Advertisement

Journal of Cancer Research and Clinical Oncology

, Volume 145, Issue 1, pp 97–107 | Cite as

Combination of gold nanoparticles with low-LET irradiation: an approach to enhance DNA DSB induction in HT29 colorectal cancer stem-like cells

  • Mahdi Abbasian
  • Azam Baharlouei
  • Zahra Arab-BafraniEmail author
  • David A. Lightfoot
Original Article – Cancer Research
  • 67 Downloads

Abstract

Purpose

High-linear energy transfer (high LET) irradiation has significant cytotoxic effects on different cancerous stem-like cells (CSLCs) such as colorectal CSLCs. A review of the literature has indicated that the presence of gold nanoparticles (GNPs) enables low-LET irradiation to produce highly non-homogeneous dose distributions like high-LET irradiation. The purpose of this study was to evaluate the radioresponsiveness of HT29 colorectal CSLCs under low-LET irradiation (X-ray) and in the presence of GNPs.

Methods

Radioresponsiveness was evaluated using the ϒ-H2AX foci formation assay, the clonogenic assay, the cell cycle progression assay and analyses of radiobiological parameters.

Results

In the presence of GNPs, the survival fraction of HT29 CSLCs was significantly reduced and caused significant changes in the radiobiological parameters after irradiation. In addition, ϒ-H2AX assay showed that in the presence of GNPs, the persistent DNA double-strand breaks were significantly increased in irradiated HT29 CSLCs. The relative biological effectiveness value of GNPs with X-rays was about 1.6 for HT-29 CSLCs at the 10% of cell survival fraction (D10 level) when compared to X-rays alone.

Conclusion

Therefore, the combination of GNPs with X-ray irradiation has the potential to kill HT29 CSLCs greater than the X-ray alone, and may be considered as an alternative for high-LET irradiation.

Keywords

Cancer stem-like cell Gold nanoparticle DNA DSBs RBE value 

Notes

Acknowledgements

The authors are highly thankful to all technicians who provided support during the course of research. The part of this work was supported by Stem Cell Research Center, Golestan University of Medical Science (Grant no: 950818185).

Author contributions

ABZ and AM designed the research. ABZ, AM and BA performed the experiments. ABZ, AM, and LDA contributed to analysis and interpretation of data. AM and ABZ wrote the manuscript. All authors reviewed the manuscript.

