The Effects of Fucoidan Derived from Sargassum filipendula and Fucus vesiculosus on the Survival and Mineralisation of Osteogenic Progenitors

Dhanak Gupta; Diana C. Martinez; Miguel Angel Puertas-Mejía; Vanessa L. Hearnden; Gwendolen C. Reilly; Giacomina Brunetti

doi:10.3390/ijms25042085

The Effects of Fucoidan Derived from Sargassum filipendula and Fucus vesiculosus on the Survival and Mineralisation of Osteogenic Progenitors

Dhanak Gupta^*, Diana C. Martinez, Miguel Angel Puertas-Mejía, Vanessa L. Hearnden, Gwendolen C. Reilly, Giacomina Brunetti (Editor)

^*Corresponding author for this work

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Abstract

Osteosarcoma is a bone cancer primarily affecting teenagers. It has a poor prognosis and diminished quality of life after treatment due to chemotherapy side effects, surgical complications and post-surgical osteoporosis risks. The sulphated polysaccharide fucoidan, derived from brown algae, has been a subject of interest for its potential anti-cancer properties and its impact on bone regeneration. This study explores the influence of crude, low-molecular-weight (LMW, 10–50 kDa), medium-molecular-weight (MMW, 50–100 kDa) and high-molecular-weight (HMW, >100 kDa) fractions from Sargassum filipendula, harvested from the Colombian sea coast, as well as crude fucoidan from Fucus vesiculosus, on a specific human osteoprogenitor cell type, human embryonic-derived mesenchymal stem cells. Fourier transform infrared spectroscopy coupled with attenuated total reflection (FTIR-ATR) results showed the highest sulphation levels and lowest uronic acid content in crude extract from F. vesiculosus. There was a dose-dependent drop in focal adhesion formation, proliferation and osteogenic differentiation of cells for all fucoidan types, but the least toxicity was observed for LMW and MMW. Transmission electron microscopy (TEM), JC-1 (5,50,6,60-tetrachloro-1,10,3,30-tetraethylbenzimi-dazolylcarbocyanine iodide) staining and cytochrome c analyses confirmed mitochondrial damage, swollen ER and upregulated autophagy due to fucoidans, with the highest severity in the case of F. vesiculosus fucoidan. Stress-induced apoptosis-like cell death by F. vesiculosus fucoidan and stress-induced necrosis-like cell death by S. filipendula fucoidans were also confirmed. LMW and MMW doses of

Original language	English
Article number	2085
Number of pages	23
Journal	International Journal of Molecular Sciences
Volume	25
Issue number	4
DOIs	https://doi.org/10.3390/ijms25042085
Publication status	Published - 8 Feb 2024

Bibliographical note

Acknowledgments
Dhanak Gupta was funded by the Newton Fund. Hybridoma extracts for fucoidan Ab staining were kindly provided by Paul Knox, Centre for Plant Sciences, University of Leeds, UK. Flow cytometry was performed with technical support from the Flow Group at the Medical School, the University of Sheffield. Confocal imaging work was performed at the Wolfson Light Microscopy Facility, the University of Sheffield. We thank Christopher J. Hill for his support with TEM based at Department of Molecular Biology and Biotechnology (MBB), University of Sheffield.

Keywords

apoptosis
mitochondria
fucoidan
brown algae
bone healing
necrosis
osteosarcoma
human embryonic-derived mesenchymal progenitor cells

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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title = "The Effects of Fucoidan Derived from Sargassum filipendula and Fucus vesiculosus on the Survival and Mineralisation of Osteogenic Progenitors",

