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A Photoactive Magnetic Nanoparticle-Porphyrin Biomaterial Capable of Upregulation of Cancer PDT Having a Concomitant Immune Signature in Noncancerous Cells

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Abstract

While most metal-based nanomaterials lack regulatory approval for clinical applications in pharmacology, the FDA-approved Feraheme (ferumoxytol) has been among the few exceptions. Further, the approval of several iron nanoparticles (NPs) in nanotherapeutics has inspired the need to develop a new immunoprotective biomaterial (BM) involving superparamagnetic iron oxide NPs. This article emphasizes the impact of superparamagnetic NPs on porphyrins in the capacity of intensifying their biological activities under biocompatible conditions. To explore the cancer photodynamic therapy (PDT) and post-PDT anti-inflammatory and immunoprotective significance in developing BMs as anti-cancer drugs, the photobiological significance of a hydrophilic BM of superparamagnetic Fe3O4 NP functionalized with a tri-pyridyl porphyrin photosensitizer (PS) through a flexible 4-phenylaminoacetic acid linker is investigated. Fluorescence confocal microscopy with spectral imaging indicated high uptake of the BM Fe3O4 NP-porphyrin (C-NP) in the human gastric cancer (AGS) cell line. The potential of the synthesized BM to promote apoptosis through the upregulation of p21 expression and sub-G0-G1 phase arrest of the cell cycle has been reported. Under PDT conditions, higher apoptosis rates were obtained by C-NP than its free base precursor C. The Fe3O4 NPs have been found to influence the porphyrin PS by enhancing their anti-inflammatory properties apparently by reducing nitric oxide (under light irradiation and in the dark), myeloperoxidase, and superoxide production in murine macrophages.

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Acknowledgements

STIC-SAIF Kochi is acknowledged for the NMR; we thank Dr. Ramkrishna Laha, Postdoctoral Associate, Ernest Mario School of Pharmacy, Rutgers University, New Brunswick, for helping us with the mass spectra. The authors further acknowledge the help and guidance received from Prof. Subrata Banerjee, Ex-professor and Head, Biophysics & Structural Genomics Division, Saha Institute of Nuclear Physics (SINP), Kolkata; Dr. Yashmin Choudhury, Department of Biotechnology, Assam University, Silchar, India; and Dr. Aviva Levina, School of Chemistry, The University of Sydney, Australia.

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Author notes

  1. Debdulal Sharma, Subhojit Das, and Zeaul Hoque Mazumdar have contributed equally to the paper.

Authors and Affiliations

  1. Department of Chemistry, Assam University, Silchar, Assam, 788 011, India

    Debdulal Sharma, Zeaul Hoque Mazumdar & Devashish Sengupta

  2. Department of Chemistry, National Institute of Technology, Agartala, Tripura, 799 046, India

    Subhojit Das

  3. Department of Zoology, Charuchandra College, Kolkata, West Bengal, 700 029, India

    Avinaba Mukherjee

  4. Biomolecular Engineering, Institute for Biology of the Stem Cells, UCSC, Santa Cruz, CA, USA

    Saran Chattopadhyaya

  5. Department of Biotechnology, Assam University, Silchar, Assam, 788 011, India

    Biswajit Das & Mahuya Sengupta

  6. Chemical Sciences Division, Saha Institute of Nuclear Physics, Kolkata, West Bengal, 700 064, India

    Samita Basu

  7. Department of Pharmaceutical Science, Assam University, Silchar, Assam, 788 011, India

    Partha Palit

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Contributions

The manuscript was written through the contributions of all authors. All authors have approved the final version of the manuscript. DS conceived, designed, and standardized the experiments by initially synthesizing the precursor porphyrins. DS synthesized the nanoparticles and functionalized them along with SD and ZHM. The biological studies were carried out by AM and SC at the Department of Zoology, Charuchandra College, Kolkata 700 029, India, and the School of Biological Sciences, Ramkrishna Mission Vivekananda Educational & Research Institute (RKMVERI), Narendrapur, Kolkata 700 103, India. MS and BD performed the immunomodulatory experiments on macrophage cell line at the Department of Biotechnology, Assam University, Silchar 788 011, India. AM conducted the photobiological assays related to ROS and GSH in AGS cell line. PP helped with the interpretation of the results of the photobiological assays along with DS and AM. DS performed the Alder’s synthesis under various conditions, performed different methods of isolation and characterization of the various porphyrin derivatives at Assam University, Silchar (AUS), and performed lifetime emission experiments along with SB at Saha Institute of Nuclear Physics, Kolkata 700 064, India.

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Correspondence to Devashish Sengupta.

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The authors declare no competing interests.

Research Involving Humans and Animals Statement

As investigators, we conducted animal research ethically and humanely by using the minimum number of animals needed for scientifically valid results and ensuring appropriate housing, feeding, and sanitation. We administered appropriate anesthetics, analgesics, or tranquilizers to minimize any pain and discomfort, and obtained approval and oversight from an institutional animal experiment committee.

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All the authors have reviewedand registered their consent to the final version of the manuscript.

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Our work did not involve any experiments on human subjects, as such, informed consent is not applicable to the current research work.

Funding Statement

This work was supported by the DBT project (Reg. No. BT/PR25024/NER/95/961/2017) granted to Devashish Sengupta by the Department of Biotechnology, Ministry of Science and Technology, Government of India.

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Sharma, D., Das, S., Mazumdar, Z.H. et al. A Photoactive Magnetic Nanoparticle-Porphyrin Biomaterial Capable of Upregulation of Cancer PDT Having a Concomitant Immune Signature in Noncancerous Cells. BioNanoSci. 13, 625–637 (2023). https://doi.org/10.1007/s12668-023-01104-2

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  • DOI: https://doi.org/10.1007/s12668-023-01104-2

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