The influence of Spirulina platensis filtrates on caco-2 proliferative activity and expression of apoptosis-related microRNAs and mRNA

Marine Drugs

Volumn 15, Issue 3, 2017, Pages

  Smieszek, Agnieszká ^a   Giezek, Ewa ^a   Chrapiec, Martyna ^a   Murat, Martyna ^a   Mucha, Aleksandra ^a   Michalak, Izabela ^b   Marycz, Krzysztof ^a,c  

^a WROC AW UNIVERSITY OF ENVIRONMENTAL AND LIFE SCIENCES   (Poland)

^b WROCLAW UNIVERSITY OF TECHNOLOGY   (Poland)

^c WROCLAW RESEARCH CENTRE EIT   (Poland)

Author keywords

Anti cancer effect; Apoptosis; Colon; Cytotoxic effect; Human colon cancer; Morphology; Proliferation; Spirulina

Indexed keywords

ALGAL EXTRACT; ANTINEOPLASTIC AGENT; ARTHROSPIRA PLATENSIS EXTRACT; CYCLIN D1; MESSENGER RNA; METALLOPROTEINASE; MICRORNA; MICRORNA 145; MICRORNA 146; MICRORNA 17; MYC PROTEIN; NITRIC OXIDE; PROTEIN BAX; PROTEIN BCL 2; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; WNT10B PROTEIN;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTHROSPIRA PLATENSIS; ARTICLE; AUTOCRINE EFFECT; CACO-2 CELL LINE; CELL CYCLE G0 PHASE; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; COLON CANCER; CONTROLLED STUDY; DRUG CYTOTOXICITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; UPREGULATION; CELL SURVIVAL; CHEMISTRY; COLON TUMOR; DRUG EFFECTS; GENETICS; METABOLISM; MITOCHONDRION; SPIRULINA; TUMOR CELL LINE;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CACO-2 CELLS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; COLONIC NEOPLASMS; HUMANS; METALLOPROTEASES; MICRORNAS; MITOCHONDRIA; NITRIC OXIDE; PROTO-ONCOGENE PROTEINS C-BCL-2; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SPIRULINA; UP-REGULATION;

EID: 85016464925     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md15030065     Document Type: Article

References (60)

