Composite Conjugated Polymer/Fullerene Nanoparticles as Sensitizers in Photodynamic Therapy for Cancer

BioNanoScience

Volumn 4, Issue 1, 2014, Pages 15-26

  Doshi, Mona ^a   Treglown, Kirsten ^a   Copik, Alicja ^b   Gesquiere, Andre J ^a  

^a UNIVERSITY OF CENTRAL FLORIDA   (United States)

^b UNIVERSITY OF CENTRAL FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Apoptosis; Conducting polymer; Oxidative stress; Reactive oxygen species; ROS; Tumor

Indexed keywords

CELL CULTURE; CELL DEATH; CELLS; CHARGE TRANSFER; CONDUCTING POLYMERS; CYTOLOGY; DISEASES; FULLERENES; NANOPARTICLES; OXIDATIVE STRESS; PHOTODYNAMIC THERAPY; TUMORS;

ABSORPTION CROSS SECTIONS; APOPTOTIC CELL DEATH; COMPOSITE NANOPARTICLES; NANOPARTICLE UPTAKES; PHOTODYNAMIC THERAPY (PDT); POLYMER NANOPARTICLES; REACTIVE OXYGEN SPECIES; ROS;

CONJUGATED POLYMERS;

CONJUGATED POLYMER; FULLERENE; NANOPARTICLE; PHOTOSENSITIZING AGENT; POLY 2 METHOXY 5 (2 ETHYLHEXYLOXY) 1,4 PHENYLENEVINYLENE; POLYMER; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BREAST CANCER; CELL COUNTING; CELL MEDIATED CYTOTOXICITY; CELL VIABILITY; CONTROLLED STUDY; FLOW CYTOMETRY; FLUORESCENCE IMAGING; FLUORESCENCE SPECTROSCOPY; HUMAN; HUMAN CELL; LIGHT SCATTERING; LUNG CANCER; MOUSE; MTT ASSAY; NEOPLASM; NONHUMAN; OVARY CANCER; PHOTODYNAMIC THERAPY; ULTRAVIOLET SPECTROSCOPY; ZETA POTENTIAL;

EID: 84926301694     PISSN: 21911630     EISSN: 21911649     Source Type: Journal    
DOI: 10.1007/s12668-013-0114-5     Document Type: Article

References (80)

