Tumor PDT-associated immune response: relevance of sphingolipids

Sphingolipids have become recognized as essential effector molecules in signal transduction with involvement in various aspects of cell function and death, immune response and cancer treatment response. Major representatives of sphingolipids family, ceramide, sphingosine and sphingosine-1-phosphate (S1P), have attracted interest in their relevance to tumor response to photodynamic therapy (PDT) because of their roles as enhancers of apoptosis, mediators of cell growth and vasculogenesis, and regulators of immune response. Our recent in vivo studies with mouse tumor models have confirmed that PDT treatment has a pronounced impact on sphingolipid profile in the targeted tumor and that significant advances in therapeutic gain with PDT can be attained by combining this modality with adjuvant treatment with ceramide analog LCL29.

[1]  R. Proia,et al.  S1P1 receptor overrides regulatory T cell-mediated immune suppression through Akt-mTOR , 2009, Nature Immunology.

[2]  Y. Liu,et al.  N-(4-Hydroxyphenyl)retinamide increases dihydroceramide and synergizes with dimethylsphingosine to enhance cancer cell killing , 2008, Molecular Cancer Therapeutics.

[3]  M. Tainsky,et al.  De Novo Ceramide Accumulation Due to Inhibition of Its Conversion to Complex Sphingolipids in Apoptotic Photosensitized Cells* , 2004, Journal of Biological Chemistry.

[4]  H. Mukhtar,et al.  Phthalocyanine 4-photodynamic therapy induces ceramide generation and apoptosis in acid sphingomyelinase-deficient mouse embryonic fibroblasts. , 2000, International journal of oncology.

[5]  M. Korbelik,et al.  Photodynamic therapy-generated vaccines: relevance of tumour cell death expression , 2007, British Journal of Cancer.

[6]  Nancy L Oleinick,et al.  The role of apoptosis in response to photodynamic therapy: what, where, why, and how , 2002, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[7]  S. Spiegel,et al.  Sphingolipid metabolism and cell growth regulation , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[8]  B. Taffe,et al.  Reactive oxygen species generation is independent of de novo sphingolipids in apoptotic photosensitized cells. , 2003, Experimental cell research.

[9]  M. Korbelik,et al.  Induction of tumor immunity by photodynamic therapy. , 1996, Journal of clinical laser medicine & surgery.

[10]  P. V. Van Veldhoven,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 , 2007, Molecular Cancer Research.

[11]  Zheng Huang,et al.  A Review of Progress in Clinical Photodynamic Therapy , 2005, Technology in cancer research & treatment.

[12]  M. Korbelik,et al.  Increased tumour dihydroceramide production after Photofrin-PDT alone and improved tumour response after the combination with the ceramide analogue LCL29. Evidence from mouse squamous cell carcinomas , 2009, British Journal of Cancer.

[13]  T. Uchiyama,et al.  Possible role of ceramide as an indicator of chemoresistance: decrease of the ceramide content via activation of glucosylceramide synthase and sphingomyelin synthase in chemoresistant leukemia. , 2003, Clinical cancer research : an official journal of the American Association for Cancer Research.

[14]  S. Gatt,et al.  Caspase-dependent and -independent cell death of Jurkat human leukemia cells induced by novel synthetic ceramide analogs , 2006, Leukemia.

[15]  D. Boothman,et al.  Niemann-Pick human lymphoblasts are resistant to phthalocyanine 4-photodynamic therapy-induced apoptosis. , 1999, Biochemical and biophysical research communications.

[16]  A. Bielawska,et al.  The ceramide analog, B13, induces apoptosis in prostate cancer cell lines and inhibits tumor growth in prostate cancer xenografts , 2004, The Prostate.

[17]  P. Codogno,et al.  Is Autophagy the Key Mechanism by Which the Sphingolipid Rheostat Controls the Cell Fate Decision? , 2007, Autophagy.

[18]  M. Cabot,et al.  Increasing intracellular ceramide: an approach that enhances the cytotoxic response in prostate cancer cells. , 2003, Urology.

[19]  A. Haimovitz-Friedman,et al.  12-O-tetradecanoylphorbol-13-acetate-induced apoptosis in LNCaP cells is mediated through ceramide synthase. , 1998, Cancer research.

[20]  Y. Hannun,et al.  Serine Palmitoyltransferase Regulates de NovoCeramide Generation during Etoposide-induced Apoptosis* , 2000, The Journal of Biological Chemistry.

[21]  T. Dougherty,et al.  HOW DOES PHOTODYNAMIC THERAPY WORK? , 1992, Photochemistry and photobiology.

[22]  F. Scarlatti,et al.  The FASEB Journal express article 10.1096/fj.03-0292fje. Published online October 16, 2003. Resveratrol induces growth inhibition and apoptosis in metastatic breast cancer cells via de novo ceramide signaling , 2022 .

