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Published in: Cancer Cell International 1/2022

Open Access 01-12-2022 | Research

Antitumor immunity and therapeutic properties of marine seaweeds-derived extracts in the treatment of cancer

Authors: Mostafa M. El-Sheekh, Mohamed Nassef, Eman Bases, Shimaa El Shafay, Rania El-shenody

Published in: Cancer Cell International | Issue 1/2022

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Abstract

Marine seaweeds are important sources of drugs with several pharmacological characteristics. The present study aims to evaluate the antitumor and antitumor immunological potentials of the extracts from the brown alga Padina pavonica and the red alga Jania rubens, inhibiting the Egyptian marine coasts. Hep-G2 cell lines were used for assessment of the antitumor efficacy of Padina pavonica and Jania rubens extracts in vitro, while Ehrlich ascites carcinoma (EAC) cells were applied to gain more antitumor immunity and antitumor insights of P. pavonica and J. rubens extracts in vivo. In vitro antitumor potentials of P. pavonica and J. rubens extracts were analyzed against human liver cancer Hep-G2 cells by MTT and trypan blue exclusion assays. In vivo antitumor immunological potentials of P. pavonica and J. rubens extracts at low, high, and prophylactic doses were analyzed by blood counting and flow cytometry in mice challenged with Ehrlich ascites carcinoma (EAC) cells. In vitro results revealed that P. pavonica and J. rubens extracts caused significant decreases in the number and viability of Hep-G2 cells in a dose-dependent manner as compared to untreated Hep-G2 cells or Cisplatin®-treated Hep-G2 cells. In vivo findings showed that P. pavonica and J. rubens extracts at low, high, and prophylactic doses significantly reduced the number and viability of EAC tumor cells accompanied by increases in EAC apoptosis compared to naïve EAC mouse. Additionally, P. pavonica and J. rubens extracts at low and prophylactic doses remarkably increased both the total WBC count and the relative numbers of lymphocytes and decreased the relative numbers of neutrophils and monocytes. Flow cytometric analysis showed that P. pavonica and J. rubens extracts at the treatment and the prophylactic doses resulted in a significant increase in the phenotypic expressions of CD4+ T, CD8+ T, and CD335 cells compared to naïve EAC mouse. Overall, both extracts P. pavonica and J. rubens possess potential antitumor and antitumor immunological effects with less toxicity, opening new approaches for further studies of the chemical and biological mechanisms behind these effects.
Literature
2.
go back to reference Baskar R, Lee KA, Yeo R, Yeoh KW. Cancer and radiation therapy: current advances and future directions. Int J Medical Sci. 2012;9(3):193–9.CrossRef Baskar R, Lee KA, Yeo R, Yeoh KW. Cancer and radiation therapy: current advances and future directions. Int J Medical Sci. 2012;9(3):193–9.CrossRef
3.
go back to reference Weinberg R. The biology of cancer. In: Garland science. W.W. Norton & Company: USA; 2013. Weinberg R. The biology of cancer. In: Garland science. W.W. Norton & Company: USA; 2013.
4.
go back to reference Brabec V, Kasparkova J. Modifications of DNA by platinum complexes. Relation to resistance of tumors to platinum antitumor drugs. Drug Resist Updates. 2005;8(3):131–46.CrossRef Brabec V, Kasparkova J. Modifications of DNA by platinum complexes. Relation to resistance of tumors to platinum antitumor drugs. Drug Resist Updates. 2005;8(3):131–46.CrossRef
5.
go back to reference Torigoe T, Izumi H, Ishiguchi H, Yoshida Y, Tanabe M, Yoshida T, Igarashi T, Niina I, Wakasugi T, Imaizumi T, Momii Y, Kuwano M, Kohno K. Cisplatin resistance and transcription factors. Curr Med Chem Anti-Cancer Agents. 2005;5(1):15–27.PubMedCrossRef Torigoe T, Izumi H, Ishiguchi H, Yoshida Y, Tanabe M, Yoshida T, Igarashi T, Niina I, Wakasugi T, Imaizumi T, Momii Y, Kuwano M, Kohno K. Cisplatin resistance and transcription factors. Curr Med Chem Anti-Cancer Agents. 2005;5(1):15–27.PubMedCrossRef
6.
go back to reference Odeh F, Ismail SI, Abu-Dahab R, Mahmoud IS, Al Bawab A. Thymoquinone in liposomes: a study of loading efficiency and biological activity towards breast cancer. Drug Deliv. 2012;19(8):371–7.PubMedCrossRef Odeh F, Ismail SI, Abu-Dahab R, Mahmoud IS, Al Bawab A. Thymoquinone in liposomes: a study of loading efficiency and biological activity towards breast cancer. Drug Deliv. 2012;19(8):371–7.PubMedCrossRef
7.
go back to reference Badary OA, Abdel-Naim AB, Abdel-Wahab MH, Hamada FM. The influence of thymoquinone on doxorubicin-induced hyperlipidemic nephropathy in rats. Toxicology. 2000;143(3):219–26.PubMedCrossRef Badary OA, Abdel-Naim AB, Abdel-Wahab MH, Hamada FM. The influence of thymoquinone on doxorubicin-induced hyperlipidemic nephropathy in rats. Toxicology. 2000;143(3):219–26.PubMedCrossRef
8.
