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International Journal of Photoenergy
Volume 2011, Article ID 713726, 11 pages
http://dx.doi.org/10.1155/2011/713726
Review Article

Overview of Cell Death Mechanisms Induced by Rose Bengal Acetate-Photodynamic Therapy

Department of Biological and Environmental Science and Technology (Di.S.Te.B.A.), University of Salento, 73100 Lecce, Italy

Received 7 July 2011; Accepted 5 September 2011

Academic Editor: Peter Robertson

Copyright © 2011 Elisa Panzarini et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Hanahan and R. A. Weinberg, “The hallmarks of cancer,” Cell, vol. 100, no. 1, pp. 57–70, 2000. View at Google Scholar · View at Scopus
  2. G. P. Dunn, A. T. Bruce, H. Ikeda, L. J. Old, and R. D. Schreiber, “Cancer immunoediting: from immunosurveillance to tumor escape,” Nature Immunology, vol. 3, no. 11, pp. 991–998, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  3. K. Plaetzer, B. Krammer, J. Berlanda, F. Berr, and T. Kiesslich, “Photophysics and photochemistry of photodynamic therapy: fundamental aspects,” Lasers in Medical Science, vol. 24, no. 2, pp. 259–268, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. Z. Luksiene, “Photodynamic therapy: mechanism of action and ways to improve the efficiency of treatment,” Medicina (Kaunas, Lithuania), vol. 39, no. 12, pp. 1137–1150, 2003. View at Google Scholar · View at Scopus
  5. R. L. Lipson and E. J. Baldes, “The photodynamic properties of a particular hematoporphyrin derivative,” Archives of Dermatology, vol. 82, no. 4, pp. 508–516, 1960. View at Google Scholar
  6. T. J. Dougherty, J. E. Kaufman, A. Goldfarb et al., “Photoradiation therapy for the treatment of malignant tumors,” Cancer Research, vol. 38, no. 8, pp. 2628–2635, 1978. View at Google Scholar · View at Scopus
  7. T. J. Dougherty, C. J. Gomer, B. W. Henderson et al., “Photodynamic therapy,” Journal of the National Cancer Institute, vol. 90, no. 12, pp. 889–905, 1998. View at Google Scholar · View at Scopus
  8. E. Buytaert, M. Dewaele, and P. Agostinis, “Molecular effectors of multiple cell death pathways initiated by photodynamic therapy,” Biochimica et Biophysica Acta, vol. 1776, no. 1, pp. 86–107, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. P. Castano, P. Mroz, and M. R. Hamblin, “Photodynamic therapy and anti-tumour immunity,” Nature Reviews Cancer, vol. 6, no. 7, pp. 535–545, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. M. Korbelik, “PDT-associated host response and its role in the therapy outcome,” Lasers in Surgery and Medicine, vol. 38, no. 5, pp. 500–508, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. P. Castano, T. N. Demidova, and M. R. Hamblin, “Mechanisms in photodynamic therapy: part one—photosensitizers, photochemistry and cellular localization,” Photodiagnosis and Photodynamic Therapy, vol. 1, no. 4, pp. 279–293, 2004. View at Publisher · View at Google Scholar · View at Scopus
  12. M. R. Detty, S. L. Gibson, and S. J. Wagner, “Current clinical and preclinical photosensitizers for use in photodynamic therapy,” Journal of Medicinal Chemistry, vol. 47, no. 16, pp. 3897–3915, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  13. R. M. Szeimies, S. Karrer, C. Abels et al., “9-acetoxy-2,7,12,17-tetrakis-(β-methoxyethyl)-porphycene(ATMPn), a novel photosensitizer for photodynamic therapy: uptake kinetics and intracellular localization,” Journal of Photochemistry and Photobiology B: Biology, vol. 34, no. 1, pp. 67–72, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. V. Král, J. Davis, A. Andrievsky et al., “Synthesis and biolocalization of water-soluble sapphyrins,” Journal of Medicinal Chemistry, vol. 45, no. 5, pp. 1073–1078, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Agostinis, A. Vantieghem, W. Merlevede, and P. A. M. de Witte, “Hypericin in cancer treatment: more light on the way,” International Journal of Biochemistry and Cell Biology, vol. 34, no. 3, pp. 221–241, 2002. View at Publisher · View at Google Scholar · View at Scopus
