Advertisement

Role of apoptosis and necrosis in cell death induced by nanoparticle-mediated photothermal therapy

  • Varun P. Pattani
  • Jay Shah
  • Alexandra Atalis
  • Anirudh Sharma
  • James W. Tunnell
Research Paper

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.

Keywords

Gold nanoparticles Gold nanorods Photothermal therapy (PTT) Plasmon resonance Two-photon imaging Cancer therapy 

Notes

Acknowledgments

We acknowledge the National Institutes of Health (Grant R01CA132032) for the financial support of this work. Additionally, we acknowledge the two-photon microscope use in the project described was supported by Award Number S10RR027950 from the National Center for Research Resources. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center for Research Resources or the National Institutes of Health.

Conflict of interest

The authors have no conflicts of interest to report.

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.200801546 CrossRefGoogle Scholar
  2. Brioude A, Jiang XC, Pileni MP (2005) Optical properties of gold nanorods: DDA simulations supported by experiments. J Phys Chem B 109:13138–13142CrossRefGoogle Scholar
  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.2010.01.140 CrossRefGoogle Scholar
  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.201001109 CrossRefGoogle Scholar
  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 113:12090–12094CrossRefGoogle Scholar
  6. Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73CrossRefGoogle Scholar
  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.2008.04.026 CrossRefGoogle Scholar
  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/nl062962v CrossRefGoogle Scholar
  9. El-Sayed MA (2001) Some interesting properties of metals confined in time and nanometer space of different shapes. Acc Chem Res 34:257–264CrossRefGoogle Scholar
  10. Frei III E AK (2000) Principles of dose, schedule, and combination chemotherapy. In: al Be (ed) Cancer medicine. BCDecker, HamiltonGoogle Scholar
  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 2:574–577CrossRefGoogle Scholar
  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 57:3823–3829Google Scholar
  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 8:808–815Google Scholar
  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: 10.1177/1091581812465969 CrossRefGoogle Scholar
  15. Green DR, Reed JC (1998) Mitochondria and apoptosis. Science 281:1309–1312CrossRefGoogle Scholar
  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 52:237–245CrossRefGoogle Scholar
  17. Helmchen F, Denk W (2002) Deep tissue two-photon microscopy. Nature 12(5):593–601Google Scholar
  18. Howlader N et al (2012) SEER cancer statistics review, 1975–2009 (vintage 2009 populations). National Cancer Institute, BethesdaGoogle Scholar
  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/ja057254a CrossRefGoogle Scholar
  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: 10.1117/1.3486538 CrossRefGoogle Scholar
  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 185:249–258CrossRefGoogle Scholar
  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/jp057170o CrossRefGoogle Scholar
  23. Jana NR, Gearheart L, Murphy CJ (2001) Wet chemical synthesis of high aspect ratio cylindrical gold nanorods. J Phys Chem B 105:4065–4067CrossRefGoogle Scholar
  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 40:1647–1671CrossRefGoogle Scholar
  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 98:77–83CrossRefGoogle Scholar
  26. Khlebtsov B, Zharov V, Melnikov A, Tuchin V, Khlebtsov N (2006) Optical amplification of photothermal therapy with gold nanoparticles and nanoclusters. Nanotechnology 17:5167CrossRefGoogle Scholar
  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.2008.1 CrossRefGoogle Scholar
  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/jp054385p CrossRefGoogle Scholar
  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.200801788 Google Scholar
  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.2010.08.068 CrossRefGoogle Scholar
  31. Liao HW, Hafner JH (2005) Gold nanorod bioconjugates. Chem Mater 17:4636–4641. doi: 10.1021/cm050935k CrossRefGoogle Scholar
  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 Google Scholar
  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 41:189–207CrossRefGoogle Scholar
  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 65:271–284CrossRefGoogle Scholar
  35. Majno G, Joris I (1995) Apoptosis, oncosis, and necrosis. An overview of cell death. Am J Pathol 146:3Google Scholar
  36. Mundt A, Roeske J, Weichselbaum R (2000) Physical and biologic basis of radiation oncology. In: al Be (ed) Cancer medicine. BCDecker, HamiltonGoogle Scholar
  37. Nikoobakht B, El-Sayed MA (2003) Preparation and growth mechanism of gold nanorods (NRs) using seed-mediated growth method. Chem Mater 15:1957–1962CrossRefGoogle Scholar
  38. Park J et al (2008) Two-photon-induced photoluminescence imaging of tumors using near-infrared excited gold nanoshells. Opt Express 16:1590–1599CrossRefGoogle Scholar
  39. Pattani VP, Tunnell JW (2012) Nanoparticle-mediated photothermal therapy: A comparative study of heating for different particle types. Lasers Surg Med 44:675–684CrossRefGoogle Scholar
  40. Patterson MS, Chance B, Wilson BC (1989) Time resolved reflectance and transmittance for the non-invasive measurement of tissue optical properties. Appl Opt 28:2331–2336CrossRefGoogle Scholar
  41. Pollock R (2000) Principles of Surgical Oncology. In: al Be (ed) Cancer Medicine. BCDecker, HamiltonGoogle Scholar
  42. Szabó C (2005) Mechanisms of cell necrosis Critical care medicine 33:S530–S534CrossRefGoogle Scholar
  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.200701974 CrossRefGoogle Scholar
  44. Trump BE, Berezesky IK, Chang SH, Phelps PC (1997a) The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol Pathol 25:82CrossRefGoogle Scholar
  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: 10.1177/019262339702500116 CrossRefGoogle Scholar
  46. Wang DS, Hsu FY, Lin CW (2009) Surface plasmon effects on two photon luminescence of gold nanorods. Opt Express 17:11350–11359CrossRefGoogle Scholar
  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/nl103992v CrossRefGoogle Scholar
  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.20223 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Varun P. Pattani
    • 1
  • Jay Shah
    • 1
  • Alexandra Atalis
    • 1
  • Anirudh Sharma
    • 1
  • James W. Tunnell
    • 1
  1. 1.Department of Biomedical EngineeringThe University of Texas at AustinAustinUSA

Personalised recommendations