go back to reference Sun LR, Zhou W, Zhang HM, Guo QS, Yang W, Li BJ, Sun ZH, Shuo-hui Gao SH, Cui RJ. Modulation of multiple signaling pathways of the plant-derived natural products in cancer. Front Oncol. 2019;9:1153.PubMedPubMedCentralCrossRef Sun LR, Zhou W, Zhang HM, Guo QS, Yang W, Li BJ, Sun ZH, Shuo-hui Gao SH, Cui RJ. Modulation of multiple signaling pathways of the plant-derived natural products in cancer. Front Oncol. 2019;9:1153.PubMedPubMedCentralCrossRef
9.
go back to reference Patel SM, Nagulapalli Venkata KCN, Bhattacharyya P, Sethi G, Bishayee A. Potential of neem (Azadirachta indica L.) for prevention and treatment of oncologic diseases. Semin Cancer Biol. 2016;40(41):100–15.PubMedCrossRef Patel SM, Nagulapalli Venkata KCN, Bhattacharyya P, Sethi G, Bishayee A. Potential of neem (Azadirachta indica L.) for prevention and treatment of oncologic diseases. Semin Cancer Biol. 2016;40(41):100–15.PubMedCrossRef
10.
go back to reference Ashrafizadeh M, Zarrabi A, Hashemipour M, Vosough M, Najafi M, Shahinozzaman M, Hushmandi K, Haroon Khan H, Mirzaei H. Sensing the scent of death: modulation of microRNAs by curcumin in gastrointestinal cancers. Pharmacol res. 2020;160: 105199.PubMedCrossRef Ashrafizadeh M, Zarrabi A, Hashemipour M, Vosough M, Najafi M, Shahinozzaman M, Hushmandi K, Haroon Khan H, Mirzaei H. Sensing the scent of death: modulation of microRNAs by curcumin in gastrointestinal cancers. Pharmacol res. 2020;160: 105199.PubMedCrossRef
11.
go back to reference Mirzaei S, Gholami MH, Zabolian A, Saleki H, Farahani MV, Hamzehlou S, Far FB, Sharifzadeh SO, Samarghandian S, Khan H, Aref AR, Ashrafizadeh M, Zarrabi A, Sethi G. Caffeic acid and its derivatives as potential modulators of oncogenic molecular pathways: new hope in the fight against cancer. Pharmacol Res. 2021;171: 105759.PubMedCrossRef Mirzaei S, Gholami MH, Zabolian A, Saleki H, Farahani MV, Hamzehlou S, Far FB, Sharifzadeh SO, Samarghandian S, Khan H, Aref AR, Ashrafizadeh M, Zarrabi A, Sethi G. Caffeic acid and its derivatives as potential modulators of oncogenic molecular pathways: new hope in the fight against cancer. Pharmacol Res. 2021;171: 105759.PubMedCrossRef
12.
go back to reference Abadi AJ, Mirzaei S, Mahabady MK, Hashemi F, Zabolian A, Hashemi F, Zabolian A, Hashemi F, Raee P, Aghamiri S, Ashrafizadeh M, Aref AR, Hamblin MR, Hushmandi K, Zarrabi A, Sethi G. Curcumin and its derivatives in cancer therapy: potentiating antitumor activity of cisplatin and reducing side effects. Phytother Res. 2022;36(1):189–213.PubMedCrossRef Abadi AJ, Mirzaei S, Mahabady MK, Hashemi F, Zabolian A, Hashemi F, Zabolian A, Hashemi F, Raee P, Aghamiri S, Ashrafizadeh M, Aref AR, Hamblin MR, Hushmandi K, Zarrabi A, Sethi G. Curcumin and its derivatives in cancer therapy: potentiating antitumor activity of cisplatin and reducing side effects. Phytother Res. 2022;36(1):189–213.PubMedCrossRef
13.
go back to reference Wamtinga RS, Rainatou B, Claudia C, Marie HT, Mario D, Marc D. A survey of marine natural compounds and their derivatives with anti-cancer activity reported in 2012. Molecules. 2015;20:7097–142.CrossRef Wamtinga RS, Rainatou B, Claudia C, Marie HT, Mario D, Marc D. A survey of marine natural compounds and their derivatives with anti-cancer activity reported in 2012. Molecules. 2015;20:7097–142.CrossRef
14.
go back to reference Khalid S, Abbas M, Saeed F, Bader-Ul-Ain H, Suleria HAR. Therapeutic potential of seaweed bioactive compounds. Seaweed Biomater. 2018;1:7–26. Khalid S, Abbas M, Saeed F, Bader-Ul-Ain H, Suleria HAR. Therapeutic potential of seaweed bioactive compounds. Seaweed Biomater. 2018;1:7–26.
15.
go back to reference Rai SK, Smriti B, Gunaseelan S, Ashokkumar B, Varalakshmi P. Polyphenolic compound from Brown Macroalga Padina tetrastromatica imparts oxidative stress tolerance in SH-SY5Y, RAW 264.7, HeLa Cell Lines and in Caenorhabditis elegans. Chem Select. 2019;4(20):6342–7. Rai SK, Smriti B, Gunaseelan S, Ashokkumar B, Varalakshmi P. Polyphenolic compound from Brown Macroalga Padina tetrastromatica imparts oxidative stress tolerance in SH-SY5Y, RAW 264.7, HeLa Cell Lines and in Caenorhabditis elegans. Chem Select. 2019;4(20):6342–7.
