Upconversion nanoparticle-mediated photodynamic therapy induces THP-1 macrophage apoptosis via ROS bursts and activation of the mitochondrial caspase pathway

International Journal of Nanomedicine

Volumn 10, Issue , 2015, Pages 3719-3736

  Zhu, Xing ^a   Wang, Hao ^b   Zheng, Longbin ^a   Zhong, Zhaoyu ^a   Li, Xuesong ^a   Zhao, Jing ^c   Kou, Jiayuan ^a   Jiang, Yueqing ^a   Zheng, Xiufeng ^a   Liu, Zhongni ^a   Li, Hongxia ^a   Cao, Wenwu ^b,d   Tian, Ye ^a   Wang, You ^b   Yang, Liming ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

^b HARBIN INSTITUTE OF TECHNOLOGY   (China)

^c JINING NO 1 PEOPLE S HOSPITAL   (China)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Apoptosis; Atherosclerosis; Fluorescent nanoparticles; Macrophages; Photodynamic therapy; Reactive oxygen species

Indexed keywords

CASPASE 3; CASPASE 9; CYTOCHROME C; MALONALDEHYDE; NANOPARTICLE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; UPCONVERSION FLUORESCENT CHLORIN E6 NANOPARTICLE; CARRIER PROTEIN; CASPASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PHYTOCHLORIN; PORPHYRIN; RADIOSENSITIZING AGENT;

APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; CELL MEMBRANE DEPOLARIZATION; CELL VIABILITY; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SIGNALING; MACROPHAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL PERMEABILITY; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SECRETION; UPREGULATION; CELL LINE; CHEMISTRY; CYTOSOL; DRUG EFFECTS; METABOLISM; MITOCHONDRION; PHOTOCHEMOTHERAPY; PROCEDURES;

APOPTOSIS; CASPASES; CELL LINE; CYTOCHROMES C; CYTOSOL; HUMANS; MACROPHAGES; MEMBRANE POTENTIAL, MITOCHONDRIAL; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NANOPARTICLES; PHOTOCHEMOTHERAPY; POLY(ADP-RIBOSE) POLYMERASES; PORPHYRINS; RADIATION-SENSITIZING AGENTS; REACTIVE OXYGEN SPECIES;

EID: 84930503730     PISSN: 11769114     EISSN: 11782013     Source Type: Journal    
DOI: 10.2147/IJN.S82162     Document Type: Article

References (52)

