Role of apoptosis and necrosis in cell death induced by nanoparticle-mediated photothermal therapy
Source abstract
Abstract
Current cancer therapies can cause significant collateral damage due to a lack of specificity and sensitivity. Therefore, we explored the cell death pathway response to gold nanorod (GNR)-mediated photothermal therapy as a highly specific cancer therapeutic to understand the role of apoptosis and necrosis during intense localized heating. By developing this, we can optimize photothermal therapy to induce a maximum of ‘clean’ cell death pathways, namely apoptosis, thereby reducing external damage. GNRs were targeted to several subcellular localizations within colorectal tumor cells in vitro, and the cell death pathways were quantitatively analyzed after photothermal therapy using flow cytometry. In this study, we found that the cell death response to photothermal therapy was dependent on the GNR localization. Furthermore, we demonstrated that nanorods targeted to the perinuclear region irradiated at 37.5 W/cm2 laser fluence rate led to maximum cell destruction with the ‘cleaner’ method of apoptosis, at similar percentages as other anti-cancer targeted therapies. We believe that this indicates the therapeutic potential for GNR-mediated photothermal therapy to treat cancer effectively without causing damage to surrounding tissue.
Source: openaire · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Nanoplatforms for cancer theranostics · Gold and Silver Nanoparticles Synthesis and Applications · Photoacoustic and Ultrasonic Imaging
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (48)
Show source-provided references
1. Alkilany AM, Nagaria PK, Hexel CR, Shaw TJ, Murphy CJ, Wyatt MD (2009) Cellular uptake and cytotoxicity of gold nanorods: molecular origin of cytotoxicity and surface effects. Small 5:701–708. doi: 10.1002/smll.20080154610.1002/smll.200801546 ↗
2. Brioude A, Jiang XC, Pileni MP (2005) Optical properties of gold nanorods: DDA simulations supported by experiments. J Phys Chem B 109:13138–1314210.1021/jp0507288 ↗
3. Chen CL et al (2010a) In situ real-time investigation of cancer cell photothermolysis mediated by excited gold nanorod surface plasmons. Biomaterials 31:4104–4112. doi: 10.1016/j.biomaterials.2010.01.14010.1016/j.biomaterials.2010.01.140 ↗
4. Chen H, Shao L, Ming T, Sun Z, Zhao C, Yang B, Wang J (2010b) Understanding the photothermal conversion efficiency of gold nanocrystals. Small 6:2272–2280. doi: 10.1002/smll.20100110910.1002/smll.201001109 ↗
5. Cole JR, Mirin NA, Knight MW, Goodrich GP, Halas NJ (2009) Photothermal efficiencies of nanoshells and nanorods for clinical therapeutic applications. J Phys Chem C 113:12090–1209410.1021/jp9003592 ↗
6. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:7310.1126/science.2321027 ↗
7. Dickerson EB et al (2008) Gold nanorod assisted near-infrared plasmonic photothermal therapy (PPTT) of squamous cell carcinoma in mice. Cancer Lett 269:57–66. doi: 10.1016/j.canlet.2008.04.02610.1016/j.canlet.2008.04.026 ↗
8. Durr NJ, Larson T, Smith DK, Korgel BA, Sokolov K, Ben-Yakar A (2007) Two-photon luminescence imaging of cancer cells using molecularly targeted gold nanorods. Nano Lett 7:941–945. doi: 10.1021/nl062962v10.1021/nl062962v ↗
9. El-Sayed MA (2001) Some interesting properties of metals confined in time and nanometer space of different shapes. Acc Chem Res 34:257–26410.1021/ar960016n ↗
