Skip to main content
SpringerLink
Log in

In vitro activity studies of hyperthermal near-infrared nanoGUMBOS in MDA-MB-231 breast cancer cells

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

A new kind of material called nanoGUMBOS, comprised entirely of cations and anions, has been developed by pairing various functional ions that exhibit fluorescence activity with biocompatible ions, in a process very much akin to that employed in ionic liquid chemistry. In the present study, spectral and biological properties of NIR absorbing nanoGUMBOS were evaluated using electron microscopy, dynamic light scattering, absorbance, thermal imaging, and live/dead fluorescence assays in conjunction with malignant MDA-MB-231 and non-malignant HS-578-BST epithelial human breast cells. The primary focus of this study was to maximize heat generation using NIR laser irradiation and minimize non-specific cytotoxicity using biocompatible constituent ions (e.g. amino acids, vitamins, or organic acids). Concurrently, in order to generate highly responsive nanomaterials for NIR-laser-triggered hyperthermia, optimization of the nanoparticle size, shape, and uniformity was carried out. Evaluation of data from hyperthermal studies of NIR absorbing nanoGUMBOS shows that these materials can achieve temperatures above the threshold for killing cancerous cells. Additionally, in vitro cell based assays demonstrated their promising hyperthermal effects on cancer derived epithelial cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Notes and references

  1. American Cancer Society. Cancer Facts & Figures 2014. http://www.cancer.org/acs/groups/content/@research/documents/document/acspc-041780.pdf (accessed May 26, 2014).

    Google Scholar 

  2. D. A. Berry, K. A. Cronin, S. K. Plevritis, D. G. Fryback, L. Clarke, M. Zelen, J. S. Mandelblatt, A. Y. Yakovlev, J. D. F. Habbema, E. J. Feuer and C. Collaborators, Effect of Screening and Adjuvant Therapy on Mortality from Breast Cancer, N. Engl. J. Med., 2005, 353, 1784–1792.

    Article  CAS  PubMed  Google Scholar 

  3. E. S. Glazer and S. A. Curley, The Ongoing History of Thermal Therapy for Cancer, Surg. Oncol. Clin. N. Am., 2011, 20, 229–235.

    Article  PubMed  Google Scholar 

  4. R. Kitture, S. Ghosh, P. Kulkarni, X. L. Liu, D. Maity, S. I. Patil, D. Jun, Y. Dushing, S. L. Laware, B. A. Chopade and S. N. Kale, Fe3O4-Citrate-Curcumin: Promising Conjugates for Superoxide Scavenging, Tumor Suppression and Cancer Hyperthermia, J. Appl. Phys.. 2012, 111, 064702.

    Article  CAS  Google Scholar 

  5. D. K. Kim, M. S. Amin, S. Elborai, S. H. Lee, Y. Koseoglu and M. Muhammed, Energy Absorption of Superparamagnetic Iron Oxide Nanoparticles by Microwave Irradiation, J. Appl. Phys., 2005, 97, 10J510.

    Article  CAS  Google Scholar 

  6. Z. Fan, D. Senapati, S. A. Khan, A. K. Singh, A. Hamme, B. Yust, D. Sardar and P. C. Ray, Popcorn-Shaped Magnetic CorePlasmonic Shell Multifunctional Nanoparticles for the Targeted Magnetic Separation and Enrichment, Label-Free SERS Imaging, and Photothermal Destruction of Multidrug-Resistant Bacteria, Chem.–Eur. J., 2013, 19, 2839–2847.

    Article  CAS  PubMed  Google Scholar 

  7. K. E. Peyer, S. Tottori, F. M. Qiu, L. Zhang and B. J. Nelson, Magnetic Helical Micromachines, Chem.–Eur. J., 2013, 19, 28–38.