  16. J. C. Stockert, A. Juarranz, A. Villanueva, and M. Cañete, “Photodynamic damage to HeLa cell microtubules induced by thiazine dyes,” Cancer Chemotherapy and Pharmacology, vol. 39, no. 1-2, pp. 167–169, 1996. View at Publisher · View at Google Scholar · View at Scopus
  17. G. Bottiroli, A. C. Croce, P. Balzarini et al., “Enzyme-assisted cell photosensitization: a proposal for an efficient approach to tumor therapy and diagnosis. The Rose Bengal fluorogenic substrate,” Photochemistry and Photobiology, vol. 66, no. 3, pp. 374–383, 1997. View at Google Scholar · View at Scopus
  18. L. Brancaleon and H. Moseley, “Laser and non-laser light sources for photodynamic therapy,” Lasers in Medical Science, vol. 17, no. 3, pp. 173–186, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. B. W. Henderson and T. J. Dougherty, “How does photodynamic therapy work?” Photochemistry and Photobiology, vol. 55, no. 1, pp. 145–157, 1992. View at Google Scholar · View at Scopus
  20. A. Greer, “Christopher Foote's discovery of the role of singlet oxygen [ o12(Δ1g)] in photosensitized oxidation reactions,” Accounts of Chemical Research, vol. 39, no. 11, pp. 797–804, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  21. K. J. Davies, “Oxidative stress: the paradox of aerobic life,” Biochemical Society Symposium, vol. 61, pp. 1–31, 1995. View at Google Scholar · View at Scopus
  22. M. Sundaresan, Z. X. Yu, V. J. Ferrans, K. Irani, and T. Finkel, “Requirement for generation of H2O2 for platelet-derived growth factor signal transduction,” Science, vol. 270, no. 5234, pp. 296–299, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Demple and L. Harrison, “Repair of oxidative damage to DNA: enzymology and biology,” Annual Review of Biochemistry, vol. 63, pp. 915–948, 1994. View at Google Scholar · View at Scopus
  24. J. Fang, T. Seki, and H. Maeda, “Therapeutic strategies by modulating oxygen stress in cancer and inflammation,” Advanced Drug Delivery Reviews, vol. 61, no. 4, pp. 290–302, 2009. View at Publisher · View at Google Scholar · View at PubMed
  25. J. Paczkowski, J. J. M. Lamberts, B. Paczkowska, and D. C. Neckers, “Photophysical properties of Rose Bengal and its derivatives (XII),” Journal of Free Radicals in Biology and Medicine, vol. 1, no. 5-6, pp. 341–351, 1985. View at Google Scholar
  26. D. C. Neckers, “Rose Bengal,” Journal of Photochemistry and Photobiology, vol. 47, no. 1, pp. 1–29, 1989. View at Google Scholar
  27. I. E. Kochevar, C. R. Lambert, M. C. Lynch, and A. C. Tedesco, “Comparison of photosensitized plasma membrane damage caused by singlet oxygen and free radicals,” Biochimica et Biophysica Acta, vol. 1280, no. 2, pp. 223–230, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. P. C. Lee and M. A. J. Rodgers, “Laser flash photokinetic studies of Rose Bengal sensitized photodynamic interactions of nucleotides and DNA,” Photochemistry and Photobiology, vol. 45, no. 1, pp. 79–86, 1987. View at Google Scholar · View at Scopus
  29. N. Houba-Herin, C. M. Calberg-Bacq, J. Piette, and A. van de Vorst, “Mechanisms for dye-mediated photodynamic action: singlet oxygen production, deoxyguanosine oxidation and phage inactivating efficiencies,” Photochemistry and Photobiology, vol. 36, no. 3, pp. 297–306, 1982. View at Google Scholar · View at Scopus
