The Effect of Sulfated (1→3)-α-l-Fucan from the Brown Alga Saccharina cichorioides Miyabe on Resveratrol-Induced Apoptosis in Colon Carcinoma Cells
Open accessAbstract
Accumulating data clearly indicate that the induction of apoptosis by nontoxic natural compounds is a potent defense against the development and progression of many malignancies, including colon cancer. Resveratrol and the fucoidans have been shown to possess potent anti-tumor activity in vitro and in vivo. The aim of the present study was to examine whether the combination of a fucoidan from the brown alga Saccharina cichorioides Miyabe and resveratrol would be an effective preventive and/or therapeutic strategy against colon cancer. Based on NMR spectroscopy and MALDI-TOF analysis, the fucoidan isolated and purified from Saccharina cichorioides Miyabe was (1→3)-α-l-fucan with sulfate groups at C2 and C4 of the α-l-fucopyranose residues. The fucoidan enhanced the antiproliferative activity of resveratrol at nontoxic doses and facilitated resveratrol-induced apoptosis in the HCT 116 human colon cancer cell line. Apoptosis was realized by the activation of initiator caspase-9 and effector caspase-7 and -3, followed by the cleavage of PARP. Furthermore, significant inhibition of HCT 116 colony formation was associated with the sensitization of cells to resveratrol by the fucoidan. Taken together, these results demonstrate that the combination of the algal fucoidan with resveratrol may provide a potential therapy against human colon cancer.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Fucoidan from S. cichorioides enhanced antiproliferative activity of resveratrol at nontoxic doses and facilitated resveratrol-induced apoptosis in HCT116 cells.
“The fucoidan from S. cichorioides enhanced the antiproliferative activity of resveratrol at nontoxic doses and facilitated the resveratrol-induced apoptosis in the HCT116 cell line.”
From Anticancer and Cancer Preventive Properties of Marine Polysaccharides: Some Results and Prospects (2013) · cites this paper as [59]
Fucoidans may enhance the anticancer action of some low molecular weight compounds.
“Fucoidans may enhance the anticancer action of some low molecular weight compounds.”
From Anticancer and Cancer Preventive Properties of Marine Polysaccharides: Some Results and Prospects (2013) · cites this paper as [59]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Apoptosis: A Review of Programmed Cell Death
Elmore, S. (2007) · Toxicologic Pathology · doi:10.1080/01926230701320337 · Cited by 13,853 · see citing works
Jemal, A., Siegel, R. L., Ward, E., Hao, Y., Xu, J., Murray, T., & Thun, M. J. (2008) · CA A Cancer Journal for Clinicians · doi:10.3322/ca.2007.0010 · Cited by 10,184 · see citing works
Green, D. R., & Reed, J. C. (1998) · Science · doi:10.1126/science.281.5381.1309 · Cited by 8,998 · see citing works
Apoptosis in the Pathogenesis and Treatment of Disease
Thompson, C. B. (1995) · Science · doi:10.1126/science.7878464 · Cited by 6,524 · see citing works
A colorimetric method for the determination of sugars
DUBOIS, M., GILLES, K., HAMILTON, J. K., REBERS, P. A., & SMITH, F. (1951) · Nature · doi:10.1038/168167a0 · Cited by 2,504 · see citing works
Borst, O., Walker, B., Münzer, P., Russo, A., Schmid, E., Faggio, C., Bigalke, B., Laufer, S., Gawaz, M., & Lang, F. J. W. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350110 · Cited by 1,867 · see citing works
A note on the determination of the ester sulphate content of sulphated polysaccharides
Dodgson, K. S., & Price, R. (1962) · Biochemical Journal · doi:10.1042/bj0840106 · Cited by 1,645 · see citing works
Molecular mechanisms of resistance and toxicity associated with platinating agents
Rabik, C. A., & Dolan, M. E. (2006) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2006.09.006 · Cited by 1,566 · see citing works
Berridge, M. V., & Tan, A. S. (1993) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1993.1311 · Cited by 1,443 · see citing works
Role of resveratrol in prevention and therapy of cancer: preclinical and clinical studies.
