Bioluminescence-activated deep-tissue photodynamic therapy of cancer

Theranostics

Volumn 5, Issue 8, 2015, Pages 805-817

  Kim, Yi Rang ^a,b   Kim, Seonghoon ^a   Choi, Jin Woo ^c,d   Choi, Sung Yong ^a   Lee, Sang Hee ^a   Kim, Homin ^a   Hahn, Sei Kwang ^e   Koh, Gou Young ^a   Yun, Seok Hyun ^a,d  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b University of Ulsan College of Medicine   (South Korea)

^c Wonkwang University   (South Korea)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

Bioluminescence; Cancer; Photobiology; Photodynamic therapy; Photomedicine; Photosensitizers; Resonance energy transfer

Indexed keywords

CHLORIN 6; PHOTOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; PHYTOCHLORIN; PORPHYRIN; RADIOSENSITIZING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BIOLUMINESCENCE ACTIVATED DEEP TISSUE PHOTODYNAMIC THERAPY; CANCER CELL; COLON CANCER; CONTROLLED STUDY; CYTOTOXICITY; DISTANT METASTASIS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LASER; LEWIS CARCINOMA; LUNG METASTASIS; LYMPH NODE; LYMPH VESSEL; MELANOMA B16; MONOLAYER CULTURE; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; C57BL MOUSE; DISEASE MODEL; HUMAN; LUMINESCENCE; METABOLISM; NEOPLASMS; PHOTOCHEMOTHERAPY; PROCEDURES;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; LASERS; LUMINESCENCE; MICE, INBRED C57BL; NEOPLASMS; PHOTOCHEMOTHERAPY; PORPHYRINS; RADIATION-SENSITIZING AGENTS;

EID: 84941283644     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.11520     Document Type: Article

References (74)

1. Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, Gollnick SO, et al. Photodynamic therapy of cancer: an update. CA Cancer J Clin. 2011; 61: 250-81.
2. Brown SB, Brown EA, Walker I. The present and future role of photodynamic therapy in cancer treatment. Lancet Oncol. 2004; 5: 497-508.
3. Castano AP, Mroz P, Hamblin MR. Photodynamic therapy and anti-tumour immunity. Nat Rev Cancer. 2006; 6: 535-45.
4. Huang Y-Y, Chen AC-H, Carroll JD, Hamblin MR. Biphasic dose response in low level light therapy. Dose Response. 2009; 7: 358-83.
5. Wollensak G, Spoerl E, Seiler T. Riboflavin/ultraviolet-A-induced collagen crosslinking for the treatment of keratoconus. Am J Ophthalmol. 2003; 135: 620-7.
6. Ye H, Daoud-El Baba M, Peng R-W, Fussenegger M. A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science. 2011; 332: 1565-8.
7. Cheong W-F, Prahl SA, Welch AJ. A review of the optical properties of biological tissues. IEEE J Quantum Electron. 1990; 26: 2166-85.
8. Ntziachristos V, Ripoll J, Wang LV, Weissleder R. Looking and listening to light: the evolution of whole-body photonic imaging. Nat Biotechnol. 2005; 23: 313-20.
9. Choi M, Choi JW, Kim S, Nizamoglu S, Hahn SK, Yun SH. Light-guiding hydrogels for cell-based sensing and optogenetic synthesis in vivo. Nat Photonics. 2013; 7: 987-94.
10. Kim T-I, McCall JG, Jung YH, Huang X, Siuda ER, Li Y, et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science. 2013; 340: 211-6.
11. Bagley AF, Hill S, Rogers GS, Bhatia SN. Plasmonic Photothermal Heating of Intraperitoneal Tumors through the Use of an Implanted Near-Infrared Source. ACS Nano. 2013; 7: 8089-97.
12. Ran C, Zhang Z, Hooker J, Moore A. In vivo photoactivation without "light": use of Cherenkov radiation to overcome the penetration limit of light. Mol Imaging Biol. 2012; 14: 156-62.
13. Theodossiou T, Hothersall JS, Woods EA, Okkenhaug K, Jacobson J, MacRobert AJ. Firefly Luciferin-activated Rose Bengal In Vitro Photodynamic Therapy by Intracellular Chemiluminescence in Transgenic NIH 3T3 Cells. Cancer Res. 2003; 63: 1818-21.
14. Schipper ML, Patel MR, Gambhir SS. Evaluation of firefly luciferase bioluminescence mediated photodynamic toxicity in cancer cells. Mol Imaging Biol. 2006; 8: 218-25.
15. Hsu C-Y, Chen C-W, Yu H-P, Lin Y-F, Lai P-S. Bioluminescence resonance energy transfer using luciferase-immobilized quantum dots for self-illuminated photodynamic therapy. Biomaterials. 2013; 34: 1204-12.
16. Huang L, Chen T-C, Lin F-H. Luminol As In Situ Light Source in Meso-Tetraphenylporphyrin-Mediated Photodynamic Therapy. Curr Med Chem. 2013; 20: 1195-202.
17. Berglund K, Birkner E, Augustine GJ, Hochgeschwender U. Light-Emitting Channelrhodopsins for Combined Optogenetic and Chemical-Genetic Control of Neurons. PLoS One. 2013; 8: e59759.
18. Yuan H, Chong H, Wang B, Zhu C, Liu L, Yang Q, et al. Chemical molecule-induced light-activated system for anticancer and antifungal activities. J Am Chem Soc. 2012; 134: 13184-7.
19. So M-K, Xu C, Loening AM, Gambhir SS, Rao J. Self-illuminating quantum dot conjugates for in vivo imaging. Nat Biotechnol. 2006; 24: 339-43.
20. Angers S, Salahpour A, Joly E, Hilairet S, Chelsky D, Dennis M, et al. Detection of ß2-adrenergic receptor dimerization in living cells using bioluminescence resonance energy transfer (BRET). Proc Natl Acad Sci U S A. 2000; 97: 3684-9.
21. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, Larsen B, et al. A global protein kinase and phosphatase interaction network in yeast. Science. 2010; 328: 1043-6.
22. Collins BM, Skinner CF, Watson PJ, Seaman MNJ, Owen DJ. Vps29 has a phosphoesterase fold that acts as a protein interaction scaffold for retromer assembly. Nat Struct Mol Biol. 2005; 12: 594-602.
23. Pfleger KD, Eidne KA. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat Methods. 2006; 3: 165-74.
24. Carriba P, Navarro G, Ciruela F, Ferré S, Casadó V, Agnati L, et al. Detection of heteromerization of more than two proteins by sequential BRET-FRET. Nat Methods. 2008; 5: 727-33.
25. Yuan H, Bai H, Liu L, Lv F, Wang S. A glucose-powered antimicrobial system using organic-inorganic assembled network materials. Chem Commun. 2015; 51: 722-4.
26. Buturlakin M, Kiseleva V, Shmelev V. Interaction of human serum albumin and luminol. Biofizika. 1975; 20: 975-7.