16.
go back to reference Arivarasu L, Perumal S. Anticancer activity of Sargassum Sp. seaweed crude extracts against the breast cancer cell line. Oncol Res Treat. 2021;6:S6. Arivarasu L, Perumal S. Anticancer activity of Sargassum Sp. seaweed crude extracts against the breast cancer cell line. Oncol Res Treat. 2021;6:S6.
17.
go back to reference Ibrahim MY, Hashim NM, Mohan S, Abdulla MA, Abdelwahab SI, Arbab IA, Ishag OE. α-Mangostin from Cratoxylum arborescens: an in vitro and in vivo toxicological evaluation. Arab J Chem. 2015;8(1):129–37.CrossRef Ibrahim MY, Hashim NM, Mohan S, Abdulla MA, Abdelwahab SI, Arbab IA, Ishag OE. α-Mangostin from Cratoxylum arborescens: an in vitro and in vivo toxicological evaluation. Arab J Chem. 2015;8(1):129–37.CrossRef
18.
go back to reference Unissa R, Cheruvu SS, Tejaswi M, Raghavi M, Bindu NH, Nishita T, Bhavana P. Evaluation of the in vitro cytotoxic activity of Jania rubens against Jurkat and molt-4 human cancer cell lines. Trop J Na Prod Res. 2017;1(5):199–202.CrossRef Unissa R, Cheruvu SS, Tejaswi M, Raghavi M, Bindu NH, Nishita T, Bhavana P. Evaluation of the in vitro cytotoxic activity of Jania rubens against Jurkat and molt-4 human cancer cell lines. Trop J Na Prod Res. 2017;1(5):199–202.CrossRef
19.
go back to reference Moussavou G, Kwak DH, Obiang-Obonou BW, Maranguy CAO, Dinzouna-Boutamba S-D, Lee DH, Pissibanganga OGM, Ko K, Seo JI, Choo YK. Anticancer effects of different seaweeds on human colon and breast cancers. Mar Drugs. 2014;12:4898–911.PubMedPubMedCentralCrossRef Moussavou G, Kwak DH, Obiang-Obonou BW, Maranguy CAO, Dinzouna-Boutamba S-D, Lee DH, Pissibanganga OGM, Ko K, Seo JI, Choo YK. Anticancer effects of different seaweeds on human colon and breast cancers. Mar Drugs. 2014;12:4898–911.PubMedPubMedCentralCrossRef
20.
go back to reference Ganesan AR, Tiwari U, Rajauria G. Seaweed nutraceuticals and their therapeutic role in disease prevention. Food Sci Human Wellness. 2019;8(3):252–63.CrossRef Ganesan AR, Tiwari U, Rajauria G. Seaweed nutraceuticals and their therapeutic role in disease prevention. Food Sci Human Wellness. 2019;8(3):252–63.CrossRef
21.
go back to reference Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DDA, Câmara RBG, Rocha HAO. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother. 2010;64(1):21–8.PubMedCrossRef Costa LS, Fidelis GP, Cordeiro SL, Oliveira RM, Sabry DDA, Câmara RBG, Rocha HAO. Biological activities of sulfated polysaccharides from tropical seaweeds. Biomed Pharmacother. 2010;64(1):21–8.PubMedCrossRef
22.
go back to reference Yende SR, Harle UN, Chaugule BB. Therapeutic potential and health benefits of Sargassum species. Pharmacog Rev. 2014;8(15):1.CrossRef Yende SR, Harle UN, Chaugule BB. Therapeutic potential and health benefits of Sargassum species. Pharmacog Rev. 2014;8(15):1.CrossRef
23.
go back to reference Liang W, Mao X, Peng X, Tang S. Effects of sulfate group in red seaweed polysaccharides on anticoagulant activity and cytotoxicity. Carbohyd Polym. 2014;101:776–85.CrossRef Liang W, Mao X, Peng X, Tang S. Effects of sulfate group in red seaweed polysaccharides on anticoagulant activity and cytotoxicity. Carbohyd Polym. 2014;101:776–85.CrossRef
24.
go back to reference Xue M, Ge Y, Zhang J, Wang Q, Hou L, Liu Y, Li Q. Anticancer properties and mechanisms of fucoidan on mouse breast cancer in vitro and in vivo. PLoS ONE. 2012;7(8): e43483.PubMedPubMedCentralCrossRef Xue M, Ge Y, Zhang J, Wang Q, Hou L, Liu Y, Li Q. Anticancer properties and mechanisms of fucoidan on mouse breast cancer in vitro and in vivo. PLoS ONE. 2012;7(8): e43483.PubMedPubMedCentralCrossRef
25.
go back to reference Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’incecco A, Piccoli A, Totani L, Tinari N, Morozevich GE, Berman AE, Bilan MI. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology. 2007;17:541–52.PubMedCrossRef Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’incecco A, Piccoli A, Totani L, Tinari N, Morozevich GE, Berman AE, Bilan MI. A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology. 2007;17:541–52.PubMedCrossRef
27.
go back to reference Lee JB, Hayashi K, Hashimoto M, Nakano T, Hayashi T. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharmaceut Bull. 2004;52(9):1091–4.CrossRef Lee JB, Hayashi K, Hashimoto M, Nakano T, Hayashi T. Novel antiviral fucoidan from sporophyll of Undaria pinnatifida (Mekabu). Chem Pharmaceut Bull. 2004;52(9):1091–4.CrossRef
28.