Aggarwal, B. B., Bhardwaj, A., Aggarwal, R. S., Seeram, N. P., Shishodia, S., & Takada, Y. (2004) · PubMed · Cited by 1,383 · see citing works
Overview of cell death signaling pathways
Jin, Z., & El‐Deiry, W. S. (2005) · Cancer Biology & Therapy · doi:10.4161/cbt.4.2.1508 · Cited by 1,323 · see citing works
Chemical structures and bioactivities of sulfated polysaccharides from marine algae
Jiao, G., Yu, G., Zhang, J., & Ewart, H. S. (2011) · Marine Drugs · doi:10.3390/md9020196 · Cited by 1,054 · see citing works
Cumashi, A., Ushakova, N. A., Preobrazhenskaya, M. E., D'Incecco, A., Piccoli, A., Totani, L., Tinari, N., Morozevich, G. E., Berman, A. E., Bilan, M. I., et al. (2007) · Glycobiology · doi:10.1093/glycob/cwm014 · Cited by 1,026 · see citing works
Wijesekara, I., Pangestuti, R., & Kim, S.-K. (2011) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2010.10.062 · Cited by 992 · see citing works
Programmed cell death: alive and well in the new millennium
Kaufmann, S. H., & Hengartner, M. O. (2001) · Trends in Cell Biology · doi:10.1016/s0962-8924(01)02173-0 · Cited by 673 · see citing works
Clinical Pharmacology of Resveratrol and Its Metabolites in Colorectal Cancer Patients
Patel, K. R., Brown, V. A., Jones, D. J. L., Britton, R. G., Hemingway, D., Miller, A. S., West, K., Booth, T. D., Perloff, M., Crowell, J. A., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-10-2027 · Cited by 629 · see citing works
Synytsya, A., Kim, W.-J., Kim, S.-M., Pohl, R., Synytsya, A., Kvasnička, F., Čopíková, J., & Il Park, Y. (2010) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2010.01.052 · Cited by 461 · see citing works
Resveratrol suppresses cell transformation and induces apoptosis through a p53-dependent pathway
Huang, C. (1999) · Carcinogenesis · doi:10.1093/carcin/20.2.237 · Cited by 338 · see citing works
Assay of reducing sugars in the nanomole range with 2,2′-bicinchoninate
Waffenschmidt, S., & Jaenicke, L. (1987) · Analytical Biochemistry · doi:10.1016/0003-2697(87)90278-8 · Cited by 316 · see citing works
Aisa, Y., Miyakawa, Y., Nakazato, T., Shibata, H., Saito, K., Ikeda, Y., & Kizaki, M. (2005) · American Journal of Hematology · doi:10.1002/ajh.20182 · Cited by 307 · see citing works
Fucoidan present in brown algae induces apoptosis of human colon cancer cells
Kim, E. J., Park, S. Y., Lee, J.-Y., & Park, J. H. Y. (2010) · BMC Gastroenterology · doi:10.1186/1471-230x-10-96 · Cited by 275 · see citing works
Vishchuk, O. S., Ermakova, S. P., & Zvyagintseva, T. N. (2011) · Carbohydrate Research · doi:10.1016/j.carres.2011.09.034 · Cited by 267 · see citing works
Self-citationYang, C., Chung, D., Shin, I.-S., Lee, H., Kim, J., Lee, Y., & You, S. (2008) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2008.08.006 · Cited by 254 · see citing works
Ermakova, S., Sokolova, R., Kim, S.-M., Um, B.-H., Isakov, V., & Zvyagintseva, T. (2011) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-011-9178-2 · Cited by 229 · see citing works
Self-citationSynthesis and Biological Evaluation of Resveratrol and Analogues as Apoptosis-Inducing Agents
Roberti, M., Pizzirani, D., Simoni, D., Rondanin, R., Baruchello, R., Bonora, C., Buscemi, F., Grimaudo, S., & Tolomeo, M. (2003) · Journal of Medicinal Chemistry · doi:10.1021/jm030785u · Cited by 216 · see citing works
Colburn, N. H., Wendel, E. J., & Abruzzo, G. K. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.11.6912 · Cited by 185 · see citing works
Fucoidan Induces Apoptosis through Activation of Caspase-8 on Human Breast Cancer MCF-7 Cells
Yamasaki-Miyamoto, Y., Yamasaki, M., Tachibana, H., & Yamada, K. (2009) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf9010406 · Cited by 181 · see citing works
Zhang, Z., Teruya, K., Eto, H., & Shirahata, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027441 · Cited by 167 · see citing works