abstract = "Osteosarcoma is a bone cancer primarily affecting teenagers. It has a poor prognosis and diminished quality of life after treatment due to chemotherapy side effects, surgical complications and post-surgical osteoporosis risks. The sulphated polysaccharide fucoidan, derived from brown algae, has been a subject of interest for its potential anti-cancer properties and its impact on bone regeneration. This study explores the influence of crude, low-molecular-weight (LMW, 10–50 kDa), medium-molecular-weight (MMW, 50–100 kDa) and high-molecular-weight (HMW, >100 kDa) fractions from Sargassum filipendula, harvested from the Colombian sea coast, as well as crude fucoidan from Fucus vesiculosus, on a specific human osteoprogenitor cell type, human embryonic-derived mesenchymal stem cells. Fourier transform infrared spectroscopy coupled with attenuated total reflection (FTIR-ATR) results showed the highest sulphation levels and lowest uronic acid content in crude extract from F. vesiculosus. There was a dose-dependent drop in focal adhesion formation, proliferation and osteogenic differentiation of cells for all fucoidan types, but the least toxicity was observed for LMW and MMW. Transmission electron microscopy (TEM), JC-1 (5,50,6,60-tetrachloro-1,10,3,30-tetraethylbenzimi-dazolylcarbocyanine iodide) staining and cytochrome c analyses confirmed mitochondrial damage, swollen ER and upregulated autophagy due to fucoidans, with the highest severity in the case of F. vesiculosus fucoidan. Stress-induced apoptosis-like cell death by F. vesiculosus fucoidan and stress-induced necrosis-like cell death by S. filipendula fucoidans were also confirmed. LMW and MMW doses of",

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note = "Acknowledgments Dhanak Gupta was funded by the Newton Fund. Hybridoma extracts for fucoidan Ab staining were kindly provided by Paul Knox, Centre for Plant Sciences, University of Leeds, UK. Flow cytometry was performed with technical support from the Flow Group at the Medical School, the University of Sheffield. Confocal imaging work was performed at the Wolfson Light Microscopy Facility, the University of Sheffield. We thank Christopher J. Hill for his support with TEM based at Department of Molecular Biology and Biotechnology (MBB), University of Sheffield.",

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AU - Hearnden, Vanessa L.

AU - Reilly, Gwendolen C.

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N1 - Acknowledgments Dhanak Gupta was funded by the Newton Fund. Hybridoma extracts for fucoidan Ab staining were kindly provided by Paul Knox, Centre for Plant Sciences, University of Leeds, UK. Flow cytometry was performed with technical support from the Flow Group at the Medical School, the University of Sheffield. Confocal imaging work was performed at the Wolfson Light Microscopy Facility, the University of Sheffield. We thank Christopher J. Hill for his support with TEM based at Department of Molecular Biology and Biotechnology (MBB), University of Sheffield.

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N2 - Osteosarcoma is a bone cancer primarily affecting teenagers. It has a poor prognosis and diminished quality of life after treatment due to chemotherapy side effects, surgical complications and post-surgical osteoporosis risks. The sulphated polysaccharide fucoidan, derived from brown algae, has been a subject of interest for its potential anti-cancer properties and its impact on bone regeneration. This study explores the influence of crude, low-molecular-weight (LMW, 10–50 kDa), medium-molecular-weight (MMW, 50–100 kDa) and high-molecular-weight (HMW, >100 kDa) fractions from Sargassum filipendula, harvested from the Colombian sea coast, as well as crude fucoidan from Fucus vesiculosus, on a specific human osteoprogenitor cell type, human embryonic-derived mesenchymal stem cells. Fourier transform infrared spectroscopy coupled with attenuated total reflection (FTIR-ATR) results showed the highest sulphation levels and lowest uronic acid content in crude extract from F. vesiculosus. There was a dose-dependent drop in focal adhesion formation, proliferation and osteogenic differentiation of cells for all fucoidan types, but the least toxicity was observed for LMW and MMW. Transmission electron microscopy (TEM), JC-1 (5,50,6,60-tetrachloro-1,10,3,30-tetraethylbenzimi-dazolylcarbocyanine iodide) staining and cytochrome c analyses confirmed mitochondrial damage, swollen ER and upregulated autophagy due to fucoidans, with the highest severity in the case of F. vesiculosus fucoidan. Stress-induced apoptosis-like cell death by F. vesiculosus fucoidan and stress-induced necrosis-like cell death by S. filipendula fucoidans were also confirmed. LMW and MMW doses of

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KW - bone healing

KW - necrosis

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The Effects of Fucoidan Derived from Sargassum filipendula and Fucus vesiculosus on the Survival and Mineralisation of Osteogenic Progenitors

Abstract

Bibliographical note

Keywords

UN SDGs

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