1. Kim, S.-K.; Thomas, N.V.; Li, X. Anticancer compounds from marine macroalgae and their application as medicinal foods. Adv. Food Nutr. Res. 2011, 64, 213-224. [PubMed]
2. Shalaby, E.A. Algae as promising organisms for environment and health. Plant Signal. Behav. 2011, 6, 1338-1350. [CrossRef] [PubMed]
3. Xie, P.; Fujii, I.; Zhao, J.; Shinohara, M.; Matsukura, M. A novel polysaccharide derived from algae extract induces apoptosis and cell cycle arrest in human gastric carcinoma MKN45 cells via ROS/JNK signaling pathway. Int. J. Oncol. 2016, 49, 1561-1568. [CrossRef] [PubMed]
4. Alves, C.; Pinteus, S.; Horta, A.; Pedrosa, R. High cytotoxicity and anti-proliferative activity of algae extracts on an in vitro model of human hepatocellular carcinoma. Springerplus 2016, 5, 1339. [CrossRef] [PubMed]
5. Kim, Y.-S.; Li, X.-F.; Kang, K.-H.; Ryu, B.; Kim, S.K. Stigmasterol isolated from marine microalgae Navicula incerta induces apoptosis in human hepatoma HepG2 cells. BMB Rep. 2014, 47, 433-438. [CrossRef] [PubMed]
6. Erfani, N.; Nazemosadat, Z.; Moein, M. Cytotoxic activity of ten algae from the Persian Gulf and Oman Sea on human breast cancer cell lines; MDA-MB-231, MCF-7, and T-47D. Pharmacogn. Res. 2015, 7, 133-137.
7. Kim, M.S.; Kim, J.Y.; Choi,W.H.; Lee, S.S. Effects of seaweed supplementation on blood glucose concentration, lipid profile, and antioxidant enzyme activities in patients with type 2 diabetes mellitus. Nutr. Res. Pract. 2008, 2, 62-67. [CrossRef] [PubMed]
8. Anitha, L.; Chandralekha, K. Effect of Supplementation of Spirulina on Blood Glucose, Glycosylated Hemoglobin and Lipid Profile of Male Non-Insulin Dependent Diabetics. Asian J. Exp. Biol. Sci. 2010, 1, 36-46.
9. Ahmadi, A.; Zorofchian Moghadamtousi, S.; Abubakar, S.; Zandi, K. Antiviral Potential of Algae Polysaccharides Isolated from Marine Sources: A Review. Biomed. Res. Int. 2015, 2015, 825203. [CrossRef] [PubMed]
10. Simpore, J.; Zongo, F.; Kabore, F.; Dansou, D.; Bere, A.; Nikiema, J.-B.; Pignatelli, S.; Biondi, D.M.; Ruberto, G.; Musumeci, S. Nutrition rehabilitation of HIV-infected and HIV-negative undernourished children utilizing spirulina. Ann. Nutr. Metab. 2005, 49, 373-380. [CrossRef] [PubMed]
11. Ismail, M.; Hossain, M.F.; Tanu, A.R.; Shekhar, H.U. Effect of Spirulina Intervention on Oxidative Stress, Antioxidant Status, and Lipid Profile in Chronic Obstructive Pulmonary Disease Patients. BioMed Res. Int. 2015, 2015, 486120. [CrossRef] [PubMed]
12. Bashandy, S.A.E.; El Awdan, S.A.; Ebaid, H.; Alhazza, I.M. Antioxidant Potential of Spirulina platensis Mitigates Oxidative Stress and Reprotoxicity Induced by Sodium Arsenite in Male Rats. Oxid. Med. Cell. Longev. 2016, 2016, 7174351. [CrossRef] [PubMed]
13. Wu, Q.; Liu, L.; Miron, A.; Klímová, B.; Wan, D.; Kuca, K. The antioxidant, immunomodulatory, and anti-inflammatory activities of Spirulina: An overview. Arch. Toxicol. 2016, 90, 1817-1840. [CrossRef] [PubMed]
14. Jibri, S.M.; Jakada, B.H.; Umar, H.Y.; Ahmad, T.A. Importance of Some Algal Species as a Source of Food and Supplement. Int. J. Curr. Microbiol. Appl. Sci. 2016, 5, 186-193. [CrossRef]
15. Khan, Z.; Bhadouria, P.; Bisen, P.S. Nutritional and therapeutic potential of Spirulina. Curr. Pharm. Biotechnol. 2005, 6, 373-379. [CrossRef] [PubMed]
16. De Assis, L.M.; Machado, A.R.; Motta, A.S.; Costa, J.A.V.; de Souza-Soares, L.A. Development and Characterization of Nanovesicles Containing Phenolic Compounds of Microalgae Spirulina Strain LEB-18 and Chlorella pyrenoidosa. Adv. Mater. Phys. Chem. 2014, 4, 6-12. [CrossRef]