Mahyar-Roemer, M., Katsen, A. D., Mestres, P., & Roemer, K. (2001) · International Journal of Cancer · doi:10.1002/ijc.1516 · Cited by 162 · see citing works
Nishino, T., Nishioka, C., Ura, H., & Nagumo, T. (1994) · Carbohydrate Research · doi:10.1016/s0008-6215(00)90980-7 · Cited by 157 · see citing works
Resveratrol modulation of signal transduction in apoptosis and cell survival: A mini-review
Fulda, S., & Debatin, K. (2006) · Cancer Detection and Prevention · doi:10.1016/j.cdp.2006.03.007 · Cited by 157 · see citing works
Apoptosis inducing activity of fucoidan in HCT-15 colon carcinoma cells
Hyun, J.-H., Kim, S.-C., Kang, J.-I., Kim, M.-K., Boo, H.-J., Kwon, J.-M., Koh, Y.-S., Hyun, J.-W., Park, D.-B., Yoo, E.-S., et al. (2009) · Biological & Pharmaceutical Bulletin · doi:10.1248/bpb.32.1760 · Cited by 150 · see citing works
Ye, J., Li, Y., Teruya, K., Katakura, Y., Ichikawa, A., Eto, H., Hosoi, M., Hosoi, M., Nishimoto, S., & Shirahata, S. (2005) · Cytotechnology · doi:10.1007/s10616-005-3761-8 · Cited by 146 · see citing works
Haneji, K., Matsuda, T., Tomita, M., Kawakami, H., Ohshiro, K., Uchihara, J., Masuda, M., Takasu, N., Tanaka, Y., Ohta, T., et al. (2005) · Nutrition and Cancer · doi:10.1207/s15327914nc5202_9 · Cited by 132 · see citing works
Fucoidan from Undaria pinnatifida Induces Apoptosis in A549 Human Lung Carcinoma Cells
Boo, H., Hyun, J., Kim, S., Kang, J., Kim, M., Sun-Yeou, K., Cho, H., Yoo, E.-S., & Kang, H. (2011) · Phytotherapy Research · doi:10.1002/ptr.3489 · Cited by 115 · see citing works
Polysaccharide and lipid composition of the brown seaweed Laminaria gurjanovae
Шевченко, Н. М., Anastyuk, S. D., Ивановна, Г. Н., Dmitrenok, P. S., Isakov, V. V., & Николаевна, З. Т. (2007) · Russian Journal of Bioorganic Chemistry · doi:10.1134/s1068162007010116 · Cited by 97 · see citing works
Anastyuk, S. D., Шевченко, Н. М., Nazarenko, E. L., Imbs, T. I., Иванович, Г. В., Dmitrenok, P. S., & Николаевна, З. Т. (2010) · Carbohydrate Research · doi:10.1016/j.carres.2010.07.043 · Cited by 92 · see citing works
Adjuvant therapy of colon cancer
MACDONALD, J. (2001) · Seminars in Oncology · doi:10.1016/s0093-7754(01)90043-0 · Cited by 81 · see citing works
Minutolo, F., Sala, G., Bagnacani, A., et al. (2005) · Journal of Medicinal Chemistry · doi:10.1021/jm050528k · Cited by 79 · see citing works
Lee, N. Y., Ermakova, S. P., Zvyagintseva, T. N., Kang, K. W., Dong, Z., & Choi, H. S. (2008) · Food and Chemical Toxicology · doi:10.1016/j.fct.2008.01.025 · Cited by 75 · see citing works
Self-citationAdjuvant Therapy of Colon Cancer: Current Status and Future Directions
Chung, K. Y., & Saltz, L. B. (2007) · The Cancer Journal · doi:10.1097/ppo.0b013e318074d26e · Cited by 75 · see citing works
Fukahori, S., Yano, H., Akiba, J., Ogasawara, S., Momosaki, S., Sanada, S., Kuratomi, K., Ishizaki, Y., Moriya, F., Yagi, M., et al. (2008) · Molecular Medicine Reports · doi:10.3892/mmr.1.4.537 · Cited by 67 · see citing works
Imbs, T. I., Шевченко, Н. М., Суховерхов, С. В., Semenova, T. L., Skriptsova, A. V., & Николаевна, З. Т. (2009) · Chemistry of Natural Compounds · doi:10.1007/s10600-010-9507-7 · Cited by 62 · see citing works
She, Q., Ma, W., Wang, M., Kaji, A., Ho, C., & Dong, Z. (2003) · Oncogene · doi:10.1038/sj.onc.1206370 · Cited by 57 · see citing works
Rocha, H. A. O., Franco, C. R. C., Trindade, E. D. S., Veiga, S. S., Leite, E. L., Nader, H. B., & Dietrich, C. P. (2005) · Planta Medica · doi:10.1055/s-2005-871268 · Cited by 41 · see citing works
Philchenkov, A. A., Zavelevich, M. P., Imbs, T. I., Николаевна, З. Т., & Zaporozhets, T. S. (2007) · PubMed · Cited by 35 · see citing works
Matić, I. Z., Žižak, Ž. S., Simonović, M., et al. (2010) · Journal of Medicinal Food · doi:10.1089/jmf.2009.0193 · Cited by 22 · see citing works
Chemosensitization of solid tumor cells by alteration of their susceptibility to apoptosis.