  30. J. Lenard, A. Rabson, and R. Vanderoef, “Photodynamic inactivation of infectivity of human immunodeficiency virus and other enveloped viruses using hypericin and Rose Bengal: inhibition of fusion and syncytia formation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 1, pp. 158–162, 1993. View at Publisher · View at Google Scholar · View at Scopus
  31. J. Chodosh, M. C. Banks, and W. G. Stroop, “Rose Bengal inhibits herpes simplex virus replication in vero and human corneal epithelial cells in vitro,” Investigative Ophthalmology and Visual Science, vol. 33, no. 8, pp. 2520–2527, 1992. View at Google Scholar · View at Scopus
  32. T. A. Dahl, W. R. Midden, and D. C. Neckers, “Comparison of photodynamic action by Rose Bengal in gram-positive and gram-negative bacteria,” Photochemistry and Photobiology, vol. 48, no. 5, pp. 607–612, 1988. View at Google Scholar · View at Scopus
  33. F. S. Cruz, L. A. Lopes, and W. de Souza, “The photodynamic action of Rose Bengal on Trypanosoma cruzi,” Acta Tropica, vol. 41, no. 2, pp. 99–108, 1984. View at Google Scholar · View at Scopus
  34. D. P. Valenzeno and J. P. Pooler, “Cell membrane photomodification: relative effectiveness of halogenated fluoresceins for photohemolysis,” Photochemistry and Photobiology, vol. 35, no. 3, pp. 343–350, 1982. View at Google Scholar · View at Scopus
  35. L. ver Donck, J. van Reempts, G. Vandeplassche, and M. Borgers, “A new method to study activated oxygen species induced damage in cardiomyocytes and protection by Ca2+-antagonists,” Journal of Molecular and Cellular Cardiology, vol. 20, no. 9, pp. 811–823, 1988. View at Google Scholar · View at Scopus
  36. I. A. Menon, P. K. Basu, S. D. Persad, S. Rosatone, and J. D. Wiltshire, “A study on the sequence of phototoxic effects of Rose Bengal using retinal pigment epithelial cells in vitro,” Experimental Eye Research, vol. 49, no. 1, pp. 67–73, 1989. View at Google Scholar · View at Scopus
  37. J. P. Pooler and D. P. Valenzeno, “Kinetic factors governing sensitized photooxidation of excitable cell membranes,” Photochemistry and Photobiology, vol. 28, no. 2, pp. 219–226, 1978. View at Google Scholar · View at Scopus
  38. D. S. Hull, E. C. Strickland, and K. Green, “Photodynamically induced alteration of cornea endothelial cell function,” Investigative Ophthalmology and Visual Science, vol. 18, no. 12, pp. 1226–1231, 1979. View at Google Scholar · View at Scopus
  39. D. J. Hearse, Y. Kusama, and M. Bernier, “Rapid electrophysiological changes leading to arrhythmias in the aerobic rat heart. Photosensitization studies with Rose Bengal-derived reactive oxygen intermediates,” Circulation Research, vol. 65, no. 1, pp. 146–153, 1989. View at Google Scholar · View at Scopus
  40. E. K. Matthews and Z. J. Cui, “Photodynamic action of Rose Bengal on isolated rat pancreatic acini: stimulation of amylase release,” FEBS Letters, vol. 256, no. 1-2, pp. 29–32, 1989. View at Publisher · View at Google Scholar · View at Scopus
  41. A. C. Croce, E. Wyroba, and G. Bottiroli, “Distribution and retention of Rose Bengal and disulphonated aluminium phthalocyanine: a comparative study in unicellular eukaryote,” Journal of Photochemistry and Photobiology, vol. 16, no. 3-4, pp. 318–330, 1992. View at Google Scholar · View at Scopus
  42. D. K. Luttrull, O. Valdes-Aguilera, S. M. Linden, J. Paczkowski, and D. C. Neckers, “Rose Bengal aggregation in rationally synthesized dimeric systems,” Photochemistry and Photobiology, vol. 47, no. 4, pp. 551–557, 1988. View at Google Scholar · View at Scopus