1. Kumar, A., Cascarini, L., McCaul, J. A., Kerawala, C. J., Coombes, D., Godden, D., et al. (2013). How should we manage oral leukoplakia? British Journal of Oral and Maxillofacial Surgery, 51(5), 377–383. doi:10.1016/j.bjoms.2012.10.018.
2. Milovanovic, J., Djukic, V., Milovanovic, A., Jotic, A., Banko, B., Jesic, S., et al. (2013). Clinical outcome of early glottic carcinoma in Serbia. Auris, Nasus, Larynx, 40(4), 394–399. doi:10.1016/j.anl.2012.11.013.
3. Moore, E. J., & Hinni, M. L. (2013). Critical review: Transoral laser microsurgery and robotic-assisted surgery for oropharynx cancer including human papillomavirus-related cancer. International Journal of Radiation Oncology, Biology, and Physics, 85(5), 1163–1167. doi:10.1016/j.ijrobp.2012.08.033.
4. No, D., Osterberg, E. C., Otto, B., Naftali, I., Choi, B. (2013). Evaluation of continence following 532 nm laser prostatectomy for patients previously treated with radiation therapy or brachytherapy. Lasers in Surgery and Medicine, 45(6), 358–361. doi:10.1002/lsm.22152.
5. Rosch, T. (2012). Progress in endoscopy: areas of current interest and topics to watch out for. Endoscopy, 44(12), 1148–1157. doi:10.1055/s-0032-1325994.
6. Kalbasi, A., June, C. H., Haas, N., Vapiwala, N. (2013). Radiation and immunotherapy: a synergistic combination. Journal of Clinical Investigation, 123(7), 2756–2763. doi:10.1172/jci69219.
7. Suneja, G., Poorvu, P. D., Hill-Kayser, C., Lustig, R. A. (2013). Acute toxicity of proton beam radiation for pediatric central nervous system malignancies. Pediatric Blood & Cancer, 60(9), 1431–1436. doi:10.1002/pbc.24554.
8. Dent, S., Oyan, B., Honig, A., Mano, M., Howell, S. (2013). HER2-targeted therapy in breast cancer: a systematic review of neoadjuvant trials. Cancer Treatment Reviews, 39(6), 622–631. doi:10.1016/j.ctrv.2013.01.002.
9. Heinemann, V., Douillard, J. Y., Ducreux, M., Peeters, M. (2013). Targeted therapy in metastatic colorectal cancer—an example of personalised medicine in action. Cancer Treatment Reviews, 39(6), 592–601. doi:10.1016/j.ctrv.2012.12.011.
10. Verbrugghe, M., Verhaeghe, S., Lauwaert, K., Beeckman, D., Van Hecke, A. (2013). Determinants and associated factors influencing medication adherence and persistence to oral anticancer drugs: a systematic review. Cancer Treatment Reviews, 39(6), 610–621. doi:10.1016/j.ctrv.2012.12.014.
11. Mountzios, G., Soultati, A., Pectasides, D., Pectasides, E., Dimopoulos, M. A., Papadimitriou, C. A. (2013). Developments in the systemic treatment of metastatic cervical cancer. Cancer Treatment Reviews, 39(5), 430–443. doi:10.1016/j.ctrv.2012.05.009.
12. Droge, W. (2002). Free radicals in the physiological control of cell function. Physiological Reviews, 82(1), 47–95.
13. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. International Journal of Biochemistry & Cell Biology, 39(1), 44–84. doi:10.1016/j.biocel.2006.07.001.
14. Valko, M., Rhodes, C. J., Moncol, J., Izakovic, M., Mazur, M. (2006). Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-Biological Interactions, 160(1), 1–40. doi:10.1016/j.cbi.2005.12.009.
15. Wallace, D. C. (2005). A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: a dawn for evolutionary medicine. Annual Review of Genetics, 39, 359–407. doi:10.1146/annurev.genet.39.110304.095751.
16. Baynes, J. W., & Thorpe, S. R. (1999). Role of oxidative stress in diabetic complications—a new perspective on an old paradigm. Diabetes, 48(1), 1–9. doi:10.2337/diabetes.48.1.1.
17. Hensley, K., Robinson, K. A., Gabbita, S. P., Salsman, S., Floyd, R. A. (2000). Reactive oxygen species, cell signaling, and cell injury. Free Radical Biology and Medicine, 28(10), 1456–1462. doi:10.1016/S0891-5849(00)00252-5.