    Article  CAS  PubMed  Google Scholar 

  8. K. H. Bae, M. Park, M. J. Do, N. Lee, J. H. Ryu, G. W. Kim, C. Kim, T. G. Park and T. Hyeon, Chitosan Oligosaccharide-Stabilized Ferrimagnetic Iron Oxide Nanocubes for Magnetically Modulated Cancer Hyperthermia, ACS Nano, 2012, 6, 5266–5273.

    Article  CAS  PubMed  Google Scholar 

  9. F. P. Gao, Y. Y. Cai, J. Zhou, X. X. Xie, W. W. Ouyang, Y. H. Zhang, X. F. Wang, X. D. Zhang, X. W. Wang, L. Y. Zhao and J. T. Tang, Pullulan Acetate Coated Magnetite Nanoparticles for Hyper-Thermia: Preparation, Characterization and In Vitro Experiments, Nano Res., 2010, 3, 23–31.

    Article  CAS  Google Scholar 

  10. D.-H. Kim, E. A. Vitol, J. Liu, S. Balasubramanian, D. J. Gosztola, E. E. Cohen, V. Novosad and E. A. Rozhkova, Stimuli-Responsive Magnetic Nanomicelles as Multifunctional Heat and Cargo Delivery Vehicles, Langmuir, 2013, 29, 7425–7432.

    Article  CAS  PubMed  Google Scholar 

  11. J. Li, J. Han, T. Xu, C. Guo, X. Bu, H. Zhang, L. Wang, H. Sun and B. Yang, Coating Urchinlike Gold Nanoparticles with Polypyrrole Thin Shells to Produce Photothermal Agents with High Stability and Photothermal Transduction Efficiency, Langmuir, 2013, 29, 7102–7110.

    Article  CAS  PubMed  Google Scholar 

  12. Y. Y. Su, X. P. Wei, F. Peng, Y. L. Zhong, Y. M. Lu, S. Su, T. T. Xu, S. T. Lee and Y. He, Gold Nanoparticles-Decorated Silicon Nanowires as Highly Efficient Near-Infrared Hyperthermia Agents for Cancer Cells Destruction, Nano Lett., 2012, 12, 1845–1850.

    Article  CAS  PubMed  Google Scholar 

  13. J. T. Robinson, K. Welsher, S. M. Tabakman, S. P. Sherlock, H. L. Wang, R. Luong and H. J. Dai, High Performance In Vivo Near-IR (<1 µm) Imaging and Photothermal Cancer Therapy with Carbon Nanotubes, Nano Res., 2010, 3, 779–793.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. X. H. Huang, I. H. El-Sayed, W. Qian and M. A. El-Sayed, Cancer Cell Imaging and Photothermal Therapy in the Near-Infrared Region by Using Gold Nanorods, J. Am. Chem. Soc., 2006, 128, 2115–2120.

    Article  CAS  PubMed  Google Scholar 

  15. L. R. Hirsch, R. J. Stafford, J. A. Bankson, S. R. Sershen, B. Rivera, R. E. Price, J. D. Hazle, N. J. Halas and J. L. West, Nanoshell-Mediated Near-Infrared Thermal Therapy of Tumors Under Magnetic Resonance Guidance, Proc. Natl. Acad. Sci. U. S. A., 2003, 100, 13549–13554.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. L. J. Meng, L. Y. Niu, L. Li, Q. H. Lu, Z. F. Fei and P. J. Dyson, Gold Nanoparticles Grown on Ionic Liquid-Functionalized Single-Walled Carbon Nanotubes: New Materials for Photothermal Therapy, Chem.–Eur. J., 2012, 18, 13314–13319.

    Article  CAS  PubMed  Google Scholar 

  17. P. Yang, Q. Z. Xu, S. Y. Jin, Y. Lu, Y. Zhao and S. H. Yu, Synthesis of Multifunctional Ag@Au@Phenol Formaldehyde Resin Particles Loaded with Folic Acids for Photothermal Therapy, Chem.–Eur. J., 2012, 18, 9294–9299.