17. Konícková, R.; Va nková, K.; Vaníková, J.; Vá nová, K.; Muchová, L.; Subhanová, I.; Zadinová, M.; Zelenka, J.; Dvorák, A.; Kolár, M.; et al. Anti-Cancer effects of blue-green alga Spirulina platensis, a natural source of bilirubin-like tetrapyrrolic compounds. Ann. Hepatol. 2014, 13, 273-283. [PubMed]
18. Feng, Y.; Zhu, J.; Ou, C.; Deng, Z.; Chen, M.; Huang,W.; Li, L. MicroRNA-145 inhibits tumour growth and metastasis in colorectal cancer by targeting fascin-1. Br. J. Cancer 2014, 110, 2300-2309. [CrossRef] [PubMed]
19. Dews, M.; Homayouni, A.; Yu, D.; Murphy, D.; Sevignani, C.;Wentzel, E.; Furth, E.E.; Lee,W.M.; Enders, G.H.; Mendell, J.T.; et al. Augmentation of tumor angiogenesis by a Myc-Activated microRNA cluster. Nat. Genet. 2006, 38, 1060-1065. [CrossRef] [PubMed]
20. Omrane, I.; Kourda, N.; Stambouli, N.; Privat, M.; Medimegh, I.; Arfaoui, A.; Uhrhammer, N.; Bougatef, K.; Baroudi, O.; Bouzaienne, H.; et al. MicroRNAs 146a and 147b Biomarkers for Colorectal Tumor's Localization. BioMed Res. Int. 2014, 2014, e584852. [CrossRef] [PubMed]
21. Chen, F.; Zhang, Q. Inhibitive effects of spirulina on aberrant crypts in colon induced by dimethylhydrazine. Zhonghua Yu Fang Yi Xue Za Zhi 1995, 29, 13-17. [PubMed]
22. Álvarez-González, I.; Islas-Islas, V.; Chamorro-Cevallos, G.; Barrios, J.P.; Paniagua, N.; Vásquez-Garzón, V.R.; Villa-Treviño, S.; Madrigal-Santillán, O.; Morales-González, J.A.; Madrigal-Bujaidar, E. Inhibitory Effect of Spirulina maxima on the Azoxymethane-induced Aberrant Colon Crypts and Oxidative Damage in Mice. Pharmacogn. Mag. 2015, 11, S619-S624. [PubMed]
23. Smieszek, A.; Donesz-Sikorska, A.; Grzesiak, J.; Krzak, J.; Marycz, K. Biological effects of sol-gel derived ZrO2 and SiO2/ZrO2 coatings on stainless steel surface-In vitro model using mesenchymal stem cells. J. Biomater. Appl. 2014, 29, 699-714. [CrossRef] [PubMed]
24. Kornicka, K.; Marycz, K.; Tomaszewski, K.A.; Maredziak, M.; Śmieszek, A. The Effect of Age on Osteogenic and Adipogenic Differentiation Potential of Human Adipose Derived Stromal Stem Cells (hASCs) and the Impact of Stress Factors in the Course of the Differentiation Process. Oxid. Med. Cell. Longev. 2015, 2015, e309169. [CrossRef] [PubMed]
25. Śmieszek, A.; Czyrek, A.; Basinska, K.; Trynda, J.; Skaradzi ńska, A.; Siudzi ńska, A.; Maredziak, M.; Marycz, K. Effect of Metformin on Viability, Morphology, and Ultrastructure of Mouse Bone Marrow-Derived Multipotent Mesenchymal Stromal Cells and Balb/3T3 Embryonic Fibroblast Cell Line. BioMed. Res. Int. 2015, 2015, e769402. [CrossRef] [PubMed]
26. Chomczynski, P.; Sacchi, N. Single-Step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 1987, 162, 156-159. [CrossRef]
27. Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: Sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 2015, 136, E359-E386. [CrossRef] [PubMed]
28. Ren, B.-J.; Zhou, Z.-W.; Zhu, D.-J.; Ju, Y.-L.; Wu, J.-H.; Ouyang, M.-Z.; Chen, X.-W.; Zhou, S.-F. Alisertib Induces Cell Cycle Arrest, Apoptosis, Autophagy and Suppresses EMT in HT29 and Caco-2 Cells. Int. J. Mol. Sci. 2015, 17, 41. [CrossRef] [PubMed]
29. Moussavou, G.; Kwak, D.H.; Obiang-Obonou, B.W.; Ogandaga Maranguy, C.A.; Dinzouna-Boutamba, S.-D.; Lee, D.H.; Manvoudou Pissibanganga, O.G.; Ko, K.; Seo, J.I.; Choo, Y.K. Anticancer Effects of Different Seaweeds on Human Colon and Breast Cancers. Mar. Drugs 2014, 12, 4898-4911. [CrossRef] [PubMed]
30. O'Neill, A.M.; Burrington, C.M.; Gillaspie, E.A.; Lynch, D.T.; Horsman, M.J.; Greene, M.W. High-FatWestern diet-induced obesity contributes to increased tumor growth in mouse models of human colon cancer. Nutr. Res. 2016, 36, 1325-1334. [CrossRef] [PubMed]