Compliance with ethical standards

Conflict of interest

The author(s) declare no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Arab-Bafrani Z, Shahbazi-Gahrouei D, Abbasian M et al (2016) Multiple MTS assay as the alternative method to determine survival fraction of the irradiated HT-29 colon cancer cells. J Med Signals Sens 6:112–116Google Scholar
  2. Bodgi L, Canet A, Pujo-Menjouet L et al (2016) Mathematical models of radiation action on living cells: from the target theory to the modern approaches. A historical and critical review. J Theor Biol 394:93–101CrossRefGoogle Scholar
  3. Botchkina GI, Zuniga ES, Das MM et al (2010) New-generation taxoid SB-T-1214 inhibits stem cell-related gene expression in 3D cancer spheroids induced by purified colon tumor-initiating cells. Mol Cancer 9:1–12CrossRefGoogle Scholar
  4. Butterworth KT, Coulter JA, Jain S et al (2011) Evaluation of cytotoxicity and radiation enhancement using 1.9 nm gold particles: potential application for cancer therapy. Nanotechnology 21(29):295101CrossRefGoogle Scholar
  5. Chattopadhyay N, Cai Z, Kwon YL et al (2013) Molecularly targeted gold nanoparticles enhance the radiation response of breast cancer cells and tumor xenografts to X-radiation. Breast Cancer Res Treat 137:81–91CrossRefGoogle Scholar
  6. Chen W-S, Lee Y-J, Yu Y-C et al (2010) Enhancement of p53-mutant human colorectal cancer cells radiosensitivity by flavonoid fisetin. Int J Radiat Oncol Biol Phys 77:1527–1535CrossRefGoogle Scholar
  7. Chithrani DB, Jelveh S, Jalali F et al (2010) Gold nanoparticles as radiation sensitizers in cancer therapy. Radiat Res 173:719–728CrossRefGoogle Scholar
  8. Cui X, Oonishi K, Tsujii H et al (2011) Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res 71:3676–3687CrossRefGoogle Scholar
  9. Diaz A, Leon K (2011) Therapeutic approaches to target cancer stem cells. Cancers (Basel) 3:3331–3352CrossRefGoogle Scholar
  10. Diehn M, Cho RW, Lobo NA et al (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:780–783CrossRefGoogle Scholar
  11. Dunne AL, Price ME, Mothersill C et al (2003) Relationship between clonogenic radiosensitivity, radiation-induced apoptosis and DNA damage/repair in human colon cancer cells. Br J Cancer 89:2277–2283CrossRefGoogle Scholar
  12. Escherichia R, Billen D (2014) Free radical scavenging and the expression of potentially lethal damage in X-irradiated repair-deficient Escherichia coli. Radiat Res 111:354–360Google Scholar
  13. Eyler CE, Rich JN (2009) Survival of the fittest: cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26:2839–2845CrossRefGoogle Scholar
  14. Fanali C (2014) Cancer stem cells in colorectal cancer from pathogenesis to therapy: controversies and perspectives. World J Gastroenterol 20:923CrossRefGoogle Scholar
  15. Fang DD, Kim YJ, Lee CN et al (2010) Expansion of CD133(+) colon cancer cultures retaining stem cell properties to enable cancer stem cell target discovery. Br J Cancer 102:1265–1275CrossRefGoogle Scholar
  16. Fertil B, Dertinger H, Courdi A, Malaise EP (2012) Mean inactivation dose: a useful concept for intercomparison of human cell survival curves. Radiat Res 178:AV237–AV243CrossRefGoogle Scholar
  17. Frykholm G, Glimelius B, Richter S, Carlsson J (1991) Heterogeneity in antigenic expression and radiosensitivity in human colon carcinoma cell lines. In Vitro Cell Dev Biol 27A:900–906CrossRefGoogle Scholar
  18. Gadoue SM, Toomeh D, Zygmanski P, Sajo E (2017) Angular dose anisotropy around gold nanoparticles exposed to X-rays. Nanomed Nanotechnol Biol Med 13:1653–1661CrossRefGoogle Scholar
  19. Gandomani HS, Yousefi SM, Aghajani M et al (2017) Colorectal cancer in the world: incidence, mortality and risk factors. Biomed Res Ther 4:1656CrossRefGoogle Scholar