    Article  CAS  PubMed  Google Scholar 

  18. B. Pelaz, V. Grazu, A. Ibarra, C. Magen, P. del Pino, J. M. de la Fuente, Tailoring the Synthesis and Heating Ability of Gold Nanoprisms for Bioapplications, Langmuir, 2012, 28, 8965–8970.

    Article  CAS  PubMed  Google Scholar 

  19. J. F. Lovell, C. S. Jin, E. Huynh, H. L. Jin, C. Kim, J. L. Rubinstein, W. C. W. Chan, W. G. Cao, L. V. Wang and G. Zheng, Porphysome Nanovesicles Generated by Porphyrin Bilayers for Use as Multimodal Biophotonic Contrast Agents, Nat. Mater., 2011, 10, 324–332.

    Article  CAS  PubMed  Google Scholar 

  20. S. Lal, S. E. Clare and N. J. Halas, Nanoshell-Enabled Photothermal Cancer Therapy: Impending Clinical Impact, Acc. Chem. Res., 2008, 41, 1842–1851.

    Article  CAS  PubMed  Google Scholar 

  21. H. W. Huang and C. T. Liauh, Review: Therapeutical Applications of Heat in Cancer Therapy, J. Med. Biol. Eng., 2012, 32, 1–10.

    Article  Google Scholar 

  22. A. N. Bashkatov, E. A. Genina, V. I. Kochubey and V. V. Tuchin, Optical Properties of Human Skin, Subcutaneous and Mucous Tissues in the Wavelength Range from 400 to 2000 nm, J. Phys. D: Appl. Phys., 2005, 38, 2543–2555.

    Article  CAS  Google Scholar 

  23. X. S. Li, G. L. Ferrel, M. C. Guerra, T. Hode, J. A. Lunn, O. Adalsteinsson, R. E. Nordquist, H. Liu and W. R. Chen, Preliminary Safety and Efficacy Results of Laser Immunotherapy for the Treatment of Metastatic Breast Cancer Patients, Photochem. Photobiol. Sci., 2011, 10, 817–821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. B. Sivakumar, R. G. Aswathy, Y. Nagaoka, M. Suzuki, T. Fukuda, Y. Yoshida, T. Maekawa and D. N. Sakthikumar, Multifunctional Carboxymethyl Cellulose-Based Magnetic Nanovector as a Theragnostic System for Folate Receptor Targeted Chemotherapy, Imaging, and Hyperthermia against Cancer, Langmuir, 2013, 29, 3453–3466.

    Article  CAS  PubMed  Google Scholar 

  25. D. Bhattacharya, M. Das, D. Mishra, I. Banerjee, S. K. Sahu, T. K. Maiti and P. Pramanik, Folate Receptor Targeted, Carboxymethyl Chitosan Functionalized Iron Oxide Nanoparticles: A Novel Ultradispersed Nanoconjugates for Bimodal Imaging, Nanoscale, 2011, 3, 1653–1662.

    Article  CAS  PubMed  Google Scholar 

  26. G. M. van Dam, G. Themelis, L. M. A. Crane, N. J. Harlaar, R. G. Pleijhuis, W. Kelder, A. Sarantopoulos, J. S. de Jong, H. J. G. Arts, A. G. J. van der Zee, J. Bart, P. S. Low and V. Ntziachristos, Intraoperative Tumor-Specific Fluorescence Imaging in Ovarian Cancer by Folate Receptor-Alpha Targeting: First In-Human Results, Nat. Med., 2011, 17, 1315–U1202.

    Article  PubMed  CAS  Google Scholar 

  27. J. E. Rosen, L. Chan, D. B. Shieh and F. X. Gu, Iron Oxide Nanoparticles for Targeted Cancer Imaging and Diagnostics, Nanomed. Nanotechnol. Biol. Med., 2012, 8, 275–290.