18. Zhou, H., Liu, X., Liu, L., Yang, Z., Zhang, S., Tang, M., et al. (2009). Oxidative stress and apoptosis of human brain microvascular endothelial cells induced by free fatty acids. Journal of International Medical Research, 37(6), 1897–1903.
19. Nogueira, V., Park, Y., Chen, C.-C., Xu, P.-Z., Chen, M.-L., Tonic, I., et al. (2008). Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell, 14(6), 458–470. doi:10.1016/j.ccr.2008.11.003.
20. Huang, P., Trachootham, D., Alexandre, J. (2009). Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nature Reviews Drug Discovery, 8(7), 579–591. doi:10.1038/nrd2803.
21. Huang, P., Trachootham, D., Zhou, Y., Zhang, H., Demizu, Y., Chen, Z., et al. (2006). Selective killing of oncogenically transformed cells through a ROS-mediated mechanism by beta-phenylethyl isothiocyanate. Cancer Cell, 10(3), 241–252. doi:10.1016/j.ccr.2006.08.009.
22. Konan, Y. N., Gurny, R., Allemann, E. (2002). State of the art in the delivery of photosensitizers for photodynamic therapy. Journal of Photochemistry and Photobiology B: Biology, 66(2), 89–106. doi:10.1016/s1011-1344(01)00267-6.
23. Luan, L., Ding, L., Zhang, W., Shi, J., Yu, X., Liu, W. (2013). A naphthalocyanine based near-infrared photosensitizer: synthesis and in vitro photodynamic activities. Bioorganic & Medicinal Chemistry Letters, 23(13), 3775–3779. doi:10.1016/j.bmcl.2013.04.093.
24. Lukyanets, E. A. (1999). Phthalocyanines as photosensitizers in the photodynamic therapy of cancer. Journal of Porphyrins Phthalocyanines, 3(6–7), 424–432. doi:10.1002/(Sici)1099-1409.
25. da Silva, A. R., Ribeiro, J. N., Rettori, D., Jorge, R. A. (2008). Type II photooxidation mechanism of biomolecules using chloro(5,10,15,20-tetraphenylporphyrinato)indium(II) as a photosensitizer. Journal of the Brazilian Chemical Society, 19(7), 1311–1320.
26. Dolmans, D. E. J. G. J., Fukumura, D., Jain, R. K. (2003). Photodynamic therapy for cancer. Nature Reviews Cancer, 3(5), 380–387. doi:10.1038/nrc1071.
27. Dougherty, T. J., Gomer, C. J., Henderson, B. W., Jori, G., Kessel, D., Korbelik, M., et al. (1998). Photodynamic therapy. Journal of the National Cancer Institute, 90(12), 889–905. doi:10.1093/jnci/90.12.889.
28. Kim, S., Ohulchanskyy, T. Y., Pudavar, H. E., Pandey, R. K., Prasad, P. N. (2007). Organically modified silica nanoparticles co-encapsulating photosensitizing drug and aggregation-enhanced two-photon absorbing fluorescent dye aggregates for two-photon photodynamic therapy. Journal of the American Chemical Society, 129(9), 2669–2675. doi:10.1021/ja0680257.
29. Shirasu, N., Nam, S. O., Kuroki, M. (2013). Tumor-targeted photodynamic therapy. Anticancer Research, 33(7), 2823–2831.
30. Lim, C.-K., Heo, J., Shin, S., Jeong, K., Seo, Y. H., Jang, W.-D., et al. (2013). Nanophotosensitizers toward advanced photodynamic therapy of cancer. Cancer Letters, 334(2), 176–187. doi:10.1016/j.canlet.2012.09.012.
31. Tian, G., Ren, W., Yan, L., Jian, S., Gu, Z., Zhou, L., et al. (2012). Red-emitting upconverting nanoparticles for photodynamic therapy in cancer cells under near-infrared excitation. Small, 9(11), 1929–1938. doi:10.1002/smll.201201437.
32. Bridot, J. L., Faure, A. C., Laurent, S., Riviere, C., Billotey, C., Hiba, B., et al. (2007). Hybrid gadolinium oxide nanoparticles: multimodal contrast agents for in vivo imaging. Journal of the American Chemical Society, 129(16), 5076–5084. doi:10.1021/ja068356j.
33. Cheon, J., & Lee, J. H. (2008). Synergistically integrated nanoparticles as multimodal probes for nanobiotechnology. Accounts Chemistry Research, 41(12), 1630–1640. doi:10.1021/ar800045c.
34. Kim, J., Piao, Y., Hyeon, T. (2009). Multifunctional nanostructured materials for multimodal imaging, and simultaneous imaging and therapy. Chemical Society Reviews, 38(2), 372–390. doi:10.1039/b709883a.