1. Wang FP, Gao QP, Guo SY, et al. The sonodynamic effect of curcumin on THP-1 cell-derived macrophages. Biomed Res Int. 2013;2013:737264.
2. Capewell S, Lloyd-Jones DM. Optimal cardiovascular prevention strategies for the 21st century. JAMA. 2010;304:2057–2058.
3. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145(3):341–355.
4. Yang EH, Gumina RJ, Lennon RJ, et al. Emergency coronary artery bypass surgery for percutaneous coronary interventions: changes in the incidence, clinical characteristics, and indications from 1979 to 2003. J Am Coll Cardiol. 2005;46(11):2004–2009.
5. Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer. 2003;3(5):380–387.
6. Castano AP, Mroz P, Hamblin MR. Photodynamic therapy and anti-tumour immunity. Nat Rev Cancer. 2006;6(7):535–545.
7. Tian G, Ren W, Yan L, et al. Red-emitting upconverting nanoparticles for photodynamic therapy in cancer cells under near-infrared excitation. Small. 2013;9(11):1929–1938.
8. Tang G, Hyman S, Schneider JH Jr, et al. Application of photodynamic therapy to the treatment of atherosclerotic plaques. Neurosurgery. 1993;32(3):438–443.
9. Waksman R, McEwan PE, Moore TI, et al. PhotoPoint photodynamic therapy promotes stabilization of atherosclerotic plaques and inhibits plaque progression. J Am Coll Cardiol. 2008;52(12):1024–1032.
10. Peng C, Li Y, Liang H, et al. Detection and photodynamic therapy of inflamed atherosclerotic plaques in the carotid artery of rabbits. J Photochem Photobiol B. 2011;102(1):26–31.
11. Liu Q, Sun Y, Li C, et al. 18F-labeled magnetic-upconversion nanophosphors via rare-earth cation-assisted ligand assembly. ACS Nano. 2011;5(4):3146–3157.
12. Cheng L, Yang K, Li Y, et al. Facile preparation of multifunctional upconversion nanoprobes for multimodal imaging and dual-targeted photothermal therapy. Angew Chem Int Ed Engl. 2011;50(32):7385–7390.
13. Frangioni JV. In vivo near-infrared fluorescence imaging. Curr Opin Chem Biol. 2003;7(5):626–634.
14. Chatterjee DK, Rufaihah AJ, Zhang Y. Upconversion fluorescence imaging of cells and small animals using lanthanide doped nanocrystals. Biomaterials. 2008;29(7):937–943.
15. Cao Z, Zhu W, Wang W, et al. Stable cerasomes for simultaneous drug delivery and magnetic resonance imaging. Int J Nanomedicine. 2014;9:5103.
16. Qian HS, Guo HC, Ho PC, et al. Mesoporous-Silica-coated up-conversion fluorescent nanoparticles for photodynamic therapy. Small. 2009;5(20):2285–2290.
17. Guo H, Qian H, Idris NM, Zhang Y. Singlet oxygen-induced apoptosis of cancer cells using upconversion fluorescent nanoparticles as a carrier of photosensitizer. Nanomedicine. 2010;6(3):486–495.
18. Xiong L, Chen Z, Tian Q, Cao T, Xu C, Li F. High contrast upconversion luminescence targeted imaging in vivo using peptide-labeled nanophosphors. Anal Chem. 2009;81(21):8687–8694.
19. Cheng L, Yang K, Shao M, Lee ST, Liu Z. Multicolor in vivo imaging of upconversion nanoparticles with emissions tuned by luminescence resonance energy transfer. J Phys Chem C. 2011;115(6):2686–2692.
20. Wang C, Cheng L, Liu Z. Drug delivery with upconversion nanoparticles for multi-functional targeted cancer cell imaging and therapy. Biomaterials. 2011;32(4):1110–1120.
21. Chou LC, Yang JS, Huang LJ, et al. The synthesized 2-(2-fluorophenyl)-6, 7-methylenedioxyquinolin-4-one (CHM-1) promoted G2/M arrest through inhibition of CDK1 and induced apoptosis through the mitochondrial-dependent pathway in CT-26 murine colorectal adenocarcinoma cells. J Gastroenterol. 2009;44(10):1055–1063.
22. Wang C, Tao H, Cheng L, Liu Z. Near-infrared light induced in vivo photodynamic therapy of cancer based on upconversion nanoparticles. Biomaterials. 2011;32(26):6145–6154.
23. Tabas I. Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol. 2010;10(1):36–46.
24. Martinet W, Verheye S, De Meyer GR. Selective depletion of macrophages in atherosclerotic plaques via macrophage-specific initiation of cell death. Trends Cardiovasc Med. 2007;17(2):69–75.
25. Copley L, van der Watt P, Wirtz KW, Parker MI, Leaner VD. Photolon™, a chlorin e6 derivative, triggers ROS production and light-dependent cell death via necrosis. Int J Biochem Cell Biol. 2008;40(2):227–235.
26. Ong CY, Ling SK, Ali RM, et al. Systematic analysis of in vitro photo-cytotoxic activity in extracts from terrestrial plants in Peninsula Malaysia for photodynamic therapy. J Photochem Photobiol B. 2009;96(3):216–222.