  20. Garza-Treviño EN, Said-Fernández SL, Martínez-Rodríguez HG (2015) Understanding the colon cancer stem cells and perspectives on treatment. Cancer Cell Int 15:2CrossRefGoogle Scholar
  21. Girard YK, Wang C, Ravi S et al (2013) A 3D fibrous scaffold inducing tumoroids: a platform for anticancer drug development. PLoS One 8:e75345CrossRefGoogle Scholar
  22. Goodhead DT (1994) Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int J Radiat Biol 65:7CrossRefGoogle Scholar
  23. Goodhead DT (1999) Mechanisms for the biological effectiveness of high-LET radiations. J Radiat Res 40(Suppl):1–13CrossRefGoogle Scholar
  24. Hada M, Georgakilas AG (2008) Formation of clustered DNA damage after high-LET irradiation: a review. J Radiat Res 49:203–210CrossRefGoogle Scholar
  25. Hall EJ, Willson S (1988) Radiobiology for the radiologist. Wolters Kluwer, PhiladelphiaGoogle Scholar
  26. Halperin EC, Perez CA, Brady LW (2007) Principles and practice of radiation oncology. Wolters-Kluwer, PhiladelphiaGoogle Scholar
  27. He Z, Subramaniam D, Zhang Z et al (2009) Honokiol radiosensitizes colorectal cancer cells: enhanced activity in cells with mismatch repair defects. AJP Gastrointest Liver Physiol 301:G929–G937CrossRefGoogle Scholar
  28. Held KD, Kawamura H, Kaminuma T et al (2016) Effects of charged particles on human tumor cells. Front Oncol 6:23CrossRefGoogle Scholar
  29. Hirota Y, Masunaga SI, Kondo N et al (2014) High linear-energy-transfer radiation can overcome radioresistance of glioma stem-like cells to low linear-energy-transfer radiation. J Radiat Res 55:75–83CrossRefGoogle Scholar
  30. Ismail IH, Wadhra TI, Hammarsten O (2007) An optimized method for detecting gamma-H2AX in blood cells reveals a significant interindividual variation in the gamma-H2AX response among humans. Nucleic Acids Res 35:e36CrossRefGoogle Scholar
  31. Jain S, Ch B, Coulter JA, Hounsell ARKT (2011) Cell-specific radiosensitization by gold nanoparticles at megavoltage radiation energies. Int J Radiat Oncol Biol Phys 79:531–539CrossRefGoogle Scholar
  32. Jamal M, Rath BH, Tsang PS et al (2012) The brain microenvironment preferentially enhances the. Neoplasia 14:150–158CrossRefGoogle Scholar
  33. Kahlert UD, Mooney SM, Natsumeda M et al (2017) Targeting cancer stem-like cells in glioblastoma and colorectal cancer through metabolic pathways. Int J Cancer 140:10–22CrossRefGoogle Scholar
  34. Khiari H, Hsairi M (2017) Colorectal cancer incidence and clinicopathological features in northern Tunisia 2007–2009. Color Cancer 6:131–141CrossRefGoogle Scholar
  35. Kim S, Rhee JG, Song X et al (2012) Breast cancer stem cell-like cells are more sensitive to ionizing radiation than non-stem cells: role of ATM. PLoS One 7:e50423CrossRefGoogle Scholar
  36. Kirkland SC (2009) Type I collagen inhibits differentiation and promotes a stem cell-like phenotype in human colorectal carcinoma cells. Br J Cancer 101:320–326CrossRefGoogle Scholar
  37. Larionov A, Krause A, Miller W (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinform 6:62CrossRefGoogle Scholar
  38. Li S-D, Howell SB (2010) CD44-targeted microparticles for delivery of cisplatin to peritoneal metastases. Mol Pharm 7:280–290CrossRefGoogle Scholar
  39. Liu Z, Xiong L, Ouyang G et al (2017) Investigation of copper cysteamine nanoparticles as a new type of radiosensitizers for colorectal carcinoma treatment. Sci Rep 7:1–11CrossRefGoogle Scholar
  40. Lundholm L, Hååg P, Zong D, Juntti T, Mörk B, Lewensohn RVK (2013) Resistance to DNA-damaging treatment in non-small cell lung cancer tumor-initiating cells involves reduced DNA-PK/ATM activation and diminished cell cycle arrest. Cell Death Dis 4:e478CrossRefGoogle Scholar
  41. Mahon E, Salvati A, Baldelli Bombelli F et al (2012) Designing the nanoparticle-biomolecule interface for “targeting and therapeutic delivery”. J Control Release 161:164–174CrossRefGoogle Scholar