35. Mulder, W. J. M., Strijkers, G. J., Van Tilborg, G. A. F., Cormode, D. P., Fayad, Z. A., Nicolay, K. (2009). Nanoparticulate assemblies of amphiphiles and diagnostically active materials for multimodality imaging. Accounts Chemistry Research, 42(7), 904–914. doi:10.1021/ar800223c.
36. Chen, J.-Y., Lee, Y.-M., Zhao, D., Mak, N.-K., Wong, R. N.-S., Chan, W.-H., et al. (2010). Quantum dot-mediated photoproduction of reactive oxygen species for cancer cell annihilation. Photochemistry and Photobiology, 86(2), 431–437. doi:10.1111/j.1751-1097.2009.00652.x.
37. Chou, K. L., Meng, H., Cen, Y., Li, L., Chen, J. Y. (2013). Dopamine-quantum dot conjugate: a new kind of photosensitizers for photodynamic therapy of cancers. Journal of Nanoparticle Research, 15(1), 9. doi:10.1007/s11051-012-1348-9.
38. Ito, S., Miyoshi, N., Degraff, W. G., Nagashima, K., Kirschenbaum, L. J., Riesz, P. (2009). Enhancement of 5-aminolevulinic acid-induced oxidative stress on two cancer cell lines by gold nanoparticles. Free Radical Research, 43(12), 1214–1224. doi:10.3109/10715760903271249.
39. Xue, C., Wu, J., Lan, F., Liu, W., Yang, X., Zeng, F., et al. (2010). Nano titanium dioxide induces the generation of ROS and potential damage in HaCaT cells under UVA irradiation. Journal of Nanoscience and Nanotechnology, 10(12), 8500–8507. doi:10.1166/jnn.2010.2682.
40. Liu, L., Xiao, L., Cao, C. H. (2013). Novel magnetic-fluorescent CS-Fe3O4@ZnS:Mn/ZnS (core/shell) nanoparticles: preparation, characterization and damage to bovine serum albumin under UV irradiation. Materials Chemistry and Physics, 140(2–3), 575–582. doi:10.1016/j.matchemphys.2013.04.007.
41. 2 nanocomposites for magnetic resonance imaging and potential photodynamic therapy. Nanoscale, 5(5), 2107–2113. doi:10.1039/c3nr33978e.
42. Wang, F., Chen, X. L., Zhao, Z. X., Tang, S. H., Huang, X. Q., Lin, C. H., et al. (2011). Synthesis of magnetic, fluorescent and mesoporous core-shell-structured nanoparticles for imaging, targeting and photodynamic therapy. Journal of Materials Chemistry, 21(30), 11244–11252. doi:10.1039/c1jm10329f.
43. Perrier, M., Gary-Bobo, M., Lartigue, L., Brevet, D., Morere, A., Garcia, M., et al. (2013). Mannose-functionalized porous silica-coated magnetic nanoparticles for two-photon imaging or PDT of cancer cells. Journal of Nanoparticle Research, 15(5), 17. doi:10.1007/S11051-013-1602-9.
44. Huang, P., Lin, J., Wang, S., Zhou, Z., Li, Z., Wang, Z., et al. Photosensitizer-conjugated silica-coated gold nanoclusters for fluorescence imaging-guided photodynamic therapy. Biomaterials, 34(19), 4643–4654. doi: 10.1016/j.biomaterials.2013.02.063.
45. Ohulchanskyy, T. Y., Roy, I., Goswami, L. N., Chen, Y., Bergey, E. J., Pandey, R. K., et al. (2007). Organically modified silica nanoparticles with covalently incorporated photosensitizer for photodynamic therapy of cancer. Nano Letters, 7(9), 2835–2842. doi:10.1021/nl0714637.
46. Tao, X., Yang, Y. J., Liu, S., Zheng, Y. Z., Fu, J., Chen, J. F. (2013). Poly(amidoamine) dendrimer-grafted porous hollow silica nanoparticles for enhanced intracellular photodynamic therapy. Acta Biomaterialia, 9(5), 6431–6438. doi:10.1016/j.actbio.2013.01.028.
47. Cohen, BA., & Bergkvist, M. Targeted in vitro photodynamic therapy via aptamer-labeled, porphyrin-loaded virus capsids. Journal of Photochemistry and Photobiology B: Biology, 121, 67–74. doi:10.1016/j.jphotobiol.2013.02.013.
48. Ferreira, D. M., Saga, Y. Y., Aluicio-Sarduy, E., Tedesco, A. C. Chitosan nanoparticles for melanoma cancer treatment by photodynamic therapy and electrochemotherapy using aminolevulinic acid derivatives. Current Medicinal Chemistry, 20(14), 1904–1911.