go back to reference Mak W, Hamid N, Liu T, Lu J, White W. Fucoidan from New Zealand Undaria pinnatifida: monthly variations and determination of antioxidant activities. Carbohyd Polym. 2004;95:606–14.CrossRef Mak W, Hamid N, Liu T, Lu J, White W. Fucoidan from New Zealand Undaria pinnatifida: monthly variations and determination of antioxidant activities. Carbohyd Polym. 2004;95:606–14.CrossRef
29.
go back to reference Maruyama H, Tamauchi H, Hashimoto M, Nakano T. Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida. In Vivo (Athens, Greece). 2003;17(3):245. Maruyama H, Tamauchi H, Hashimoto M, Nakano T. Antitumor activity and immune response of Mekabu fucoidan extracted from Sporophyll of Undaria pinnatifida. In Vivo (Athens, Greece). 2003;17(3):245.
30.
go back to reference Jha B, Reddy CRK, Thakur MC, Rao MU. Seaweeds of India: The diversity and distribution of seaweeds of gujarat coast. Springer Science & Business Media. vol. 3. 2009. Jha B, Reddy CRK, Thakur MC, Rao MU. Seaweeds of India: The diversity and distribution of seaweeds of gujarat coast. Springer Science & Business Media. vol. 3. 2009.
31.
go back to reference Kanaan H, Belous O. Marine algae of the Lebanese coast. New York: Nova Science Publisher, Inc.; 2016. Kanaan H, Belous O. Marine algae of the Lebanese coast. New York: Nova Science Publisher, Inc.; 2016.
32.
go back to reference Guiry MD, Guiry GM. AlgaeBase. Worldwide electronic publication, National University of Ireland, Galway. 2019. Available Online: http://www.Algaebase.Org. Accessed on 9 Jun 2019. 2019 Guiry MD, Guiry GM. AlgaeBase. Worldwide electronic publication, National University of Ireland, Galway. 2019. Available Online: http://​www.​Algaebase.​Org. Accessed on 9 Jun 2019. 2019
33.
go back to reference El-Sheekh MM, El-Shenody RAEK, Bases EA, El Shafay SM. Comparative assessment of antioxidant activity and biochemical composition of four seaweeds, Rocky Bay of Abu Qir in Alexandria, Egypt. Food Sci Technol. 2020;41:29–40.CrossRef El-Sheekh MM, El-Shenody RAEK, Bases EA, El Shafay SM. Comparative assessment of antioxidant activity and biochemical composition of four seaweeds, Rocky Bay of Abu Qir in Alexandria, Egypt. Food Sci Technol. 2020;41:29–40.CrossRef
34.
go back to reference Maisuthisakul P, Pongsawatmanit R. Effect of sample preparation methods and extraction time on yield and antioxidant activity from kradonbok (Careya sphaerica Roxb.) leaves. Kasetsart J (Nat Sci). 2004;38(5):8–14. Maisuthisakul P, Pongsawatmanit R. Effect of sample preparation methods and extraction time on yield and antioxidant activity from kradonbok (Careya sphaerica Roxb.) leaves. Kasetsart J (Nat Sci). 2004;38(5):8–14.
35.
go back to reference Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63.PubMedCrossRef Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983;65(1–2):55–63.PubMedCrossRef
36.
go back to reference Halle W, Halder M, Worth A, Genschow E. The registry of cytotoxicity: toxicity testing in cell cultures to predict acute toxicity (LD50) and to reduce testing in animals. Altern Lab Anim. 2003;31(2):89.PubMedCrossRef Halle W, Halder M, Worth A, Genschow E. The registry of cytotoxicity: toxicity testing in cell cultures to predict acute toxicity (LD50) and to reduce testing in animals. Altern Lab Anim. 2003;31(2):89.PubMedCrossRef
37.
go back to reference Gothoskar SV, Ranadive KJ. Anticancer screening of SAN-AB: an extract of marking nut, Semecarpus anacardium. Ind J Experim Biol. 1971;9(3):372. Gothoskar SV, Ranadive KJ. Anticancer screening of SAN-AB: an extract of marking nut, Semecarpus anacardium. Ind J Experim Biol. 1971;9(3):372.
38.
go back to reference Alves C, Silva J, Pinteus S, Gaspar H, Alpoim MC, Botana LM, Pedrosa R. From marine origin to therapeutics: the antitumor potential of marine algae-derived compounds. Front Pharmacol. 2018;9:777.PubMedPubMedCentralCrossRef Alves C, Silva J, Pinteus S, Gaspar H, Alpoim MC, Botana LM, Pedrosa R. From marine origin to therapeutics: the antitumor potential of marine algae-derived compounds. Front Pharmacol. 2018;9:777.PubMedPubMedCentralCrossRef
39.
go back to reference Okolie CL, Mason B, Critchley AT. Seaweeds as a source of proteins for use in pharmaceuticals and high‐value applications. In: Novel proteins for food, pharmaceuticals and agriculture: sources, applications and advances. Wiley. Chapter: 11 (Edition: 1) 2018. Okolie CL, Mason B, Critchley AT. Seaweeds as a source of proteins for use in pharmaceuticals and high‐value applications. In: Novel proteins for food, pharmaceuticals and agriculture: sources, applications and advances. Wiley. Chapter: 11 (Edition: 1) 2018.