  43. G. Bottiroli, A. C. Croce, P. Baglioni et al., “Fluorogenic substrates for diagnosis and photodynamic treatment of tumors,” 2000, US Patent 6036941. View at Google Scholar
  44. G. Bottiroli, A. C. Croce, M. Biggiogera et al., “Photosensitizer damage targets in Rose Bengal acetate treated cells,” Lasers in Surgery and Medicine, no. 173, pp. 13–41, 2001. View at Google Scholar
  45. A. C. Croce, D. Locatelli, M. Monici et al., “Application of Xuorogenic substrates to photodynamic therapy: Rose Bengal acetate,” Lasers in Surgery and Medicine, no. 121, pp. 9–26, 1997. View at Google Scholar
  46. A. C. Croce, R. Supino, K. S. Lanza, D. Locatelli, P. Baglioni, and G. Bottiroli, “Photosensitizer accumulation in spontaneous multidrug resistant cells: a comparative study with Rhodamine 123, Rose Bengal acetate and Photofrin,” Photochemical and Photobiological Sciences, vol. 1, no. 1, pp. 71–78, 2002. View at Publisher · View at Google Scholar
  47. C. Soldani, M. G. Bottone, A. C. Croce, A. Fraschini, G. Bottiroli, and C. Pellicciari, “The Golgi apparatus is a primary site of intracellular damage after photosensitization with Rose Bengal acetate,” European Journal of Histochemistry, vol. 48, no. 4, pp. 443–448, 2004. View at Google Scholar
  48. C. Soldani, M. G. Bottone, A. C. Croce et al., “Apoptosis in tumour cells photosensitized with Rose Bengal acetate is induced by multiple organelle photodamage,” Histochemistry and Cell Biology, vol. 128, no. 5, pp. 485–495, 2007. View at Publisher · View at Google Scholar · View at PubMed
  49. N. L. Oleinick and H. H. Evans, “The photobiology of photodynamic therapy: cellular targets and mechanisms,” Radiation Research, vol. 150, supplement 5, pp. S146–S156, 1998. View at Google Scholar
  50. N. N. Danial and S. J. Korsmeyer, “Cell death: critical control points,” Cell, vol. 116, no. 2, pp. 205–219, 2004. View at Publisher · View at Google Scholar
  51. G. Häcker, “The morphology of apoptosis,” Cell and Tissue Research, vol. 301, no. 1, pp. 5–17, 2000. View at Google Scholar
  52. M. O. Hengartner, “The biochemistry of apoptosis,” Nature, vol. 407, no. 6805, pp. 770–776, 2000. View at Publisher · View at Google Scholar · View at PubMed
  53. D. W. Nicholson, “Caspase structure, proteolytic substrates, and function during apoptotic cell death,” Cell Death and Differentiation, vol. 6, no. 11, pp. 1028–1042, 1999. View at Google Scholar
  54. I. N. Lavrik, A. Golks, and P. H. Krammer, “Caspase: pharmacological manipulation of cell death,” Journal of Clinical Investigation, vol. 115, no. 10, pp. 2665–2672, 2005. View at Publisher · View at Google Scholar · View at PubMed
  55. M. G. Bottone, C. Soldani, A. Fraschini et al., “Enzyme-assisted photosensitization with Rose Bengal acetate induces structural and functional alteration of mitochondria in HeLa cells,” Histochemistry and Cell Biology, vol. 127, no. 3, pp. 263–271, 2007. View at Publisher · View at Google Scholar · View at PubMed
  56. M. G. Bottone, C. Soldani, A. Fraschini et al., “Enzyme-assisted photosensitization activates different apoptotic pathways in Rose Bengal acetate treated HeLa cells,” Histochemistry and Cell Biology, vol. 131, no. 3, pp. 391–399, 2009. View at Publisher · View at Google Scholar · View at PubMed
  57. E. Panzarini, B. Tenuzzo, F. Palazzo, A. Chionna, and L. Dini, “Apoptosis induction and mitochondria alteration in human HeLa tumour cells by photoproducts of Rose Bengal acetate,” Journal of Photochemistry and Photobiology B, vol. 83, no. 1, pp. 39–47, 2006. View at Publisher · View at Google Scholar · View at PubMed