27. Lee-Chen S, Yu C, Wu D, Jan K. Differential effects of luminol, nickel, and arsenite on the rejoining of ultraviolet light and alkylation-induced DNA breaks. Environ Mol Mutagen. 1994; 23: 116-20.
28. Ikushima T. Bimodal induction of sister-chromatid exchanges by luminol, an inhibitor of poly (ADP-ribose) synthetase, during the S-phase of the cell cycle. Chromosoma. 1990; 99: 360-4.
29. Celli JP, Spring BQ, Rizvi I, Evans CL, Samkoe KS, Verma S, et al. Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem Rev. 2010; 110: 2795-838.
30. Loening AM, Fenn TD, Wu AM, Gambhir SS. Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng Des Sel. 2006; 19: 391-400.
31. So M-K, Loening AM, Gambhir SS, Rao J. Creating self-illuminating quantum dot conjugates. Nat Protoc. 2006; 1: 1160-4.
32. Collins HA, Khurana M, Moriyama EH, Mariampillai A, Dahlstedt E, Balaz M, et al. Blood-vessel closure using photosensitizers engineered for two-photon excitation. Nat Photonics. 2008; 2: 420-4.
33. Lee SJ, Koo H, Jeong H, Huh MS, Choi Y, Jeong SY, et al. Comparative study of photosensitizer loaded and conjugated glycol chitosan nanoparticles for cancer therapy. J Control Release. 2011; 152: 21-9.
34. Douillard S, Olivier D, Patrice T. In vitro and in vivo evaluation of Radachlorin® sensitizer for photodynamic therapy. Photochem Photobiol Sci. 2009; 8: 405-13.
35. Rota C, Chignell CF, Mason RP. Evidence for free radical formation during the oxidation of 2'-7'-dichlorofluorescin to the fluorescent dye 2'-7'-dichlorofluorescein by horseradish peroxidase:: Possible implications for oxidative stress measurements. Free Radic Biol Med. 1999; 27: 873-81.
36. Wang H, Luo K, Tan L-Z, Ren B-G, Gu L-Q, Michalopoulos G, et al. p53-induced gene 3 mediates cell death induced by glutathione peroxidase 3. J Biol Chem. 2012; 287: 16890-902.
37. Kalghatgi S, Spina CS, Costello JC, Liesa M, Morones-Ramirez JR, Slomovic S, et al. Bactericidal antibiotics induce mitochondrial dysfunction and oxidative damage in mammalian cells. Sci Transl Med. 2013; 5: 192ra85.
38. Gorski DH, Beckett MA, Jaskowiak NT, Calvin DP, Mauceri HJ, Salloum RM, et al. Blockade of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 1999; 59: 3374.
39. Mauceri HJ, Hanna NN, Beckett MA, Gorski DH, Staba MJ, Stellato KA, et al. Combined effects of angiostatin and ionizing radiation in antitumour therapy. Nature. 1998; 394: 287-91.
40. Nielsen BS, Lund LR, Christensen IJ, Johnsen M, Usher PA, Wulf-Andersen L, et al. A precise and efficient stereological method for determining murine lung metastasis volumes. Am J Physiol. 2001; 158: 1997-2003.
41. Jackson JD. Classical electrodynamics. Classical Electrodynamics, 3rd Edition, by John David Jackson, pp 832 ISBN 0-471-30932-X Wiley-VCH, July 1998. 1998; 1.
42. Medintz IL, Hildebrandt N. FRET-Förster resonance energy transfer from theory to applications. In. Wiley-VCH Verlag GmbH. 1999. http://dx.doi.org/10.1002/9783527656028.
43. Mitsunaga M, Ogawa M, Kosaka N, Rosenblum LT, Choyke PL, Kobayashi H. Cancer cell-selective in vivo near infrared photoimmunotherapy targeting specific membrane molecules. Nat Med. 2011; 17: 1685-91.
44. Bulina ME, Chudakov DM, Britanova OV, Yanushevich YG, Staroverov DB, Chepurnykh TV, et al. A genetically encoded photosensitizer. Nat Biotechnol. 2005; 24: 95-9.
45. Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr. 1993; 57: 715S-24S.
46. Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta. 2006; 1757: 509-17.
47. del Carmen MG, Rizvi I, Chang Y, Moor AC, Oliva E, Sherwood M, et al. Synergism of epidermal growth factor receptor-targeted immunotherapy with photodynamic treatment of ovarian cancer in vivo. J Natl Cancer Inst. 2005; 97: 1516-24.
48. Duska LR, Hamblin MR, Miller JL, Hasan T. Combination photoimmunotherapy and cisplatin: Effects on human ovarian cancer ex vivo. J Natl Cancer Inst. 1999; 91: 1557-63.
49. Rizvi I, Dinh TA, Yu WP, Chang YC, Sherwood ME, Hasan T. Photoimmunotherapy and irradiance modulation reduce chemotherapy cycles and toxicity in a murine model for ovarian carcinomatosis: perspective and results. Isr J Chem. 2012; 52: 776-87.
50. Tang P, Zhang D-M, Xuan N, Tsui S, Waye M, Kong S-K, et al. Photodynamic therapy inhibits P-glycoprotein mediated multidrug resistance via JNK activation in human hepatocellular carcinoma using the photosensitizer pheophorbide a. Mol Cancer. 2009; 8: 56-67.