40.
go back to reference Zandi K, Tajbakhsh S, Nabipour I, Rastian Z, Yousefi F, Sharafian S, Sartavi K. In vitro antitumor activity of Gracilaria corticata (a red alga) against Jurkat and molt-4 human cancer cell lines. Afr J Biotechnol. 2010;9(40):6787–90. Zandi K, Tajbakhsh S, Nabipour I, Rastian Z, Yousefi F, Sharafian S, Sartavi K. In vitro antitumor activity of Gracilaria corticata (a red alga) against Jurkat and molt-4 human cancer cell lines. Afr J Biotechnol. 2010;9(40):6787–90.
41.
go back to reference Sinicrope FA, Roddey G, McDonnell TJ, Shen Y, Cleary KR, Stephens LC. Increased apoptosis accompanies neoplastic development in the human colorectum. Clin Cancer Res. 1996;2(12):1999–2006.PubMed Sinicrope FA, Roddey G, McDonnell TJ, Shen Y, Cleary KR, Stephens LC. Increased apoptosis accompanies neoplastic development in the human colorectum. Clin Cancer Res. 1996;2(12):1999–2006.PubMed
42.
go back to reference Wang D, Lippard SJ. Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov. 2005;4(4):307–20.PubMedCrossRef Wang D, Lippard SJ. Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov. 2005;4(4):307–20.PubMedCrossRef
43.
go back to reference Gheda S, El-Sheekh M, Abou-Zeid A. In vitro anticancer activity of polysaccharide extracted from red alga Jania rubens against breast and colon cancer cell lines. Asian Paci J Trop Med. 2018;11(10):583.CrossRef Gheda S, El-Sheekh M, Abou-Zeid A. In vitro anticancer activity of polysaccharide extracted from red alga Jania rubens against breast and colon cancer cell lines. Asian Paci J Trop Med. 2018;11(10):583.CrossRef
44.
go back to reference Matloub AA, El-Souda SS, El-Senousy WM, Hamed M, Aly H, Ali SA, Ibrahim NA. In vitro antiviral, cytotoxic, antioxidant and hypolipidemic activities of polysaccharide isolated from marine algae. Int J Pharmacog Phytochem Res. 2015;7(5):1099–111. Matloub AA, El-Souda SS, El-Senousy WM, Hamed M, Aly H, Ali SA, Ibrahim NA. In vitro antiviral, cytotoxic, antioxidant and hypolipidemic activities of polysaccharide isolated from marine algae. Int J Pharmacog Phytochem Res. 2015;7(5):1099–111.
45.
go back to reference Awad NE, Selim MA, Metawe HM, Matloub AA. Cytotoxic xenicane diterpenes from the brown alga Padina pavonia (L.) Gaill. Phytothera Res Int J Devoted Pharmacol Toxicol Eval Nat Prod Derivat. 2008;22(12):1610–3. Awad NE, Selim MA, Metawe HM, Matloub AA. Cytotoxic xenicane diterpenes from the brown alga Padina pavonia (L.) Gaill. Phytothera Res Int J Devoted Pharmacol Toxicol Eval Nat Prod Derivat. 2008;22(12):1610–3.
46.
go back to reference Ahmed HH, Hegazi MM, Abd-Allac HI, Eskander EF, Ellithey MS. Antitumour and antioxidant activity of some Red Sea seaweeds in Ehrlich ascites carcinoma in vivo. Z Naturforsch C. 2011;66(7–8):367–76.PubMedCrossRef Ahmed HH, Hegazi MM, Abd-Allac HI, Eskander EF, Ellithey MS. Antitumour and antioxidant activity of some Red Sea seaweeds in Ehrlich ascites carcinoma in vivo. Z Naturforsch C. 2011;66(7–8):367–76.PubMedCrossRef
47.
go back to reference Mohini S, Chandraraj S, Balaji W. Anticancer activity of methanol extract of Jania Rubens Linn. Against Ehrlich as-cites carcinoma induced Balb/C Mice. World J Pharmaceuti Sci. 2014;2(10):1224–9. Mohini S, Chandraraj S, Balaji W. Anticancer activity of methanol extract of Jania Rubens Linn. Against Ehrlich as-cites carcinoma induced Balb/C Mice. World J Pharmaceuti Sci. 2014;2(10):1224–9.
48.
go back to reference Shamsabadi FT, Khoddami A, Fard SG, Abdullah R, Othman HH, Mohamed S. Comparison of tamoxifen with edible seaweed (Eucheuma cottonii L.) extract in suppressing breast tumor. Nutr Cancer. 2013;65(2):255–62.PubMedCrossRef Shamsabadi FT, Khoddami A, Fard SG, Abdullah R, Othman HH, Mohamed S. Comparison of tamoxifen with edible seaweed (Eucheuma cottonii L.) extract in suppressing breast tumor. Nutr Cancer. 2013;65(2):255–62.PubMedCrossRef
49.
go back to reference Lee H, Selvaraj B, Lee JW. Anticancer effects of seaweed-derived bioactive compounds. Appl Sci J. 2021;11(23):11261.CrossRef Lee H, Selvaraj B, Lee JW. Anticancer effects of seaweed-derived bioactive compounds. Appl Sci J. 2021;11(23):11261.CrossRef
50.
go back to reference Khorana AA, Kuderer NM, Culakova E, Lyman GH, Francis CW. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111:4902–7.PubMedPubMedCentralCrossRef Khorana AA, Kuderer NM, Culakova E, Lyman GH, Francis CW. Development and validation of a predictive model for chemotherapy-associated thrombosis. Blood. 2008;111:4902–7.PubMedPubMedCentralCrossRef
51.
