces pancreatic cancer cell death by accumulating in mitochondria, J. Pharmacol. Exp. Ther. 341 (2013) 167-178.
44. L.B. Chen, Mitochondrial membrane potential in living cells, Annu. Rev. Cell Biol. 4 (1988) 155-181. (Pubitemid 19139255)
45. A. Bras, J.P. Albar, E. Leonardo, G.G. de Buitrago, A.C. Martinez, Ceramide-induced cell death is independent of the Fas/Fas ligand pathway and is prevented by Nur77 overexpression in A20 B cells, Cell Death Differ. 7 (2000) 262-271. (Pubitemid 30192975)
46. D. Dindo, F. Dahm, Z. Szulc, A. Bielawska, L.M. Obeid, Y.A. Hannun, R. Graf, P.-A. Clavien, Cationic long-chain ceramide LCL-30 induces cell death by mitochondrial targeting in SW403 cells, Mol. Cancer Ther. 5 (2006) 1520-151529.
47. D. Separovic, A. Kelekar, A.K. Nayak, A.L. Tarca, K. Hanada, J.S. Pierce, J. Bielawski, Increased ceramide accumulation correlates with downregulation of the autophagy protein ATG-7 in MCF-7 cells sensitized to photodamage, Arch. Biochem. Biophys. 494 (2010) 101-105.