Cree, I. A., Knight, L. A., Nicolantonio, F. D., Sharma, S., & Gulliford, T. (2002) · PubMed · Cited by 16 · see citing works
Chang, S., Huang, C.-T., & Huang, S.-M. (2010) · 中華民國大腸直腸外科醫學會雜誌 · doi:10.6312/scrstw.2010.21(3).09901 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Anticancer and Cancer Preventive Properties of Marine Polysaccharides: Some Results and Prospects
Fedorov, S., Ermakova, S., Zvyagintseva, T., & Stonik, V. (2013) · Marine Drugs · doi:10.3390/md11124876 · Cited by 189 · see citing works
Self-citationA Review on Fucoidan Structure, Extraction Techniques, and Its Role as an Immunomodulatory Agent
Jayawardena, T. U., Nagahawatta, D. P., Fernando, I. P. S., Kim, Y.-T., Kim, J.-S., Kim, W.-S., Lee, J. S., & Jeon, Y.-J. (2022) · Marine Drugs · doi:10.3390/md20120755 · Cited by 149 · see citing works
Usoltseva, R. V., Shevchenko, N. M., Malyarenko, O. S., Anastyuk, S. D., Kasprik, A. E., Zvyagintsev, N. V., & Ermakova, S. P. (2019) · Carbohydrate Polymers · doi:10.1016/j.carbpol.2019.05.079 · Cited by 73 · see citing works
Self-citation
- Authors
- Vishchuk, O., Ermakova, S., & Zvyagintseva, T.
- Affiliations
- Russian Academy of Sciences (RU)
- Laboratory of Enzyme Chemistry, G.B. Elyakov Pacific Institute of Bioorganic Chemistry, Far Eastern Branch, Russian Academy of Sciences, 159 100-Let Vladivostoku Ave., Vladivostok 690022, Russian Federation
- Corresponding author
- Vishchuk, Olesia
- ORCID
- Ermakova, Svetlana
- Venue
- Marine Drugs
- Publisher
- MDPI AG
- Published
- 2013-01-21
- Volume
- 11
- Issue
- 1
- Pages
- 194-212
- ISSN
- 1660-3397 (ISSN-L)
- PMC
- PMC3564167
- OpenAlex
- W2060899601
- Cited by
- 50
- References
- 50
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 5 · 2022: 5 · 2021: 1 · 2020: 4 · 2019: 3 · 2018: 6 · 2017: 2 · 2016: 7 · 2015: 5 · 2014: 2 · 2013: 3
- FWCI
- 8.64
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Marine Drugs (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Russian Foundation for Basic Research
- Russian Academy of Sciences
- Topics
- Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Seaweed-derived Bioactive Compounds
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Natural product bioactivities and synthesis
- Physical Sciences › Earth and Planetary Sciences › Oceanography › Marine and coastal plant biology
- Keywords
- brown algae, resveratrol, colon cancer, apoptosis, HCT116 cells, caspase activation, PARP cleavage, antiproliferative activity, combination therapy, marine polysaccharides
- MeSH terms
- Resveratrol, Phaeophyceae, Antineoplastic Agents, Carcinoma, Colonic Neoplasms, Humans, Magnetic Resonance Spectroscopy, Polysaccharides, Stilbenes, Sulfuric Acid Esters, Apoptosis, Caspases, HCT116 Cells, Cell Line, Tumor, Cell Proliferation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review