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      Engineering Multi-Walled Carbon Nanotube Therapeutic Bionanofluids to Selectively Target Papillary Thyroid Cancer Cells

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          Abstract

          Background

          The incidence of papillary thyroid carcinoma (PTC) has risen steadily over the past few decades as well as the recurrence rates. It has been proposed that targeted ablative physical therapy could be a therapeutic modality in thyroid cancer. Targeted bio-affinity functionalized multi-walled carbon nanotubes (BioNanofluid) act locally, to efficiently convert external light energy to heat thereby specifically killing cancer cells. This may represent a promising new cancer therapeutic modality, advancing beyond conventional laser ablation and other nanoparticle approaches.

          Methods

          Thyroid Stimulating Hormone Receptor (TSHR) was selected as a target for PTC cells, due to its wide expression. Either TSHR antibodies or Thyrogen or purified TSH (Thyrotropin) were chemically conjugated to our functionalized Bionanofluid. A diode laser system (532 nm) was used to illuminate a PTC cell line for set exposure times. Cell death was assessed using Trypan Blue staining.

          Results

          TSHR-targeted BioNanofluids were capable of selectively ablating BCPAP, a TSHR-positive PTC cell line, while not TSHR-null NSC-34 cells. We determined that a 2:1 BCPAP cell:α-TSHR-BioNanofluid conjugate ratio and a 30 second laser exposure killed approximately 60% of the BCPAP cells, while 65% and >70% of cells were ablated using Thyrotropin- and Thyrogen-BioNanofluid conjugates, respectively. Furthermore, minimal non-targeted killing was observed using selective controls.

          Conclusion

          A BioNanofluid platform offering a potential therapeutic path for papillary thyroid cancer has been investigated, with our in vitro results suggesting the development of a potent and rapid method of selective cancer cell killing. Therefore, BioNanofluid treatment emphasizes the need for new technology to treat patients with local recurrence and metastatic disease who are currently undergoing either re-operative neck explorations, repeated administration of radioactive iodine and as a last resort external beam radiation or chemotherapy, with fewer side effects and improved quality of life.

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          Most cited references 52

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          Selective laser photo-thermal therapy of epithelial carcinoma using anti-EGFR antibody conjugated gold nanoparticles.

          Efficient conversion of strongly absorbed light by plasmonic gold nanoparticles to heat energy and their easy bioconjugation suggest their use as selective photothermal agents in molecular cancer cell targeting. Two oral squamous carcinoma cell lines (HSC 313 and HOC 3 Clone 8) and one benign epithelial cell line (HaCaT) were incubated with anti-epithelial growth factor receptor (EGFR) antibody conjugated gold nanoparticles and then exposed to continuous visible argon ion laser at 514nm. It is found that the malignant cells require less than half the laser energy to be killed than the benign cells after incubation with anti-EGFR antibody conjugated Au nanoparticles. No photothermal destruction is observed for all types of cells in the absence of nanoparticles at four times energy required to kill the malignant cells with anti-EGFR/Au conjugates bonded. Au nanoparticles thus offer a novel class of selective photothermal agents using a CW laser at low powers. The potential of using this selective technique in molecularly targeted photothermal therapy in vivo is discussed.
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            Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction

            Biological systems are known to be highly transparent to 700-1100nm near-infrared (NIR) light. It is shown here that the strong optical absorbance of single-walled carbon nanotubes (SWNTs) in this special spectral window, an intrinsic property of SWNTs, can be utilized for optical stimulation of nanotubes inside living cells to afford multifunctional nanotube biological transporters. For oligonucleotides transported inside living cells by nanotubes, the oligos can translocate into cell nucleus upon endosomal rupture triggered by NIR laser pulses. Continuous NIR radiation can cause cell death due to excessive local heating of SWNT in vitro. Selective cancer cell destruction can be achieved via functionalization of SWNT with a folate moiety, selective internalization of SWNTs inside cells labeled with folate receptor tumor-markers and NIR triggered cell death, without harming receptor-free normal cells. Thus, the transporting capabilities of carbon nanotubes combined with suitable functionalization chemistry and their intrinsic optical properties can lead to new classes of novel nanomaterials for drug delivery and cancer therapy.
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              A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995 [see commetns].