    Article  CAS  Google Scholar 

  28. M. Liong, J. Lu, M. Kovochich, T. Xia, S. G. Ruehm, A. E. Nel, F. Tamanoi and J. I. Zink, Multifunctional Inorganic Nanoparticles for Imaging, Targeting, and Drug Delivery, ACS Nano, 2008, 2, 889–896.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. K. Kaaki, K. Herve-Aubert, M. Chiper, A. Shkilnyy, M. Souce, R. Benoit, A. Paillard, P. Dubois, M. L. Saboungi and I. Chourpa, Magnetic Nanocarriers of Doxorubicin Coated with Poly(ethylene glycol) and Folic Acid: Relation between Coating Structure, Surface Properties, Colloidal Stability, and Cancer Cell Targeting, Langmuir, 2012, 28, 1496–1505.

    Article  CAS  PubMed  Google Scholar 

  30. D. K. Bwambok, B. El-Zahab, S. K. Challa, M. Li, L. Chandler, G. A. Baker and I. M. Warner, Near-Infrared Fluorescent NanoGUMBOS for Biomedical Imaging, ACS Nano, 2009, 3, 3854–3860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. S. L. de Rooy, B. El-Zahab, M. Li, S. Das, E. Broering, L. Chandler and I. M. Warner, Fluorescent One-Dimensional Nanostructures from a Group of Uniform Materials Based on Organic Salts, Chem. Commun., 2011, 47, 8916–8918.

    Article  CAS  Google Scholar 

  32. D. K. Bwambok, S. K. Challa, M. Lowry and I. M. Warner, Amino Acid-Based Fluorescent Chiral Ionic Liquid for Enantiomeric Recognition, Anal. Chem., 2010, 82, 5028–5037.

    Article  CAS  PubMed  Google Scholar 

  33. M. Li, G. M. Ganea, C. F. Lu, S. L. De Rooy, B. El-Zahab, V. E. Fernand, R. Y. Jin, S. Aggarwal and I. M. Warner, Lipophilic Phosphonium-Lanthanide Compounds with Magnetic, Luminescent, and Tumor Targeting Properties, J. Inorg. Biochem., 2012, 107, 40–46.

    Article  CAS  PubMed  Google Scholar 

  34. A. Tesfai, B. El-Zahab, A. T. Kelley, M. Li, J. C. Garno, G. A. Baker and I. M. Warner, Magnetic and Nonmagnetic Nanoparticles from a Group of Uniform Materials Based on Organic Salts, ACS Nano, 2009, 3, 3244–3250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. M. Li, S. L. De Rooy, D. K. Bwambok, B. El-Zahab, J. F. DiTusa and I. M. Warner, Magnetic Chiral Ionic Liquids Derived from Amino Acids, Chem. Commun., 2009, 6922–6924.

    Google Scholar 

  36. S. L. de Rooy, M. Li, D. K. Bwambok, B. El-Zahab, S. Challa and I. M. Warner, Ephedrinium-Based Protic Chiral Ionic Liquids for Enantiomeric Recognition, Chirality, 2011, 23, 54–62.

    Article  PubMed  CAS  Google Scholar 

  37. J. C. Dumke, A. Qureshi, A. Hamdan, B. El-Zahab, S. Das, D. J. Hayes, D. Boldor, K. Rupnik and I. M. Warner, Photothermal Response of Near-Infrared Absorbing NanoGUMBOS, Appl. Spectrosc., 2014, 68, 340–352.

    Article  CAS  PubMed  Google Scholar 

  38. P. K. S. Magut, S. Das, V. E. Fernand, J. Losso, K. McDonough, B. M. Naylor, S. Aggarwal and I. M. Warner, Tunable Cytotoxicity of Rhodamine 6G via Anion Variations, J. Am. Chem. Soc., 2013, 135, 15873–15879.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. M. R. Cole, M. Li, B. El-Zahab, M. E. Janes, D. Hayes and I. M. Warner, Design, Synthesis, and Biological Evaluation of beta-Lactam Antibiotic-Based Imidazolium- and Pyridinium-Type Ionic Liquids, Chem. Biol. Drug Des., 2011, 78, 33–41.