31. Lee, J.-C.; Hou, M.-F.; Huang, H.-W.; Chang, F.-R.; Yeh, C.-C.; Tang, J.-Y.; Chang, H.-W. Marine algal natural products with anti-oxidative, anti-inflammatory, and anti-cancer properties. Cancer Cell Int. 2013, 13, 55. [CrossRef] [PubMed]
32. Béliveau, R.; Gingras, D. Role of nutrition in preventing cancer. Can. Fam. Phys. 2007, 53, 1905-1911.
33. Subhashini, J.; Mahipal, S.V.K.; Reddy, M.C.; Mallikarjuna Reddy, M.; Rachamallu, A.; Reddanna, P. Molecular mechanisms in C-Phycocyanin induced apoptosis in human chronic myeloid leukemia cell line-K562. Biochem. Pharmacol. 2004, 68, 453-462. [CrossRef] [PubMed]
34. Ouhtit, A.; Gaur, R.L.; Abdraboh, M.; Ireland, S.K.; Rao, P.N.; Raj, S.G.; Al-Riyami, H.; Shanmuganathan, S.; Gupta, I.; Murthy, S.N.; et al. Simultaneous Inhibition of Cell-Cycle, Proliferation, Survival, Metastatic Pathways and Induction of Apoptosis in Breast Cancer Cells by a Phytochemical Super-Cocktail: Genes That Underpin Its Mode of Action. J. Cancer 2013, 4, 703-715. [CrossRef] [PubMed]
35. Gambato, G.; Baroni, É.G.; Garcia, C.S.C.; Frassini, R.; Frozza, C.O.S.; Moura, S.; Pereira, C.M.P.; Fujii, M.T.; Colepicolo, P.; Lambert, A.P.F.; et al. Brown Algae Himantothallus grandifolius (Desmarestiales, Phaeophyceae) Suppresses Proliferation and Promotes Apoptosis-Mediated Cell Death in Tumor Cells. Adv. Biol. Chem. 2014, 4, 98. [CrossRef]
36. Yoon, J.S.; Woo, H.C.; Kim, H.R.; Kim, G.-D. The Extracts of Sargassum fulvellum Induce Pro-Apoptosis and Cell Cycle Arrest on MDA-MB-231 Human Breast Carcinoma Cells. Cancer Prev. Res. 2010, 15, 52-59.
37. Han, Y.-S.; Lee, J.H.; Lee, S.H. Fucoidan inhibits the migration and proliferation of HT-29 human colon cancer cells via the phosphoinositide-3 kinase/Akt/mechanistic target of rapamycin pathways. Mol. Med. Rep. 2015, 12, 3446-3452. [CrossRef] [PubMed]
38. Chung, T.-W.; Choi, H.-J.; Lee, J.-Y.; Jeong, H.-S.; Kim, C.-H.; Joo, M.; Choi, J.-Y.; Han, C.-W.; Kim, S.-Y.; Choi, J.-S.; et al. Marine algal fucoxanthin inhibits the metastatic potential of cancer cells. Biochem. Biophys. Res. Commun. 2013, 439, 580-585. [CrossRef] [PubMed]
39. Lagoutte, E.; Villeneuve, C.; Lafanechère, L.; Wells, C.M.; Jones, G.E.; Chavrier, P.; Rossé, C. LIMK Regulates Tumor-Cell Invasion and Matrix Degradation through Tyrosine Phosphorylation of MT1-MMP. Sci. Rep. 2016, 6, 24925. [CrossRef] [PubMed]
40. Said, A.H.; Raufman, J.-P.; Xie, G. The Role of Matrix Metalloproteinases in Colorectal Cancer. Cancers (Basel) 2014, 6, 366-375. [CrossRef] [PubMed]
41. Weng, M.T.; Tsao, P.N.; Lin, H.L.; Tung, C.C.; Change, M.C.; Chang, Y.T.;Wong, J.M.;Wei, S.C. Hes1 Increases the Invasion Ability of Colorectal Cancer Cells via the STAT3-MMP14 Pathway. PLoS ONE 2015, 10, e0144322. [CrossRef] [PubMed]
42. Scholer-Dahirel, A.; Schlabach, M.R.; Loo, A.; Bagdasarian, L.; Meyer, R.; Guo, R.;Woolfenden, S.; Yu, K.K.; Markovits, J.; Killary, K.; et al. Maintenance of adenomatous polyposis coli (APC)-mutant colorectal cancer is dependent on Wnt/-catenin signaling. Proc. Natl. Acad. Sci. USA 2011, 108, 17135-17140. [CrossRef] [PubMed]
43. Voloshanenko, O.; Erdmann, G.; Dubash, T.D.; Augustin, I.; Metzig, M.; Moffa, G.; Hundsrucker, C.; Kerr, G.; Sandmann, T.; Anchang, B.; et al. Wnt secretion is required to maintain high levels of Wnt activity in colon cancer cells. Nat. Commun. 2013, 4, 2610. [CrossRef] [PubMed]
44. Wang, G.-Q.; Lu, Z.-H.; Fang, Y.-J.; Chen, G.; Zhou, Z.-W.; Pan, Z.-Z.; Wan, D.-S. Expression and clinical significance of survivin and matrix metalloproteinase-7 in colon cancer. Ai Zheng 2009, 28, 945-949. [CrossRef] [PubMed]