              The National Cancer Data Base (NCDB) represents a national electronic registry system now capturing nearly 60% of incident cancers in the U. S. In combination with other Commission on Cancer programs, the NCDB offers a working example of voluntary, accurate, cost-effective "outcomes management" on a both a local and national scale. In addition, it is of particular value in capturing clinical information concerning rare cancers, such as those of the thyroid. For the accession years 1985-1995, NCDB captured demographic, patterns-of-care, stage, treatment, and outcome information for a convenience sample of 53,856 thyroid carcinoma cases (1% of total NCDB cases). This article focuses on overall 10-year relative survival and American Joint Committee on Cancer (AJCC) (3rd/4th edition) stage-stratified 5-year relative survival for each histologic type of thyroid carcinoma. Care patterns also are discussed. The 10-year overall relative survival rates for U. S. patients with papillary, follicular, Hürthle cell, medullary, and undifferentiated/anaplastic carcinoma was 93%, 85%, 76%, 75%, and 14%, respectively. For papillary and follicular neoplasms, current AJCC staging failed to discriminate between patients with Stage I and II disease at 5 years. Total thyroidectomy +/- lymph node sampling/dissection represented the dominant method of surgical treatment rendered to patients with papillary and follicular neoplasms. Approximately 38% of such patients receive adjuvant iodine-131 ablation/therapy. At 5 years, variation in surgical treatment (i.e., lobectomy vs. more extensive surgery) failed to translate into compelling differences in survival for any subgroup with papillary or follicular carcinoma, but longer follow-up is required to evaluate this. NCDB data appeared to validate the AMES prognostic system, as applied to papillary cases. Younger age appeared to influence prognosis favorably for all thyroid neoplasms, including medullary and undifferentiated/anaplastic carcinoma. NCDB data also revealed that unusual patients diagnosed with undifferentiated/anaplastic carcinoma before age of 45 years have better survival. The NCDB system permits analysis of care patterns and survival for large numbers of contemporaneous U. S. patients with relatively rare neoplasms, such as thyroid carcinoma. In this context, it represents an unsurpassed clinical tool for analyzing care, evaluating prognostic models, generating new hypotheses, and overcoming the volume-related drawbacks inherent in the study of such neoplasms. [See editorial on pages 2434-6, this issue.]
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 February 2016
                2016
                : 11
                : 2
                Affiliations
                [1 ]Lady Davis Institute for Medical Research-Jewish General Hospital, Montreal, QC, Canada
                [2 ]Department of Medicine, McGill University, Montreal, QC, Canada
                [3 ]Department of Surgery, McGill University, Montreal, QC, Canada
                [4 ]Division of Endocrinology, Jewish General Hospital, Montreal, QC, Canada
                Universidad de Castilla-La Mancha, SPAIN
                Author notes

                Competing Interests: The authors (I.D., P.J.R.R., M.P, E.J.M., and M.A.T.) would like to disclose to the editor and reviewers that they are also inventors on the following patent application: BIONANOFLUID FOR USE AS A CONTRAST, IMAGING, DISINFECTING AND/OR THERAPEUTIC AGENT—US Patent office PCT- CA2014/051094 on the work presented here and in other developments upon the therapeutic developments. This patent application does not conflict with the journal's open data policy regarding data present in this manuscript or the patent application. There are no further patents, products in development, or marketed products to declare. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

                Conceived and designed the experiments: ID PJRR MAT MP EJM. Performed the experiments: ID PJRR MP. Analyzed the data: ID PJRR MP EJM. Contributed reagents/materials/analysis tools: PJRR MP. Wrote the paper: ID PJRR MP EJM MAT.

                Article
                PONE-D-15-26724
                10.1371/journal.pone.0149723
                4762941
                26901566
                © 2016 Dotan et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 5, Tables: 0, Pages: 18
                Product
                Funding
                I.D. received salary support from the Israel Cancer Research Fund (ICRF).
                Categories
                Research Article
                Engineering and Technology
                Nanotechnology
                Carbon Nanotubes
                Engineering and Technology
                Equipment
                Optical Equipment
                Lasers
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Medicine and Health Sciences
                Oncology
                Cancers and Neoplasms
                Carcinomas
                Thyroid Carcinomas
                Medicine and Health Sciences
                Oncology
                Cancers and Neoplasms
                Endocrine Tumors
                Thyroid Carcinomas
                Medicine and Health Sciences
                Oncology
                Cancer Treatment
                Research and Analysis Methods
                Spectrum Analysis Techniques
                Ultraviolet-Visible Spectroscopy
                Engineering and Technology
                Nanotechnology
                Nanoparticles
                Biology and Life Sciences
                Biophysics
                Bionanotechnology
                Physical Sciences
                Physics
                Biophysics
                Bionanotechnology
                Biology and Life Sciences
                Biotechnology
                Bionanotechnology
                Engineering and Technology
                Nanotechnology
                Bionanotechnology
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                All relevant data are within the paper and its Supporting Information files.

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