    Article  CAS  PubMed  Google Scholar 

  40. A. N. Jordan, S. Das, N. Siraj, S. L. de Rooy, M. Li, B. El-Zahab, L. Chandler, G. A. Baker and I. M. Warner, Anion-Controlled Morphologies and Spectral Features of Cyanine-Based NanoGUMBOS - An Improved Photosensitizer, Nanoscale, 2012, 4, 5031–5038.

    Article  CAS  PubMed  Google Scholar 

  41. B. P. Regmi, J. Monk, B. El-Zahab, S. Das, F. R. Hung, D. J. Hayes and I. M. Warner, A Novel Composite Film for Detection and Molecular Weight Determination of Organic Vapors, J. Mater. Chem., 2012, 22, 13732–13741.

    Article  CAS  Google Scholar 

  42. A. Kumar, H. L. Ma, X. Zhang, K. Y. Huang, S. B. Jin, J. Liu, T. Wei, W. P. Cao, G. Z. Zou and X. J. Liang, Gold Nanoparticles Functionalized with Therapeutic and Targeted Peptides for Cancer Treatment, Biomaterials, 2012, 33, 1180–1189.

    Article  CAS  PubMed  Google Scholar 

  43. M. K. K. Oo, Y. M. Yang, Y. Hu, M. Gomez, H. Du and H. J. Wang, Gold Nanoparticle-Enhanced and Size-Dependent Generation of Reactive Oxygen Species from Protoporphyrin IX, ACS Nano, 2012, 6, 1939–1947.

    Article  CAS  Google Scholar 

  44. L. C. Kennedy, L. R. Bickford, N. A. Lewinski, A. J. Coughlin, Y. Hu, E. S. Day, J. L. West and R. A. Drezek, A New Era for Cancer Treatment: Gold-Nanoparticle-Mediated Thermal Therapies, Small, 2011, 7, 169–183.

    Article  CAS  PubMed  Google Scholar 

  45. B. N. Khlebtsov, E. V. Panfilova, G. S. Terentyuk, I. L. Maksimova, A. V. Ivanov and N. G. Khlebtsov, Plasmonic Nanopowders for Photothermal Therapy of Tumors, Langmuir, 2012, 28, 8994–9002.

    Article  CAS  PubMed  Google Scholar 

  46. H. Y. Liu, T. L. Liu, X. L. Wu, L. L. Li, L. F. Tan, D. Chen and F. Q. Tang, Targeting Gold Nanoshells on Silica Nanorattles: a Drug Cocktail to Fight Breast Tumors via a Single Irradiation with Near-Infrared Laser Light, Adv. Mater., 2012, 24, 755–761.

    Article  CAS  PubMed  Google Scholar 

  47. P. Russo, A Practical Minicourse in Dynamic Light Scattering, http://msg.lsu.edu/howto/DLS_Minicourse/DLS_Minicourse.pdf (accessed Oct 20, 2013).

    Google Scholar 

  48. X. D. Xu and M. B. Cortie, Shape Change and Color Gamut in Gold Nanorods, Dumbbells, and Dog Bones, Adv. Funct. Mater., 2006, 16, 2170–2176.

    Article  CAS  Google Scholar 

  49. D. B. Xiao, X. Lu, W. S. Yang, H. B. Fu, Z. G. Shuai, Y. Fang and J. N. Yao, Size-Tunable Emission from 1,3-Diphenyl-5-(2-anthryl)-2-pyrazoline Nanoparticles, J. Am. Chem. Soc., 2003, 125, 6740–6745.