  58. Y. Chicheportiche, P. R. Bourdon, H. Xu et al., “TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis,” Journal of Biological Chemistry, vol. 272, no. 51, pp. 32401–32410, 1997. View at Publisher · View at Google Scholar
  59. A. Ashkenazi and V. M. Dixit, “Death receptors: signaling and modulation,” Science, vol. 281, no. 5381, pp. 1305–1308, 1998. View at Google Scholar
  60. M. E. Peter and P. H. Krammer, “Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis,” Current Opinion in Immunology, vol. 10, no. 5, pp. 545–551, 1998. View at Publisher · View at Google Scholar
  61. A. Suliman, A. Lam, R. Datta, and R. K. Srivastava, “Intracellular mechanisms of TRAIL: apoptosis through mitochondrial-dependent and -independent pathways,” Oncogene, vol. 20, no. 17, pp. 2122–2133, 2001. View at Publisher · View at Google Scholar · View at PubMed
  62. F. Rubio-Moscardo, D. Blesa, C. Mestre et al., “Characterization of 8p21.3 chromosomal deletions in B-cell lymphoma: TRAIL-R1 and TRAIL-R2 as candidate dosage-dependent tumor suppressor genes,” Blood, vol. 106, no. 9, pp. 3214–3222, 2005. View at Publisher · View at Google Scholar · View at PubMed
  63. T. Nakagawa, H. Zhu, N. Morishima et al., “Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β,” Nature, vol. 403, no. 6765, pp. 98–103, 2000. View at Publisher · View at Google Scholar · View at PubMed
  64. N. Morishima, K. Nakanishi, H. Takenouchi, T. Shibata, and Y. Yasuhiko, “An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12,” Journal of Biological Chemistry, vol. 277, no. 37, pp. 34287–34294, 2002. View at Publisher · View at Google Scholar · View at PubMed
  65. R. V. Rao, A. Peel, A. Logvinova et al., “Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78,” FEBS Letters, vol. 514, no. 2-3, pp. 122–128, 2002. View at Publisher · View at Google Scholar
  66. F. W. Ng, M. Nguyen, T. Kwan et al., “p28 Bap31, a Bcl-2/Bcl-X(L)- and procaspase-8-associated protein in the endoplasmic reticulum,” Journal of Cell Biology, vol. 139, no. 2, pp. 327–338, 1997. View at Publisher · View at Google Scholar
  67. S. A. Susin, E. Daugas, L. Ravagnan et al., “Two distinct pathways leading to nuclear apoptosis,” Journal of Experimental Medicine, vol. 192, no. 4, pp. 571–580, 2000. View at Publisher · View at Google Scholar
  68. L. Y. Li, X. Luo, and X. Wang, “Endonuclease G is an apoptotic DNase when released from mitochondria,” Nature, vol. 412, no. 6842, pp. 95–99, 2001. View at Publisher · View at Google Scholar · View at PubMed
  69. A. Burlacu, “Regulation of apoptosis by Bcl-2 family proteins,” Journal of Cellular and Molecular Medicine, vol. 7, no. 3, pp. 249–257, 2003. View at Google Scholar
  70. T. Möröy and M. Zörnig, “Regulators of life and death: the Bcl-2 gene family,” Cellular Physiology and Biochemistry, vol. 6, no. 6, pp. 312–336, 1996. View at Google Scholar
  71. Y. Tsujimoto, “Cell death regulation by the Bcl-2 protein family in the mitochondria,” Journal of Cellular Physiology, vol. 195, no. 2, pp. 158–167, 2003. View at Publisher · View at Google Scholar · View at PubMed
  72. B. Leber, J. Lin, and D. W. Andrews, “Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes,” Apoptosis, vol. 12, no. 5, pp. 897–911, 2007. View at Publisher · View at Google Scholar · View at PubMed
  73. H. Puthalakath and A. Strasser, “Keeping killers on a tight leash: transcriptional and post-translational control of the pro-apoptotic activity of BH3-only proteins,” Cell Death and Differentiation, vol. 9, no. 5, pp. 505–512, 2002. View at Publisher · View at Google Scholar · View at PubMed