  42. Martins-Neves SR, Lopes ÁO, Carmo A et al (2012) Therapeutic implications of an enriched cancer stem-like cell population in a human osteosarcoma cell line. BMC Cancer 12:139CrossRefGoogle Scholar
  43. Matsui Y, Asano T, Kenmochi T et al (2004) Effects of carbon-ion beams on human pancreatic cancer cell lines that differ in genetic status. Am J Clin Oncol 27:24–28CrossRefGoogle Scholar
  44. McMahon SJ, Hyland WB, Muir MF et al (2011a) Biological consequences of nanoscale energy deposition near irradiated heavy atom nanoparticles. Sci Rep 1:18CrossRefGoogle Scholar
  45. McMahon SJ, Hyland WB, Muir MF et al (2011b) Nanodosimetric effects of gold nanoparticles in megavoltage radiation therapy. Radiother Oncol 100:412–416CrossRefGoogle Scholar
  46. Menegakis A, Yaromina A, Eicheler W et al (2009) Prediction of clonogenic cell survival curves based on the number of residual DNA double strand breaks measured by γH2AX staining. Int J Radiat Biol 85:1032–1041CrossRefGoogle Scholar
  47. Moncharmont C, Levy A, Gilormini M et al (2012) Targeting a cornerstone of radiation resistance: cancer stem cell. Cancer Lett 322:139–147CrossRefGoogle Scholar
  48. Moore N, Lyle S (2011) Quiescent, slow-cycling stem cell populations in cancer: a review of the evidence and discussion of significance. J Oncol 2011:396076CrossRefGoogle Scholar
  49. Nguyen GH, Murph MM, Chang JY (2011) Cancer stem cell radioresistance and enrichment: where frontline radiation therapy may fail in lung and esophageal cancers. Cancers (Basel) 3:1232–1252CrossRefGoogle Scholar
  50. Niemantsverdriet M, Goethem Van M et al (2012) High and low LET radiation differentially induce normal tissue damage signals. Radiat Oncol Biol 83:1291–1297CrossRefGoogle Scholar
  51. Ning S-T, Lee S-Y, Wei M-F et al (2016) Targeting colorectal cancer stem-like cells with anti-CD133 antibody-conjugated SN-38 nanoparticles. ACS Appl Mater Interfaces 8:17793–17804CrossRefGoogle Scholar
  52. Okayasu R (2012) Repair of DNA damage induced by accelerated heavy ions—a mini review. Int J Cancer 130:991–1000CrossRefGoogle Scholar
  53. Okayasu R, Okada M, Okabe A et al (2006) Repair of DNA damage induced by accelerated heavy ions in mammalian cells proficient and deficient in the non-homologous end-joining pathway. Radiat Res 165:59–67CrossRefGoogle Scholar
  54. Oonishi K, Cui X, Hirakawa H et al (2012) Different effects of carbon ion beams and X-rays on clonogenic survival and DNA repair in human pancreatic cancer stem-like cells. Radiother Oncol 105:258–265CrossRefGoogle Scholar
  55. Parfitt SL, Milner RJ, Salute ME et al (2011) Radiosensitivity and capacity for radiation-induced sublethal damage repair of canine transitional cell carcinoma (TCC) cell lines. Vet Comp Oncol 9:232–240CrossRefGoogle Scholar
  56. Phillips TM, Mcbride WH, Pajonk F (2006) The response of CD24 −/low/CD44 + breast cancer—initiating cells to radiation. J Natl Cancer Inst 98:1777–1785CrossRefGoogle Scholar
  57. Radonić A, Thulke S, Mackay IM et al (2004) Guideline to reference gene selection for quantitative real-time PCR. Biochem Biophys Res Commun 313:856–862CrossRefGoogle Scholar
  58. Rao G, Liu H, Li B et al (2013) Establishment of a human colorectal cancer cell line P6C with stem cell properties and resistance to chemotherapeutic drugs. Acta Pharmacol Sin 34:793–804CrossRefGoogle Scholar
  59. Roy S, Majumdar AP (2012) Signaling in colon cancer stem cells. J Mol Signal 7:11CrossRefGoogle Scholar
  60. Saberi A, Shahbazi-Gahrouei D, Abbasian M et al (2016) Gold nanoparticles in combination with megavoltage radiation energy increased radiosensitization and apoptosis in colon cancer HT-29 cells. Int J Radiat Biol 93:315–323CrossRefGoogle Scholar