go back to reference Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? The Lancet. 2001;357:539–45.CrossRef Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? The Lancet. 2001;357:539–45.CrossRef
52.
go back to reference Fogar P, Sperti C, Basso D, Sanzari MC, Greco E, Davoli C, Plebani M. Decreased total lymphocyte counts in pancreatic cancer: an index of adverse outcome. Pancreas. 2006;32(1):22–8.PubMedCrossRef Fogar P, Sperti C, Basso D, Sanzari MC, Greco E, Davoli C, Plebani M. Decreased total lymphocyte counts in pancreatic cancer: an index of adverse outcome. Pancreas. 2006;32(1):22–8.PubMedCrossRef
53.
go back to reference Schmidt H, Bastholt L, Geertsen P, Christensen IJ, Larsen S, Gehl J, Von Der Maase H. Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer. 2005;93(3):273–8.PubMedPubMedCentralCrossRef Schmidt H, Bastholt L, Geertsen P, Christensen IJ, Larsen S, Gehl J, Von Der Maase H. Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer. 2005;93(3):273–8.PubMedPubMedCentralCrossRef
54.
go back to reference Lissoni P, Fumagalli L, Brivio F, Rovelli F, Messina G, Di Fede G, Brera G. Cancer chemotherapy-induced lymphocytosis: a revolutionary discovery in the medical oncology. J Biol Regul Homeostat Agents. 2006;20(1–2):29–35. Lissoni P, Fumagalli L, Brivio F, Rovelli F, Messina G, Di Fede G, Brera G. Cancer chemotherapy-induced lymphocytosis: a revolutionary discovery in the medical oncology. J Biol Regul Homeostat Agents. 2006;20(1–2):29–35.
55.
go back to reference Olingy CE, Dinh HQ, Hedrick CC. Monocyte heterogeneity and functions in cancer. J Leukocyte Biol. 2019;106:309–22.PubMedCrossRef Olingy CE, Dinh HQ, Hedrick CC. Monocyte heterogeneity and functions in cancer. J Leukocyte Biol. 2019;106:309–22.PubMedCrossRef
56.
go back to reference Sagiv JY, Michaeli J, Assi S, Mishalian I, Kisos H, Levy L, Granot Z. Phenotypic diversity and plasticity in circulating neutrophil subpopulations in cancer. Cell Rep. 2015;10(4):562–73.PubMedCrossRef Sagiv JY, Michaeli J, Assi S, Mishalian I, Kisos H, Levy L, Granot Z. Phenotypic diversity and plasticity in circulating neutrophil subpopulations in cancer. Cell Rep. 2015;10(4):562–73.PubMedCrossRef
57.
go back to reference Baxevanis CN, Perez SA, Papamichail M. Combinatorial treatments including vaccines, chemotherapy and monoclonal antibodies for cancer therapy. Cancer Immunol Immunother. 2009;58(317):24. Baxevanis CN, Perez SA, Papamichail M. Combinatorial treatments including vaccines, chemotherapy and monoclonal antibodies for cancer therapy. Cancer Immunol Immunother. 2009;58(317):24.
58.
go back to reference Shen W, Wang H, Guo G, Tuo J. Immunomodulatory effects of Caulerpa racemosa var peltata polysaccharide and its selenizing product on T lymphocytes and NK cells in mice. Sci China Ser C Life Sci. 2008;51(9):795–801.CrossRef Shen W, Wang H, Guo G, Tuo J. Immunomodulatory effects of Caulerpa racemosa var peltata polysaccharide and its selenizing product on T lymphocytes and NK cells in mice. Sci China Ser C Life Sci. 2008;51(9):795–801.CrossRef
59.
go back to reference Caligiuri MA. Human natural killer cells. Blood J Am Soc Hematol. 2008;112(3):461–9. Caligiuri MA. Human natural killer cells. Blood J Am Soc Hematol. 2008;112(3):461–9.
60.
go back to reference Hoffman R, Donaldson J, Alban S, Franz G. Characterisation of a laminarin sulphate which inhibits basic fibroblast growth factor binding and endothelial cell proliferation. J Cell Sci. 1995;108(11):3591–8.PubMedCrossRef Hoffman R, Donaldson J, Alban S, Franz G. Characterisation of a laminarin sulphate which inhibits basic fibroblast growth factor binding and endothelial cell proliferation. J Cell Sci. 1995;108(11):3591–8.PubMedCrossRef
61.
go back to reference Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD, Meyer AS. Fucoidan from Sargassum sp. and Fucus vesiculosus reduces cell viability of lung carcinoma and melanoma cells in vitro and activates natural killer cells in mice in vivo. Int J Biol Macromol. 2011;49(3):331–6.PubMedCrossRef Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD, Meyer AS. Fucoidan from Sargassum sp. and Fucus vesiculosus reduces cell viability of lung carcinoma and melanoma cells in vitro and activates natural killer cells in mice in vivo. Int J Biol Macromol. 2011;49(3):331–6.PubMedCrossRef
62.
go back to reference Lowenthal RM, Fitton JH. Are seaweed-derived fucoidans possible future anticancer agents? J Appl Phycol. 2015;27(5):2075–7.CrossRef Lowenthal RM, Fitton JH. Are seaweed-derived fucoidans possible future anticancer agents? J Appl Phycol. 2015;27(5):2075–7.CrossRef
63.