49. Grimland, J. L., Wu, C., Ramoutar, R. R., Brumaghim, J. L., McNeill, J. Photosensitizer-doped conjugated polymer nanoparticles with high cross-sections for one- and two-photon excitation. Nanoscale, 3(4), 1451–1455.
50. Shen, X., Li, L., Wu, H., Yao, S. Q., Xu, Q. H. (2011). Photosensitizer-doped conjugated polymer nanoparticles for simultaneous two-photon imaging and two-photon photodynamic therapy in living cells. Nanoscale, 3(12), 5140–5146. doi:10.1039/c1nr11104c.
51. Gao, D., Agayan, R. R., Xu, H., Philbert, M. A., Kopelman, R. (2006). Nanoparticles for two-photon photodynamic therapy in living cells. Nano Letters, 6(11), 2383–2386. doi:10.1021/nl0617179.
52. Sariciftci, N. S., Smilowitz, L., Heeger, A. J., Wudl, F. (1992). Photoinduced electron transfer from a conducting polymer to buckminsterfullerene. Science, 258(5087), 1474–1476. doi:10.1126/science.258.5087.1474.
53. Park, S. H., Roy, A., Beaupré, S., Cho, S., Coates, N., Moon, J. S., et al. (2009). Bulk heterojunction solar cells with internal quantum efficiency approaching 100 %. Nature Photonics, 3(5), 297–302. doi:10.1038/nphoton.2009.69.
54. 2 fullerene derivatives. Nanomedicine-Nanotechnology Biology and Medicine, 9(4), 570–579. doi:10.1016/j.nano.2012.09.005.
55. Fan, J. Q., Fang, G., Zeng, F., Wang, X. D., Wu, S. Z. (2013). Water-dispersible fullerene aggregates as a targeted anticancer prodrug with both chemo- and photodynamic therapeutic actions. Small, 9(4), 613–621. doi:10.1002/smll.201201456.
56. Grynyuk, I., Grebinyk, S., Prylutska, S., Mykhailova, A., Franskevich, D., Matyshevska, O., et al. (2013). Photoexcited fullerene C-60 disturbs prooxidant–antioxidant balance in leukemic L1210 cells. Materialwissenschaft und Werkstofftechnik, 44(2–3), 139–143. doi:10.1002/mawe.201300105.
57. Liu, X. M., Zheng, M., Kong, X. G., Zhang, Y. L., Zeng, Q. H., Sun, Z. C., et al. (2013). Separately doped upconversion-C-60 nanoplatform for NIR imaging-guided photodynamic therapy of cancer cells. Chemical Communications, 49(31), 3224–3226. doi:10.1039/c3cc41013g.
58. Trpkovic, A., Todorovic-Markovic, B., Trajkovic, V. (2012). Toxicity of pristine versus functionalized fullerenes: mechanisms of cell damage and the role of oxidative stress. Archives of Toxicology, 86(12), 1809–1827. doi:10.1007/s00204-012-0859-6.
59. Chen, Z. Y., Ma, L. J., Liu, Y., Chen, C. Y. (2012). Applications of functionalized fullerenes in tumor theranostics. Theranostics, 2(3), 238–250. doi:10.7150/thno.3509.
60. Tenery, D., Worden, J. G., Hu, Z., Gesquiere, A. J. (2009). Single particle spectroscopy on composite MEH-PPV/PCBM nanoparticles. Journal of Luminescence, 129(5), 423–429. doi:10.1016/j.jlumin.2008.11.009.
61. Gratton, S. E. A., Ropp, P. A., Pohlhaus, P. D., Luft, J. C., Madden, V. J., Napier, M. E., et al. (2008). The effect of particle design on cellular internalization pathways. Proceedings of the National Academy of Sciences of the United States of America, 105(33), 11613–11618. doi:10.1073/pnas.0801763105.
62. Huhn, D., Kantner, K., Geidel, C., Brandholt, S., De Cock, I., Soenen, S. J. H., et al. (2013). Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano, 7(4), 3253–3263. doi:10.1021/nn3059295.
63. Xu, P. S., Van Kirk, E. A., Zhan, Y. H., Murdoch, W. J., Radosz, M., Shen, Y. Q. (2007). Targeted charge-reversal nanoparticles for nuclear drug delivery. Angewandten Chemistry-International Editor, 46(26), 4999–5002. doi:10.1002/anie.200605254.
64. Gao, H. J., Shi, W. D., Freund, L. B. (2005). Mechanics of receptor-mediated endocytosis. Proceedings of the National Academy of Sciences of the United States of America, 102(27), 9469–9474. doi:10.1073/pnas.0503879102.