  61. Sai S, Vares G, Kim EH et al (2015) Carbon ion beam combined with cisplatin effectively disrupts triple negative breast cancer stem-like cells in vitro. Mol Cancer 14:166CrossRefGoogle Scholar
  62. Schmid TE, Dollinger G, Beisker W et al (2010) Differences in the kinetics of γ-H2AX fluorescence decay after exposure to low and high LET radiation. Int J Radiat Biol 86:682–691CrossRefGoogle Scholar
  63. Siegel R, DeSantis C, Jemal A (2014) Colorectal cancer statistics, 2014. CA Cancer J Clin 64:104–117CrossRefGoogle Scholar
  64. Sun L, Cabarcas SM (2012) Radioresistance and cancer stem cells: survival of the fittest. J Carcinog Mutagen 1:1–12Google Scholar
  65. Suzuki M, Kase Y, Yamaguchi H et al (2000) Relative biological effectiveness for cell-killing effect on various human cell lines irradiated with heavy-ion medical accelerator in Chiba (HIMAC) carbon-ion beams. Int J Radiat Oncol 48:241–250CrossRefGoogle Scholar
  66. Takahashi A, Ma H, Nakagawa A et al (2014a) Carbon-ion beams efficiently induce cell killing in X-ray resistant human squamous tongue cancer cells. IJMPCERO 3:133–142CrossRefGoogle Scholar
  67. Takahashi M, Hirakawa H, Yajima H et al (2014b) Carbon ion beam is more effective to induce cell death in sphere-type A172 human glioblastoma cells compared with X-rays. Int J Radiat Biol 90:1125–1132CrossRefGoogle Scholar
  68. Taneja N, Davis M, Choy JS et al (2004) Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J Biol Chem 279:2273–2280CrossRefGoogle Scholar
  69. Tazi I, Nafil H, Mahmal L (2011) Monoclonal antibodies in hematological malignancies: past, present and future. J Cancer Res Ther 7:399–407CrossRefGoogle Scholar
  70. van der Meel R, Oliveira S, Altintas I et al (2012) Tumor-targeted nanobullets: anti-EGFR nanobody-liposomes loaded with anti-IGF-1R kinase inhibitor for cancer treatment. J Control Release 159:281–289CrossRefGoogle Scholar
  71. Wang L, Su W, Liu Z et al (2012) CD44 antibody-targeted liposomal nanoparticles for molecular imaging and therapy of hepatocellular carcinoma. Biomaterials 33:5107–5114CrossRefGoogle Scholar
  72. Wei B, Han X-Y, Qi C-L et al (2012) Coaction of spheroid-derived stem-like cells and endothelial progenitor cells promotes development of colon cancer. PLoS One 7:e39069CrossRefGoogle Scholar
  73. Weichselbaum RR, Beckett MA, Vijayakumar S et al (1990) Radiobiological characterization of head and neck and sarcoma cells derived from patients prior to radiotherapy. Int J Radiat Oncol Biol Phys 19:313–319CrossRefGoogle Scholar
  74. Wiskirchen J, Dittmann H, Kehlbach R et al (2001) Rhenium-188 for inhibition of human aortic smooth muscle cell proliferation. Int J Radiat Oncol Biol Phys 49:809–815CrossRefGoogle Scholar
  75. Xu W, Luo T, Pang B et al (2012) The radiosensitization of melanoma cells by gold nanorods irradiated with MV X-ray. Nano Biomed Eng 4:6–11CrossRefGoogle Scholar
  76. Yan C, Luo L, Goto S et al (2016) Enhanced autophagy in colorectal cancer stem cells does not contribute to radio-resistance. Oncotarget 7:45112Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Stem Cell Research CenterGolestan University of Medical ScienceGorgānIran
  2. 2.Department of Biotechnology, College of AgricultureIsfahan University of TechnologyIsfahanIran
  3. 3.Department of MicrobiologySouthern Illinois University at CarbondaleCarbondaleUSA
  4. 4.Department of Biochemistry and Biophysics, Faculty of MedicineGolestan University of Medical SciencesGorgānIran
  5. 5.Department of Plant, Soil and Agricultural Systems, Plant Biotechnology and Genome Core-FacilitySouthern Illinois University at CarbondaleCarbondaleUSA
  6. 6.Metabolic Disorders Research CenterGolestan University of Medical SciencesGorgānIran

Personalised recommendations