[23]  K. Hanada,et al.  A role for the de novo sphingolipids in apoptosis of photosensitized cells. , 2002, Experimental cell research.

[24]  Y. Hannun,et al.  Translational aspects of sphingolipid metabolism. , 2007, Trends in molecular medicine.

[25]  G. Velasco,et al.  De novo-synthesized ceramide is involved in cannabinoid-induced apoptosis. , 2002, The Biochemical journal.

[26]  C. Riccardi,et al.  Sphingolipids and the immune system. , 2003, Pharmacological research.

[27]  M. Cabot,et al.  Ceramides and other bioactive sphingolipid backbones in health and disease: lipidomic analysis, metabolism and roles in membrane structure, dynamics, signaling and autophagy. , 2006, Biochimica et biophysica acta.

[28]  H. Rüdiger,et al.  Induction of apoptotic cell death and prevention of tumor growth by ceramide analogues in metastatic human colon cancer. , 2001, Cancer research.

[29]  N. Oleinick,et al.  Association of Ceramide Accumulation with Photodynamic Treatment‐Induced Cell Death , 1998, Photochemistry and photobiology.

[30]  A. Giuliano,et al.  Taxol-induced ceramide generation and apoptosis in human breast cancer cells , 2001, Cancer Chemotherapy and Pharmacology.

[31]  Y. Hannun,et al.  Defects in Cell Growth Regulation by C18:0-Ceramide and Longevity Assurance Gene 1 in Human Head and Neck Squamous Cell Carcinomas* , 2004, Journal of Biological Chemistry.

[32]  S. Ben-Dor,et al.  When Do Lasses (Longevity Assurance Genes) Become CerS (Ceramide Synthases)? , 2006, Journal of Biological Chemistry.

[33]  A. Tarca,et al.  Suppression of sphingomyelin synthase 1 by small interference RNA is associated with enhanced ceramide production and apoptosis after photodamage. , 2008, Experimental cell research.

[34]  Y. Hannun,et al.  Functions of sphingolipids and sphingolipid breakdown products in cellular regulation. , 1989, Science.

[35]  Y. Hannun,et al.  Enzymes of sphingolipid metabolism: from modular to integrative signaling. , 2001, Biochemistry.

[36]  Q. Peng,et al.  Photodynamic Therapy , 1988, Methods in Molecular Biology.

[37]  H. Bonkovsky,et al.  Vascular Endothelium As a Contributor of Plasma Sphingosine 1-Phosphate , 2008, Circulation research.

[38]  Mladen Korbelik,et al.  PDT‐associated host response and its role in the therapy outcome , 2006, Lasers in surgery and medicine.

[39]  S. Ladisch,et al.  Glucosylceramide synthase inhibition enhances vincristine‐induced cytotoxicity , 2001, International journal of cancer.

[40]  S. Groshen,et al.  Ceramide Signaling in Fenretinide-induced Endothelial Cell Apoptosis* , 2002, The Journal of Biological Chemistry.

[41]  M. Cabot,et al.  Glucosylceramide synthase and apoptosis. , 2002, Biochimica et biophysica acta.

[42]  A. Giuliano,et al.  Multidrug resistance modulators and doxorubicin synergize to elevate ceramide levels and elicit apoptosis in drug‐resistant cancer cells , 1999, Cancer.

[43]  D. Separovic,et al.  Ceramide generation in response to photodynamic treatment of L5178Y mouse lymphoma cells. , 1997, Cancer research.

[44]  Yusuf A. Hannun,et al.  Biologically active sphingolipids in cancer pathogenesis and treatment , 2004, Nature Reviews Cancer.

[45]  A. Bielawska,et al.  Potent Antitumor 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 , 2006, Journal of Pharmacology and Experimental Therapeutics.

[46]  A. Bielawska,et al.  Mitochondrially targeted ceramide LCL-30 inhibits colorectal cancer in mice , 2007, British Journal of Cancer.

[47]  Y. Hannun,et al.  Sphingomyelin turnover induced by vitamin D3 in HL-60 cells. Role in cell differentiation. , 1989, The Journal of biological chemistry.

[48]  R. Kolesnick,et al.  Sphingolipids as therapeutics. , 2003, Pharmacological research.

[49]  Sarah Spiegel,et al.  Cross-talk at the crossroads of sphingosine-1-phosphate, growth factors, and cytokine signaling. , 2008, Journal of lipid research.

[50]  Sarah Spiegel,et al.  Sphingosine-1-phosphate: an enigmatic signalling lipid , 2003, Nature Reviews Molecular Cell Biology.

[51]  Chuannong Zhou,et al.  Mechanisms of tumor destruction caused by photodynamic therapy , 2005, Shanghai International Conference on Laser Medicine and Surgery.

[52]  S. Chiu,et al.  Fumonisin B1 does not prevent apoptosis in A431 human epidermoid carcinoma cells after photosensitization with a silicon phthalocyanine. , 2000, Journal of photochemistry and photobiology. B, Biology.