  74. C. Martinou and D. R. Green, “Breaking the mitochondrial barrier,” Nature Reviews Molecular Cell Biology, vol. 2, no. 1, pp. 63–67, 2001. View at Publisher · View at Google Scholar · View at PubMed
  75. M. J. Berridge, P. Lipp, and M. D. Bootman, “The versatility and universality of calcium signalling,” Nature Reviews Molecular Cell Biology, vol. 1, no. 1, pp. 11–21, 2000. View at Google Scholar
  76. R. Rizzuto, M. Brini, M. Murgia, and T. Pozzan, “Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria,” Science, vol. 262, no. 5134, pp. 744–747, 1993. View at Google Scholar
  77. M. P. Mattson and S. L. Chan, “Calcium orchestrates apoptosis,” Nature Cell Biology, vol. 5, no. 12, pp. 1041–1043, 2003. View at Publisher · View at Google Scholar · View at PubMed
  78. S. Shimizu, M. Narita, and Y. Tsujimoto, “Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC,” Nature, vol. 399, no. 6735, pp. 483–487, 1999. View at Publisher · View at Google Scholar · View at PubMed
  79. E. Panzarini, V. Inguscio, and L. Dini, “Timing the multiple cell death pathways initiated by Rose Bengal acetate photodynamic therapy,” Cell Death and Disease, vol. 2, no. 6, article e169, 2011. View at Publisher · View at Google Scholar · View at PubMed
  80. E. Panzarini, B. Tenuzzo, and L. Dini, “Photodynamic therapy-induced apoptosis of HeLa cells,” Annals of the New York Academy of Sciences, vol. 1171, pp. 617–626, 2009. View at Publisher · View at Google Scholar · View at PubMed
  81. D. R. Green and G. Kroemer, “The pathophysiology of mitochondrial cell death,” Science, vol. 305, no. 5684, pp. 626–629, 2004. View at Publisher · View at Google Scholar · View at PubMed
  82. N. Demaurex and C. Distelhorst, “Cell biology: apoptosis—the calcium connection,” Science, vol. 300, no. 5616, pp. 65–67, 2003. View at Publisher · View at Google Scholar · View at PubMed
  83. T. Finkel and N. J. Holbrook, “Oxidants, oxidative stress and the biology of ageing,” Nature, vol. 408, no. 6809, pp. 239–247, 2000. View at Publisher · View at Google Scholar · View at PubMed
  84. L. Sun, T. Chen, X. Wang, Y. Chen, and X. Wei, “Bufalin induces reactive oxygen species dependent Bax translocation and apoptosis in ASTC-a-1 Cells,” Evidence-Based Complementary and Alternative Medicine, vol. 2011, 12 pages, 2011. View at Publisher · View at Google Scholar · View at PubMed
  85. S. Zhuang and I. E. Kochevar, “Ultraviolet a radiation induces rapid apoptosis of human leukemia cells by fas ligand-independent activation of the fas death pathway,” Photochemistry and Photobiology, vol. 78, no. 1, pp. 61–67, 2003. View at Publisher · View at Google Scholar
  86. G. Kroemer, L. Galluzzi, P. Vandenabeele et al., “Classification of cell death: recommendations of the nomenclature committee on cell death 2009,” Cell Death and Differentiation, vol. 16, no. 1, pp. 3–11, 2009. View at Publisher · View at Google Scholar · View at PubMed
  87. D. J. Klionsky, A. M. Cuervo, and P. O. Seglen, “Methods for monitoring autophagy from yeast to human,” Autophagy, vol. 3, no. 3, pp. 181–206, 2007. View at Google Scholar
  88. D. J. Klionsky, H. Abeliovich, P. Agostinis et al., “Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes,” Autophagy, vol. 4, no. 2, pp. 151–175, 2008. View at Google Scholar
  89. E. L. Axe, S. A. Walker, M. Manifava et al., “Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum,” Journal of Cell Biology, vol. 182, no. 4, pp. 685–701, 2008. View at Publisher · View at Google Scholar · View at PubMed