go back to reference Fan Y, Wang W, Song W, Chen H, Teng A, Liu A. Partial characterization and antitumor activity of an acidic polysaccharide from Gracilaria lemaneiformis. Carbohyd Polym. 2012;88(4):1313–8.CrossRef Fan Y, Wang W, Song W, Chen H, Teng A, Liu A. Partial characterization and antitumor activity of an acidic polysaccharide from Gracilaria lemaneiformis. Carbohyd Polym. 2012;88(4):1313–8.CrossRef
64.
go back to reference Gesheva V, Chausheva S, Mihaylova N, Manoylov I, Doumanova L, Idakieva K, Tchorbanov A. Anticancer properties of gastropodan hemocyanins in murine model of colon carcinoma. BMC Immunol. 2014;15(1):34.PubMedPubMedCentralCrossRef Gesheva V, Chausheva S, Mihaylova N, Manoylov I, Doumanova L, Idakieva K, Tchorbanov A. Anticancer properties of gastropodan hemocyanins in murine model of colon carcinoma. BMC Immunol. 2014;15(1):34.PubMedPubMedCentralCrossRef
65.
go back to reference Ling NA, Li WL, Ji CF, Li HX, Liu XR, Qi Z. New advances in chemical structure and biological activity of seaweed polysaccharides. Chin Mar Med. 2021;40(1):69–78. Ling NA, Li WL, Ji CF, Li HX, Liu XR, Qi Z. New advances in chemical structure and biological activity of seaweed polysaccharides. Chin Mar Med. 2021;40(1):69–78.
66.
go back to reference Handayani D, Artasasta MA, Safirna N, Ayuni DF, Tallei TE, Hertiani T. Fungal isolates from marine sponge Chelonaplysilla sp.: diversity, antimicrobial and cytotoxic activities. Biodiversitas. 2020;21(5):1954–60.CrossRef Handayani D, Artasasta MA, Safirna N, Ayuni DF, Tallei TE, Hertiani T. Fungal isolates from marine sponge Chelonaplysilla sp.: diversity, antimicrobial and cytotoxic activities. Biodiversitas. 2020;21(5):1954–60.CrossRef
67.
go back to reference Sandrawati N, Hati SP, Yunita F, Putra AE, Ismed F, Tallei TE, Hertiani T, Handayani D. Antimicrobial and cytotoxic activities of marine sponge-derived fungal extracts isolated from Dactylospongia sp. J App Pharm Sci. 2020;10(4):28–33.CrossRef Sandrawati N, Hati SP, Yunita F, Putra AE, Ismed F, Tallei TE, Hertiani T, Handayani D. Antimicrobial and cytotoxic activities of marine sponge-derived fungal extracts isolated from Dactylospongia sp. J App Pharm Sci. 2020;10(4):28–33.CrossRef
68.
go back to reference Sanger G, Rarung LK, Wonggo D, Dotulong V, Damongilala LJ, Tallei TE. Cytotoxic activity of seaweeds from North Sulawesi marine waters against cervical cancer. J Appl Pharm Sci. 2021;11:66–73. Sanger G, Rarung LK, Wonggo D, Dotulong V, Damongilala LJ, Tallei TE. Cytotoxic activity of seaweeds from North Sulawesi marine waters against cervical cancer. J Appl Pharm Sci. 2021;11:66–73.
69.
go back to reference Osman NAHK, Siam A, El-Manawy IM, Jeon YJ. Anticancer Activity of a scarcely investigated Red Sea Brown Alga Hormophysa cuneiformis against HL60, A549, HCT116 and B16 Cell Lines. Egypt J Aquat Biol Fish. 2020;24(1):497–508.CrossRef Osman NAHK, Siam A, El-Manawy IM, Jeon YJ. Anticancer Activity of a scarcely investigated Red Sea Brown Alga Hormophysa cuneiformis against HL60, A549, HCT116 and B16 Cell Lines. Egypt J Aquat Biol Fish. 2020;24(1):497–508.CrossRef
70.
go back to reference Cotas J, Pacheco D, Gonçalves AM, Silva P, Carvalho LG, Pereira L. Seaweeds’ nutraceutical and biomedical potential in cancer therapy: a concise review. J Cancer Metastatis Treat. 2021;7:13. Cotas J, Pacheco D, Gonçalves AM, Silva P, Carvalho LG, Pereira L. Seaweeds’ nutraceutical and biomedical potential in cancer therapy: a concise review. J Cancer Metastatis Treat. 2021;7:13.
71.
go back to reference Liu T, Li Q, Li G, Tian C, Zhang T. Molecular mechanisms of anti-cancer bioactivities of seaweed polysaccharides. Chin Herb Med. 2022. Liu T, Li Q, Li G, Tian C, Zhang T. Molecular mechanisms of anti-cancer bioactivities of seaweed polysaccharides. Chin Herb Med. 2022.