45. Fang, Y.; Zhou, H.; Xia, J.-F.; Lin, J.-J.; Li, R.-Z.; Yang, D.-Q.; Xu, M.-Y.; Li, X.-Y. Ellagic acid regulates Wnt/-catenin signaling pathway and CDK8 in HCT 116 and HT 29 colon cancer cells. Bangladesh J. Pharmacol. 2015, 10, 47-56. [CrossRef]
46. Shan, B.-E.; Wang, M.-X.; Li, R. Quercetin inhibit human SW480 colon cancer growth in association with inhibition of cyclin D1 and survivin expression through Wnt/beta-catenin signaling pathway. Cancer Investig. 2009, 27, 604-612. [CrossRef] [PubMed]
47. Kim, E.J.; Park, S.Y.; Lee, J.-Y.; Park, J.H.Y. Fucoidan present in brown algae induces apoptosis of human colon cancer cells. BMC Gastroenterol. 2010, 10, 96. [CrossRef] [PubMed]
48. Ryu, M.J.; Kim, A.D.; Kang, K.A.; Chung, H.S.; Kim, H.S.; Suh, I.S.; Chang, W.Y.; Hyun, J.W. The green algae Ulva fasciata Delile extract induces apoptotic cell death in human colon cancer cells. In Vitro Cell. Dev. Biol. Anim. 2013, 49, 74-81. [CrossRef] [PubMed]
49. Xue, M.; Ge, Y.; Zhang, J.; Wang, Q.; Hou, L.; Liu, Y.; Sun, L.; Li, Q. Anticancer properties and mechanisms of fucoidan on mouse breast cancer in vitro and in vivo. PLoS ONE 2012, 7, e43483. [CrossRef] [PubMed]
50. Chu, W.-L.; Lim, Y.-W.; Radhakrishnan, A.K.; Lim, P.-E. Protective effect of aqueous extract from Spirulina platensis against cell death induced by free radicals. BMC Complement. Altern. Med. 2010, 10, 53. [CrossRef] [PubMed]
51. Karawita, R.; Senevirathne, M.; Athukorala, Y.; Affan, A.; Lee, Y.-J.; Kim, S.-K.; Lee, J.-B.; Jeon, Y.-J. Protective effect of enzymatic extracts from microalgae against DNA damage induced by H2O2. Mar. Biotechnol. 2007, 9, 479-490. [CrossRef] [PubMed]
52. Huang, H.-L.; Wu, S.-L.; Liao, H.-F.; Jiang, C.-M.; Huang, R.-L.; Chen, Y.-Y.; Yang, Y.-C.; Chen, Y.-J. Induction of apoptosis by three marine algae through generation of reactive oxygen species in human leukemic cell lines. J. Agric. Food Chem. 2005, 53, 1776-1781. [CrossRef] [PubMed]
53. Pardhasaradhi, B.V.V.; Ali, A.M.; Kumari, A.L.; Reddanna, P.; Khar, A. Phycocyanin-Mediated apoptosis in AK-5 tumor cells involves down-regulation of Bcl-2 and generation of ROS. Mol. Cancer Ther. 2003, 2, 1165-1170. [PubMed]
54. Liu, J.; Wang, Z. Increased Oxidative Stress as a Selective Anticancer Therapy. Oxid. Med. Cell. Longev. 2015, 2015, 294303. [CrossRef] [PubMed]
55. Xu, S.; Zhang, R.; Niu, J.; Cui, D.; Xie, B.; Zhang, B.; Lu, K.; Yu, W.; Wang, X.; Zhang, Q. Oxidative Stress Mediated-Alterations of the MicroRNA Expression Profile in Mouse Hippocampal Neurons. Int. J. Mol. Sci. 2012, 13, 16945-16960. [CrossRef] [PubMed]
56. Chi, Y.; Zhou, D. MicroRNAs in colorectal carcinoma-from pathogenesis to therapy. J. Exp. Clin. Cancer Res. 2016, 35, 43. [CrossRef] [PubMed]
57. Schee, K.; Boye, K.; Abrahamsen, T.W.; Fodstad, O.; Flatmark, K. Clinical relevance of microRNA miR-21, miR-31, miR-92a, miR-101, miR-106a and miR-145 in colorectal cancer. BMC Cancer 2012, 12, 505. [CrossRef] [PubMed]
58. Ren, A.; Dong, Y.; Tsoi, H.; Yu, J. Detection of miRNA as non-invasive biomarkers of colorectal cancer. Int. J. Mol. Sci. 2015, 16, 2810-2823. [CrossRef] [PubMed]
59. Knudsen, K.N.; Nielsen, B.S.; Lindebjerg, J.; Hansen, T.F.; Holst, R.; Sørensen, F.B. microRNA-17 Is the Most Up-Regulated Member of the miR-17-92 Cluster during Early Colon Cancer Evolution. PLoS ONE 2015, 10, e0140503. [CrossRef] [PubMed]
60. Gomes, S.E.; Simões, A.E.S.; Pereira, D.M.; Castro, R.E.; Rodrigues, C.M.P.; Borralho, P.M. miR-143 or miR-145 overexpression increases cetuximab-mediated antibody-dependent cellular cytotoxicity in human colon cancer cells. Oncotarget 2016, 7, 9368-9387. [PubMed]