10. Frei III E AK (2000) Principles of dose, schedule, and combination chemotherapy. In: al Be (ed) Cancer medicine. BCDecker, Hamilton
11. Friesen C, Herr I, Krammer PH, Debatin K-M (1996) Involvement of the CD95 (APO–1/Fas) receptor/ligand system in drug–induced apoptosis in leukemia cells. Nat Med 2:574–57710.1038/nm0596-574 ↗
12. Fulda S, Sieverts H, Friesen C, Herr I, Debatin K-M (1997) The CD95 (APO-1/Fas) system mediates drug-induced apoptosis in neuroblastoma cells. Cancer Res 57:3823–3829
13. Fulda S, Wick W, Weller M, Debatin K-M (2002) Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 8:808–81510.1038/nm735 ↗
14. Gad SC, Sharp KL, Montgomery C, Payne JD, Goodrich GP (2012) Evaluation of the toxicity of intravenous delivery of auroshell particles (gold-silica nanoshells). Int J Toxicol 31:584–594. doi: 10.1177/109158181246596910.1177/1091581812465969 ↗
15. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–131210.1126/science.281.5381.1309 ↗
16. Hanif R et al (1996) Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol 52:237–24510.1016/0006-2952(96)00181-5 ↗
17. Helmchen F, Denk W (2002) Deep tissue two-photon microscopy. Nature 12(5):593–601
18. Howlader N et al (2012) SEER cancer statistics review, 1975–2009 (vintage 2009 populations). National Cancer Institute, Bethesda
19. Huang XH, El-Sayed IH, Qian W, El-Sayed MA (2006) Cancer cell imaging and photothermal therapy in the near-infrared region by using gold nanorods. J Am Chem Soc 128:2115–2120. doi: 10.1021/ja057254a10.1021/ja057254a ↗
20. Huang X et al (2010) Comparative study of photothermolysis of cancer cells with nuclear-targeted or cytoplasm-targeted gold nanospheres: continuous wave or pulsed lasers. J Biomed Optics 15:058002. doi: 10.1117/1.348653810.1117/1.3486538 ↗
21. Idziorek T, Estaquier J, De Bels F, Ameisen J-C (1995) YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J Immunol Methods 185:249–25810.1016/0022-1759(95)00172-7 ↗
22. Jain PK, Lee KS, El-Sayed IH, El-Sayed MA (2006) Calculated absorption and scattering properties of gold nanoparticles of different size, shape, and composition: Applications in biological imaging and biomedicine. J Phys Chem B 110:7238–7248. doi: 10.1021/jp057170o10.1021/jp057170o ↗
23. Jana NR, Gearheart L, Murphy CJ (2001) Wet chemical synthesis of high aspect ratio cylindrical gold nanorods. J Phys Chem B 105:4065–406710.1021/jp0107964 ↗
24. Khlebtsov N, Dykman L (2011) Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies. Chem Soc Rev 40:1647–167110.1039/C0CS00018C ↗
25. Khlebtsov N, Trachuk L, Mel’nikov A (2005) The effect of the size, shape, and structure of metal nanoparticles on the dependence of their optical properties on the refractive index of a disperse medium. Opt Spectrosc 98:77–8310.1134/1.1858043 ↗
26. Khlebtsov B, Zharov V, Melnikov A, Tuchin V, Khlebtsov N (2006) Optical amplification of photothermal therapy with gold nanoparticles and nanoclusters. Nanotechnology 17:516710.1088/0957-4484/17/20/022 ↗
27. Kumar S, Aaron J, Sokolov K (2008) Directional conjugation of antibodies to nanoparticles for synthesis of multiplexed optical contrast agents with both delivery and targeting moieties. Nat Protoc 3:314–320. doi: 10.1038/nprot.2008.110.1038/nprot.2008.1 ↗
28. Lee KS, El-Sayed MA (2005) Dependence of the enhanced optical scattering efficiency relative to that of absorption for gold metal nanorods on aspect ratio, size, end-cap shape, and medium refractive index. J Phys Chem B 109:20331–20338. doi: 10.1021/jp054385p10.1021/jp054385p ↗