51. Khdair A, Handa H, Mao G, Panyam J. Nanoparticle-mediated combination chemotherapy and photodynamic therapy overcomes tumor drug resistance in vitro. Eur J Pharm Biopharm. 2009; 71: 214-22.
52. GoffBA, Bamberg M, Hasan T. Photoimmunotherapy of human ovarian-carcinoma cells ex vivo. Cancer Res. 1991; 51: 4762-7.
53. Celli JP, Solban N, Liang A, Pereira SP, Hasan T. Verteporfin-based photodynamic therapy overcomes gemcitabine insensitivity in a panel of pancreatic cancer cell lines. Lasers Surg Med. 2011; 43: 565-74.
54. Capella MAM, Capella LS. A light in multidrug resistance: photodynamic treatment of multidrug-resistant tumors. J Biomed Sci. 2003; 10: 361-6.
55. Li W, Zhang WJ, Ohnishi K, Yamada I, Ohno R, Hashimoto K. 5-Aminolaevulinic acid-mediated photodynamic therapy in multidrug resistant leukemia cells. J Photochem Photobiol B. 2001; 60: 79-86.
56. Teiten M-H, Bezdetnaya L, Merlin J-L, Bour-Dill C, Pauly M, Dicato M, et al. Effect of meta-tetra(hydroxyphenyl)chlorin (m THPC)-mediated photodynamic therapy on sensitive and multidrug-resistant human breast cancer cells. J Photochem Photobiol B. 2001; 62: 146-52.
57. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007; 13: 4429-34.
58. Čunderlíková B, Gangeskar L, Moan J. Acid-base properties of chlorin e 6: relation to cellular uptake. J Photochem Photobiol B. 1999; 53: 81-90.
59. Kessel D, Poretz R. Sites of photodamage induced by photodynamic therapy with a chlorin e6 triacetoxymethyl ester (CAME). Photochem Photobiol. 2000; 71: 94-6.
60. Mojzisova H, Bonneau S, Vever-Bizet C, Brault D. Cellular uptake and subcellular distribution of chlorin e6 as functions of pH and interactions with membranes and lipoproteins. Biochim Biophys Acta. 2007; 1768: 2748-56.
61. Bulina ME, Chudakov DM, Britanova OV, Yanushevich YG, Staroverov DB, Chepurnykh TV, et al. A genetically encoded photosensitizer. Nat Biotechnol. 2006; 24: 95-9.
62. Liao Z-X, Li Y-C, Lu H-M, Sung H-W. A genetically-encoded KillerRed protein as an intrinsically generated photosensitizer for photodynamic therapy. Biomaterials. 2014; 35: 500-8.
63. Watanabe R, Hanaoka H, Sato K, Nagaya T, Harada T, Mitsunaga M, et al. Photoimmunotherapy Targeting Prostate-Specific Membrane Antigen: Are Antibody Fragments as Effective as Antibodies? J Nucl Med. 2015; 56: 140-4.
64. Bulina ME, Lukyanov KA, Britanova OV, Onichtchouk D, Lukyanov S, Chudakov DM. Chromophore-assisted light inactivation (CALI) using the phototoxic fluorescent protein KillerRed. Nat Protoc. 2006; 1: 947-53.
65. Kessel D, Luo Y. Mitochondrial photodamage and PDT-induced apoptosis. J Photochem Photobiol B. 1998; 42: 89-95.
66. Kessel D, Luo Y. Photodynamic therapy: a mitochondrial inducer of apoptosis. Cell Death Differ. 1999; 6: 28-35.
67. Castano AP, Demidova TN, Hamblin MR. Mechanisms in photodynamic therapy: part three-photosensitizer pharmacokinetics, biodistribution, tumor localization and modes of tumor destruction. Photodiagnosis Photodyn Ther. 2005; 2: 91-106.
68. Loening AM, Wu AM, Gambhir SS. Red-shifted Renilla reniformis luciferase variants for imaging in living subjects. Nat Methods. 2007; 4: 641-3.
69. Boyle RW, Dolphin D. Structure and biodistribution relationships of photodynamic sensitizers. Photochem Photobiol. 1996; 64: 469-85.
70. Hamblin MR, Miller JL, Hasan T. Effect of charge on the interaction of site-specific photoimmunoconjugates with human ovarian cancer cells. Cancer Res. 1996; 56: 5205-10.
71. Spring BQ, Abu-Yousif AO, Palanisami A, Rizvi I, Zheng X, Mai ZM, et al. Selective treatment and monitoring of disseminated cancer micrometastases in vivo using dual-function, activatable immunoconjugates. Proc Natl Acad Sci U S A. 2014; 111: E933-E42.
72. Ozaslan C, Kuru B. Lymphedema after treatment of breast cancer. Am J Surg. 2004; 187: 69-72.
73. Jenkins DE, Oei Y, Hornig YS, Yu SF, Dusich J, Purchio T, et al. Bioluminescent imaging (BLI) to improve and refine traditional murine models of tumor growth and metastasis. Clin Exp Metastasis. 2003; 20: 733-44.
74. Tammela T, Saaristo A, Holopainen T, Ylä-Herttuala S, Andersson LC, Virolainen S, et al. Photodynamic ablation of lymphatic vessels and intralymphatic cancer cells prevents metastasis. Sci Transl Med. 2011; 3: 69ra11.