    Article  CAS  PubMed  Google Scholar 

  50. R. S. Huang, S. W. Duan, W. K. Bleibel, E. O. Kistner, W. Zhang, T. A. Clark, T. X. Chen, A. C. Schweitzer, J. E. Blume, N. J. Cox and M. E. Dolan, A Genome-Wide Approach to Identify Genetic Variants that Contribute to Etoposide-Induced Cytotoxicity, Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 9758–9763.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. I. M. Tynga, N. N. Houreld and H. Abrahamse, The Primary Subcellular Localization of Zinc Phthalocyanine and its Cellular Impact on Viability, Proliferation and Structure of Breast Cancer Cells (MCF-7), J. Photochem. Photobiol., B, 2013, 120, 171–176.

    Article  CAS  Google Scholar 

  52. J. Byrne, A Digest of 20 Years’ Experience in the Treatment of Cancer of the Uterus by Galvanocautery, Am. J. Obstet. Gynecol., 1899, 22, 1052.

    Google Scholar 

  53. L. Loeb, Further Investigations in Transplantation of Tumors, J. Med. Res., 1902, 8, 44–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. H. C. Huang, K. Rege and J. J. Heys, Spatiotemporal Temperature Distribution and Cancer Cell Death in Response to Extracellular Hyperthermia Induced by Gold Nanorods, ACS Nano, 2010, 4, 2892–2900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. J. F. Zhou, L. J. Meng and Q. H. Lu, Core@Shell Nanostructures for Photothermal Conversion: Tunable Noble Metal Nanoshells on Cross-Linked Polymer Submicrospheres, J. Mater. Chem., 2010, 20, 5493–5498.

    Article  CAS  Google Scholar 

  56. E. J. Moon, P. Sonveaux, P. E. Porporato, P. Danhier, B. Gallez, I. Batinic-Haberle, Y. C. Nien, T. Schroeder and M. W. Dewhirst, NADPH Oxidase-Mediated Reactive Oxygen Species Production Activates Hypoxia-Inducible Factor-1 (HIF-1) via the ERK Pathway After Hyperthermia Treatment, Proc. Natl. Acad. Sci. U. S. A., 2010, 107, 20477–20482.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Z. C. Wang, F. Cai, X. Y. Chen, M. H. Luo, L. L. Hu and Y. Lu, The Role of Mitochondria-Derived Reactive Oxygen Species in Hyperthermia-Induced Platelet Apoptosis, PLoS One, 2013, 8, e75044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. K. Hayashi, M. Moriya, W. Sakamoto and T. Yogo, Chemoselective Synthesis of Folic Acid-Functionalized Magnetite Nanoparticles via Click Chemistry for Magnetic Hyperthermia, Chem. Mater., 2009, 21, 1318–1325.

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. Bilal El-Zahab

    Present address: Department of Mechanical and Materials Engineering, Florida International University, Miami, FL, 33174, USA

Authors and Affiliations

  1. Department of Chemistry, Louisiana State University, Baton Rouge, LA, 70803, USA

    Jonathan C. Dumke, Suzana Hamdan, Kresimir Rupnik, Bilal El-Zahab & Isiah M. Warner

  2. Department of Biological and Agricultural Engineering, Louisiana State University, Baton Rouge, LA, 70803, USA

    Ammar Qureshi & Daniel J. Hayes

Authors
  1. Jonathan C. Dumke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ammar Qureshi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Suzana Hamdan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kresimir Rupnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bilal El-Zahab
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniel J. Hayes
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Isiah M. Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isiah M. Warner.

Additional information

Electronic supplementary information (ESI) available: ESI MS, 19F NMR, the absorbance spectrum for solubility and cellular uptake, cytotoxicity and photothermia tables, and the LC50 graph for the nanoGUMBOS. See DOI: 10.1039/c4pp00030g

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dumke, J.C., Qureshi, A., Hamdan, S. et al. In vitro activity studies of hyperthermal near-infrared nanoGUMBOS in MDA-MB-231 breast cancer cells. Photochem Photobiol Sci 13, 1270–1280 (2014). https://doi.org/10.1039/c4pp00030g

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c4pp00030g

Search

Navigation