72.
go back to reference Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled Annexin V. J Immunoll Methods. 1995;184:39–51.CrossRef Vermes I, Haanen C, Steffens-Nakken H, Reutelingsperger C. A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labeled Annexin V. J Immunoll Methods. 1995;184:39–51.CrossRef
73.
go back to reference Wlodkowic D, Skommer J, Darzynkiewicz Z. Flow cytometry-based apoptosis detection. In: apoptosis. Totova: Humana Press; 2009. p. 19–32.CrossRef Wlodkowic D, Skommer J, Darzynkiewicz Z. Flow cytometry-based apoptosis detection. In: apoptosis. Totova: Humana Press; 2009. p. 19–32.CrossRef
74.
go back to reference Jose GM. Biological responses of algal derived sulfated polysaccharides: an emphasis on cancer prophylaxis. Trends Biomater Artif Organs. 2015; 29(1). Jose GM. Biological responses of algal derived sulfated polysaccharides: an emphasis on cancer prophylaxis. Trends Biomater Artif Organs. 2015; 29(1).
75.
go back to reference Jose GM, Raghavankutty M, Kurup GM. Sulfated polysaccharides from Padina tetrastromatica induce apoptosis in HeLa cells through ROS triggered mitochondrial pathway. Process Biochem. 2018;68:197–204.CrossRef Jose GM, Raghavankutty M, Kurup GM. Sulfated polysaccharides from Padina tetrastromatica induce apoptosis in HeLa cells through ROS triggered mitochondrial pathway. Process Biochem. 2018;68:197–204.CrossRef
76.
go back to reference Ghouri N, Preiss D, Sattar N. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease: a narrative review and clinical perspective of prospective data. Hepatology. 2010;52:1156–61.PubMedCrossRef Ghouri N, Preiss D, Sattar N. Liver enzymes, nonalcoholic fatty liver disease, and incident cardiovascular disease: a narrative review and clinical perspective of prospective data. Hepatology. 2010;52:1156–61.PubMedCrossRef
77.
go back to reference Rajesh MJ, Latha MS. Preliminary evaluation of the antihepatotoxic activity of Kamilari, a polyherbal formulation. J Ethnopharmacol. 2004;1:99–104.CrossRef Rajesh MJ, Latha MS. Preliminary evaluation of the antihepatotoxic activity of Kamilari, a polyherbal formulation. J Ethnopharmacol. 2004;1:99–104.CrossRef
78.
go back to reference Orinya OA, Adenkola AY, Ogbe RJ. Haematological and biochemical studies on the effect of diclofenac sodium on Wistar Rattus Norvegicus. Int J Biol Chem Sci. 2016;10(5):2231–42.CrossRef Orinya OA, Adenkola AY, Ogbe RJ. Haematological and biochemical studies on the effect of diclofenac sodium on Wistar Rattus Norvegicus. Int J Biol Chem Sci. 2016;10(5):2231–42.CrossRef
79.
go back to reference Singh A, Bhat TK, Sharma OP. Clin Biochem Hepatotoxicol. J Clin Toxicol. 2011;4:001–0019. Singh A, Bhat TK, Sharma OP. Clin Biochem Hepatotoxicol. J Clin Toxicol. 2011;4:001–0019.
81.
go back to reference El Gamal AA. Biological importance of marine algae. Saudi Pharmaceut J. 2010;18(1):1–25.CrossRef El Gamal AA. Biological importance of marine algae. Saudi Pharmaceut J. 2010;18(1):1–25.CrossRef
82.
go back to reference Cüre MC, Cüre E, Kalkan Y, Kırbaş A, Tümkaya L, Yılmaz A, Yüce S. Infliximab modulates cisplatin-induced hepatotoxicity in rats. Balkan Med J. 2016;33(5):504.PubMedPubMedCentralCrossRef Cüre MC, Cüre E, Kalkan Y, Kırbaş A, Tümkaya L, Yılmaz A, Yüce S. Infliximab modulates cisplatin-induced hepatotoxicity in rats. Balkan Med J. 2016;33(5):504.PubMedPubMedCentralCrossRef
83.
go back to reference Bentli R, Parlakpinar H, Polat A, Samdanci E, Sarihan ME, Sagir M. Molsidomine prevents cisplatin-induced hepatotoxicity. Arch Med Res. 2013;44(7):521–8.PubMedCrossRef Bentli R, Parlakpinar H, Polat A, Samdanci E, Sarihan ME, Sagir M. Molsidomine prevents cisplatin-induced hepatotoxicity. Arch Med Res. 2013;44(7):521–8.PubMedCrossRef
84.
go back to reference Sastry J, Kellie SJ. Severe neurotoxicity, ototoxicity and nephrotoxicity following high-dose cisplatin and amifostine. Pediat Hematol Oncol. 2005;22(5):441–5.CrossRef Sastry J, Kellie SJ. Severe neurotoxicity, ototoxicity and nephrotoxicity following high-dose cisplatin and amifostine. Pediat Hematol Oncol. 2005;22(5):441–5.CrossRef
85.
go back to reference Tadagavadi R, Reeves WB. Neutrophils in cisplatin AKI—mediator or marker? Kidney Int. 2017;92(1):11–3.PubMedCrossRef Tadagavadi R, Reeves WB. Neutrophils in cisplatin AKI—mediator or marker? Kidney Int. 2017;92(1):11–3.PubMedCrossRef
Metadata
Title
Antitumor immunity and therapeutic properties of marine seaweeds-derived extracts in the treatment of cancer
Authors
Mostafa M. El-Sheekh
Mohamed Nassef
Eman Bases
Shimaa El Shafay
Rania El-shenody
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Cancer Cell International / Issue 1/2022
Electronic ISSN: 1475-2867
DOI
https://doi.org/10.1186/s12935-022-02683-y

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