27. Liu L, Zhang Z, Xing D. Cell death via mitochondrial apoptotic pathway due to activation of Bax by lysosomal photodamage. Free Radic Biol Med. 2011;51(1):53–68.
28. Ricchelli F, Šileikytė J, Bernardi P. Shedding light on the mitochondrial permeability transition. Biochim Biophys Acta. 2011;1807(5):482–490.
29. Magi B, Ettorre A, Liberatori S, et al. Selectivity of protein carbonylation in the apoptotic response to oxidative stress associated with photodynamic therapy: a cell biochemical and proteomic investigation. Cell Death Differ. 2004;11(8):842–852.
30. Song W, Cui H, Zhang R, et al. Apoptosis of SAS cells induced by sonodynamic therapy using 5-aminolevulinic acid sonosensitizer. Anticancer Res. 2011;31(1):39–45.
31. Duchen MR. Contributions of mitochondria to animal physiology: from homeostatic sensor to calcium signalling and cell death. J Physiol. 1999;516(1):1–17.
32. Zamzami N, Kroemer G. The mitochondrion in apoptosis: how Pandora’s box opens. Nat Rev Mol Cell Biol. 2001;2(1):67–71.
33. McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Curr Biol. 2006;16(14):R551–R560.
34. Smith DJ, Ng H, Kluck RM, et al. The mitochondrial gateway to cell death. IUBMB Life. 2008;60(6):383–389.
35. Hung HI, Schwartz JM, Maldonado EN, et al. Mitoferrin-2-dependent mitochondrial iron uptake sensitizes human head and neck squamous carcinoma cells to photodynamic therapy. J Biol Chem. 2013;288(1):677–686.
36. Woodfield K, Ruck A, Brdiczka D, et al. Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem J. 1998;336:287–290.
37. Miura T, Tanno M. The mPTP and its regulatory proteins: final common targets of signalling pathways for protection against necrosis. Cardiovasc Res. 2012;94:181–189.
38. Youle RJ, Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol. 2008;9(1):47–59.
39. Buytaert E, Callewaert G, Hendrickx N, et al. Role of endoplasmic reticulum depletion and multidomain proapoptotic BAX and BAK proteins in shaping cell death after hypericin-mediated photodynamic therapy. FASEB J. 2006;20(6):756–758.
40. Lloyd-Jones D, Adams RJ, Brown TM, et al. Heart disease and stroke statistics–2010 update a report from the American Heart Association. Circulation. 2010;121(7):e46–e215.
41. Lin G, Wang X, Yin F, et al. Passive tumor targeting and imaging by using mercaptosuccinic acid-coated near-infrared quantum dots. Int J Nanomed. 2015;10:335.
42. Lee JY, Kim JS, Cho HJ, et al. Poly (styrene)-b-poly (DL-lactide) copolymer-based nanoparticles for anticancer drug delivery. Int J Nanomed. 2014;9:2803.
43. Arora S, Swaminathan SK, Kirtane A, et al. Synthesis, characterization, and evaluation of poly (D, L-lactide-co-glycolide)-based nanoformulation of miRNA-150: potential implications for pancreatic cancer therapy. Int J Nanomed. 2014;9:2933.
44. Kim H, Kim Y, Kim IH, et al. ROS-responsive activatable photosensitizing agent for imaging and photodynamic therapy of activated macrophages. Theranostics. 2014;4(1):1.
45. Kang SU, Cho JH, Chang JW, et al. Nonthermal plasma induces head and neck cancer cell death: the potential involvement of mitogen-activated protein kinase-dependent mitochondrial reactive oxygen species. Cell Death Dis. 2014;5(2):e1056.
46. Jin H, Zhong X, Wang Z, et al. Sonodynamic effects of hematoporphyrin monomethyl ether on CNE-2 cells detected by atomic force microscopy. J Cell Biochem. 2011;112(1):169–178.
47. Li JH, Yue W, Huang Z, et al. Calcium overload induces C6 rat glioma cell apoptosis in sonodynamic therapy. Int J Radiat Biol. 2011;87(10):1061–1066.
48. Vaux DL, Korsmeyer SJ. Cell death in development. Cell. 1999;96(2):245–254.
49. Petronilli V, Penzo D, Scorrano L, et al. The mitochondrial permeability transition, release of cytochrome c and cell death correlation with the duration of pore openings in situ. J Biol Chem. 2001;276(15):12030–12034.
50. Van Loo G, Saelens X, Van Gurp M, et al. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 2002;9(10):1031–1042.
51. Li X, Zheng L, Kou J, et al. The efficacy and mechanism of apoptosis induction by hypericin-mediated sonodynamic therapy in THP-1 macrophages. Int J Nanomed. 2015;10:821–838.
52. Yoo JO, Lim YC, Kim YM, et al. Transglutaminase 2 promotes both caspase-dependent and caspase-independent apoptotic cell death via the calpain/Bax protein signaling pathway. J Biol Chem. 2012;287(18):14377–14388.