65. Lerch, S., Dass, M., Musyanovych, A., Landfester, K., Mailander, V. (2013). Polymeric nanoparticles of different sizes overcome the cell membrane barrier. European Journal of Pharmaceutics and Biopharmaceutics, 84(2), 265–274. doi:10.1016/j.ejpb.2013.01.024.
66. Tang, L., Gabrielson, N. P., Uckun, F. M., Fan, T. M., Cheng, J. J. (2013). Size-dependent tumor penetration and in vivo efficacy of monodisperse drug-silica nanoconjugates. Molecular Pharmaceutics, 10(3), 883–892. doi:10.1021/mp300684a.
67. Wang, J., Wang, D. L., Moses, D., Heeger, A. J. (2001). Dynamic quenching of 5-(2 '-ethyl-hexyloxy)-p-phenylene vinylene (MEH-PPV) by charge transfer to a C-60 derivative in solution. Journal of Applied Polymer Science, 82(10), 2553–2557. doi:10.1002/app.2106.
68. Hu, Z. J., & Gesquiere, A. J. (2009). PCBM concentration dependent morphology of P3HT in composite P3HT/PCBM nanoparticles. Chemical Physics Letters, 476(1–3), 51–55. doi:10.1016/j.cplett.2009.05.066.
69. Zhang, Y., Yang, M., Portney, N. G., Cui, D. X., Budak, G., Ozbay, E., et al. (2008). Zeta potential: a surface electrical characteristic to probe the interaction of nanoparticles with normal and cancer human breast epithelial cells. Biomedical Microdevices, 10(2), 321–328. doi:10.1007/s10544-007-9139-2.
70. Toffoli, G., Cernigoi, C., Russo, A., Gallo, A., Bagnoli, M., Boiocchi, M. (1997). Overexpression of folate binding protein in ovarian cancers. International Journal of Cancer, 74(2), 193–198. doi:10.1002/(SICI)1097-0215.
71. Ross, J. F., Chaudhuri, P. K., Ratnam, M. (1994). Differential regulation of folate receptor isoforms in normal and malignant tissues in vivo and in established cell lines. Physiologic and clinical implications. Cancer, 73(9), 2432–2443. doi:10.1002/1097-0142.
72. Schumacker, P. T. (2006). Reactive oxygen species in cancer cells: live by the sword, die by the sword. Cancer Cell, 10(3), 175–176. doi:10.1016/j.ccr.2006.08.015.
73. Parker, N., Turk, M. J., Westrick, E., Lewis, J. D., Low, P. S., Leamon, C. P. (2005). Folate receptor expression in carcinomas and normal tissues determined by a quantitative radioligand binding assay. Analytical Biochemistry, 338(2), 284–293. doi:10.1016/j.ab.2004.12.026.
74. Zhao, F., Zhao, Y., Liu, Y., Chang, X., Chen, C., Zhao, Y. Cellular uptake, intracellular trafficking, and cytotoxicity of nanomaterials. Small, 7(10), 1322–1337. doi: 10.1002/smll.201100001
75. Kim, J.-S., Yoon, T.-J., Yu, K.-N., Noh, M. S., Woo, M., Kim, B.-G., et al. (2006). Cellular uptake of magnetic nanoparticle is mediated through energy-dependent endocytosis in A549 cells. Journal of Veterinary Science, 7(4), 321–326. doi:10.4142/jvs.2006.7.4.321.
76. Fretz, M. M., Koning, G. A., Mastrobattista, A., Jiskoot, W., Storm, G. (2004). OVCAR-3 cells internalize TAT-peptide modified liposomes by endocytosis. Biochimica Et Biophysica Acta-Biomembranes, 1665(1–2), 48–56. doi:10.1016/j.bbamem.2004.06.022.
77. Chen, N. Y., Lai, H. H., Hsu, T. H., Lin, F. Y., Chen, J. Z., Lo, H. C. (2008). Induction of apoptosis in human lung carcinoma A549 epithelial cells with an ethanol extract of Tremella mesenterica. Bioscience, Biotechnology, and Biochemistry, 72(5), 1283–1289. doi:10.1271/bbb.70773.
78. Fan, T.-J., Han, L.-H., Cong, R.-S., Liang, J. (2005). Caspase family proteases and apoptosis. Acta Biochimica et Biophysica Sinica, 37(11), 719–727. doi:10.1111/j.1745-7270.2005.00108.x.
79. Pasquini, L., Pettruci, E., Riccioni, R., Petronella, A., Testa, U. (2006). Sensitivity and resistance of human cancer cells to TRAIL: mechanisms and therapeutical perspectives. Cancer Therapy, 4, 47–72.
80. Brown, J. M., & Attardi, L. D. (2005). The role of apoptosis in cancer development and treatment response. Nature Reviews Cancer, 5(3), 231–237. doi:10.1038/nrc1560.