  90. A. Simonsen and S. A. Tooze, “Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes,” Journal of Cell Biology, vol. 186, no. 6, pp. 773–782, 2009. View at Publisher · View at Google Scholar · View at PubMed
  91. N. Mizushima, “Autophagy: process and function,” Genes and Development, vol. 21, no. 22, pp. 2861–2873, 2007. View at Publisher · View at Google Scholar · View at PubMed
  92. M. Fengsrud, M. L. Sneve, A. Overbye et al., “Structural aspects of mammalian autophagy,” in Autophagy, D. Klionsky, Ed., pp. 11–25, Landes Bioscience, Georgetown, Tex, USA, 2004. View at Google Scholar
  93. P. Codogno and A. J. Meijer, “Signaling pathways in mammalian autophagy,” in Autophagy, D. Klionsky, Ed., pp. 26–47, Landes Bioscience, Georgetown, Tex, USA, 2004. View at Google Scholar
  94. C. W. Wang and D. L. Klionsky, “Microautophagy,” in Autophagy, D. Klionsky, Ed., pp. 107–125, Landes Bioscience, Georgetown, Tex, USA, 2004. View at Google Scholar
  95. P. Saftig, W. Beertsen, and E. L. Eskelinen, “LAMP-2: a control step fot phagosome and autophagosome maturation,” Autophagy, vol. 4, no. 4, pp. 510–512, 2008. View at Google Scholar
  96. W. Bursch, A. Karwan, M. Mayer et al., “Cell death and autophagy: cytokines, drugs, and nutritional factors,” Toxicology, vol. 254, no. 3, pp. 147–157, 2008. View at Publisher · View at Google Scholar · View at PubMed
  97. D. Kessel and N. L. Oleinick, “Initiation of autophagy by photodynamic therapy,” Methods in Enzymology, vol. 453, pp. 1–16, 2009. View at Publisher · View at Google Scholar
  98. M. Dewaele, W. Martinet, N. Rubio et al., “Autophagy pathways activated in response to PDT contribute to cell resistance against ROS damage,” Journal of Cellular and Molecular Medicine, vol. 15, no. 6, pp. 1402–1414, 2011. View at Publisher · View at Google Scholar · View at PubMed
  99. R. Scherz-Shouval and Z. Elazar, “ROS, mitochondria and the regulation of autophagy,” Trends in Cell Biology, vol. 17, no. 9, pp. 422–427, 2007. View at Publisher · View at Google Scholar · View at PubMed
  100. L. Dini, V. Inguscio, B. Tenuzzo, and E. Panzarini, “Rose Bengal acetate photodynamic therapy-induced autophagy,” Cancer Biology and Therapy, vol. 10, no. 10, pp. 1048–1055, 2010. View at Publisher · View at Google Scholar · View at PubMed
  101. J. J. Reiners Jr, P. Agostinis, K. Berg, N. L. Oleinick, and D. Kessel, “Assessing autophagy in the context of photodynamic therapy,” Autophagy, vol. 6, no. 1, pp. 7–18, 2010. View at Publisher · View at Google Scholar
  102. D. Kessel, “Protection of Bcl-2 by salubrinal,” Biochemical and Biophysical Research Communications, vol. 346, no. 4, pp. 1320–1323, 2006. View at Publisher · View at Google Scholar · View at PubMed
  103. D. Kessel, M. G. Vicente, and J. J. Reiners Jr, “Initiation of apoptosis and autophagy by photodynamic therapy,” Lasers in Surgery and Medicine, vol. 38, no. 5, pp. 482–488, 2006. View at Publisher · View at Google Scholar · View at PubMed
  104. P. Golstein and G. Kroemer, “Cell death by necrosis: towards a molecular definition,” Trends in Biochemical Sciences, vol. 32, no. 1, pp. 37–43, 2007. View at Publisher · View at Google Scholar · View at PubMed
  105. N. Festjens, T. V. Berghe, and P. Vandenabeele, “Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response,” Biochimica et Biophysica Acta, vol. 1757, no. 9-10, pp. 1371–1387, 2006. View at Publisher · View at Google Scholar · View at PubMed
  106. E. Wachter, C. Dees, J. Harkins et al., “Topical Rose Bengal: pre-clinical evaluation of pharmacokinetics and safety,” Lasers in Surgery and Medicine, vol. 32, no. 2, pp. 101–110, 2003. View at Publisher · View at Google Scholar · View at PubMed