29. Lee J, Lilly GD, Doty RC, Podsiadlo P, Kotov NA (2009) In vitro toxicity testing of nanoparticles in 3D cell culture. Small 5:1213–1221. doi: 10.1002/smll.20080178810.1002/smll.200801788 ↗
30. Li JL, Gu M (2010) Surface plasmonic gold nanorods for enhanced two-photon microscopic imaging and apoptosis induction of cancer cells. Biomaterials 31:9492–9498. doi: 10.1016/j.biomaterials.2010.08.06810.1016/j.biomaterials.2010.08.068 ↗
31. Liao HW, Hafner JH (2005) Gold nanorod bioconjugates. Chem Mater 17:4636–4641. doi: 10.1021/cm050935k10.1021/cm050935k ↗
32. Liopo A, Conjusteau A, Tsyboulski D, Ermolinsky B, Kazansky A, Oraevsky A (2012) Biocompatible gold nanorod conjugates for preclinical biomedical research. J Nanomed Nanotechnol. doi: 10.4172/2157-7439.S2-001
33. Maeda H (2001) The enhanced permeability and retention (EPR) effect in tumor vasculature: The key role of tumor-selective macromolecular drug targeting. Adv Enzyme Regul 41:189–20710.1016/S0065-2571(00)00013-3 ↗
34. Maeda H, Wu J, Sawa T, Matsumura Y, Hori K (2000) Tumor vascular permeability and the EPR effect in macromolecular therapeutics: a review. J Controlled Release 65:271–28410.1016/S0168-3659(99)00248-5 ↗
35. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3
36. Mundt A, Roeske J, Weichselbaum R (2000) Physical and biologic basis of radiation oncology. In: al Be (ed) Cancer medicine. BCDecker, Hamilton
37. Nikoobakht B, El-Sayed MA (2003) Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem Mater 15:1957–196210.1021/cm020732l ↗
38. Park J et al (2008) Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells. Opt Express 16:1590–159910.1364/OE.16.001590 ↗
39. Pattani VP, Tunnell JW (2012) Nanoparticle-mediated photothermal therapy: A comparative study of heating for different particle types. Lasers Surg Med 44:675–68410.1002/lsm.22072 ↗
40. Patterson MS, Chance B, Wilson BC (1989) Time resolved reflectance and transmittance for the non-invasive measurement of tissue optical properties. Appl Opt 28:2331–233610.1364/AO.28.002331 ↗
41. Pollock R (2000) Principles of Surgical Oncology. In: al Be (ed) Cancer Medicine. BCDecker, Hamilton
42. Szabó C (2005) Mechanisms of cell necrosis Critical care medicine 33:S530–S53410.1097/01.CCM.0000187002.88999.CF ↗
43. Tong L, Zhao Y, Huff TB, Hansen MN, Wei A, Cheng JX (2007) Gold nanorods mediate tumor cell death by compromising membrane integrity. Adv Mater 19:3136. doi: 10.1002/adma.20070197410.1002/adma.200701974 ↗
44. Trump BE, Berezesky IK, Chang SH, Phelps PC (1997a) The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol Pathol 25:8210.1177/019262339702500116 ↗
45. Trump BE, Berezesky IK, Chang SH, Phelps PC (1997b) The Pathways of Cell Death: Oncosis. Apoptosis, and Necrosis Toxicologic Pathology 25:82–88. doi: 10.1177/01926233970250011610.1177/019262339702500116 ↗
46. Wang DS, Hsu FY, Lin CW (2009) Surface plasmon effects on two photon luminescence of gold nanorods. Opt Express 17:11350–1135910.1364/OE.17.011350 ↗
47. Wang L et al (2011) Selective targeting of gold nanorods at the mitochondria of cancer cells: implications for cancer therapy. Nano Lett 11:772–780. doi: 10.1021/nl103992v10.1021/nl103992v ↗
48. Zharov VP, Galitovskaya EN, Johnson C, Kelly T (2005) Synergistic enhancement of selective nanophotothermolysis with gold nanoclusters: Potential for cancer therapy. Lasers Surg Med 37:219–226. doi: 10.1002/lsm.2022310.1002/lsm.20223 ↗