C-phycocyanins: Immune system modulation and its possible application as therapy against cancer

Main Article Content

Álvaro Esteban Alfaro-Alfaro
Valerie Alpízar-Cambronero
Ana Iris Duarte-Rodríguez
Joana Feng-Feng
Christopher Rosales-Leiva
Juan José Mora-Román

Abstract

Cancer is a complex, heterogeneous, and dynamic disease, characterized by uncontrolled mitosis. Historically, it has been treated with surgery, radiotherapy and chemotherapy, and in more recent years through immunotherapy. For this, different proteins have been investigated for the modulation of the immune response. A group of these are C-phycocyanins, biliproteins from bluish-green microalgae such as Spirulina platensis. The anti-inflammatory environment in healthy people is a prophylactic measure to reduce the risk of developing a certain type of cancer. Its intake has shown that behavior, by suppressing the release of pro-inflammatory substances. An immunomodulatory effect has also been appreciated by increasing or decreasing the expression of CD59, as well as by causing the macrophage proliferation and the release of inflammatory substances. The latter is an indication that there is insufficient information to corroborate its use as a prophylactic or therapeutic option against cancer. Therefore, the information about natural substances such as this one is transcendental, because although they are more attractive to treat this disease, there are no fully proven therapeutic effects.

Article Details

How to Cite
Alfaro-Alfaro, Álvaro E., Alpízar-Cambronero, V., Duarte-Rodríguez, A. I., Feng-Feng, J., Rosales-Leiva, C., & Mora-Román, J. J. (2020). C-phycocyanins: Immune system modulation and its possible application as therapy against cancer. Tecnología En Marcha Journal, 33(4), Pág. 125–139. https://doi.org/10.18845/tm.v33i4.4653
Section
Artículo científico
Author Biography

Juan José Mora-Román, Universidad de Costa Rica

Departamento de Farmacia Industrial, Facultad de Farmacia, Universidad de Costa Rica

References

C. Moses, B. García-Bloj, A. R. Harvey, and P. Blancafort, “Hallmarks of cancer: The CRISPR generation,” European Journal of Cancer, 93, 10-18, 2018.

F. Bray, J. Ferlay, I. Soerjomataram, R. L. Siegel, L. A. Torre, and A. Jemal, “Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries,” CA: A Cancer Journal for Clinicians, 68(6), 394-424, 2018.

Ministerio de Salud. (2019, Mayo). Estadística de Cáncer - Registro Nacional Tumores. [en línea]. Disponible en: https://www.ministeriodesalud.go.cr/index.php/vigilancia-de-la-salud/estadisticas-y-bases-de-datos/esta-disticas/estadistica-de-cancer-registro-nacional-tumores.

International Agency for Research on Cancer, “World cancer factsheet,” Cancer Research UK, Londres, 2014. [5] A. Ramos Molina, “Obtención y Purificación de Ficocianinas Mediante Cromatografía de Adsorción en Lecho Expandido. Escalado del Proceso, Caracterización Fisicoquímica y Aplicación como Colorantes Naturales,” tesis doctoral, Universidad de Jáen, Andalucía, España, 2011.

A. Schwabe and F. J. Bruggeman, “Contributions of Cell Growth and Biochemical Reactions to Nongenetic Variability of Cells,” Biophysical Journal, 107(2), 301-313, 2014.

L. A. Loeb, K. R. Loeb, and J. P. Anderson, “Multiple mutations and cancer,” Proceedings of the National Academy of Sciences of the United States of America, 100(3), 776-781, 2003.

A. S. Boyer, D. Walter, and C. S. Sørensen, “DNA replication and cancer: From dysfunctional replication origin activities to therapeutic opportunities,” Seminars in Cancer Biology, 37-38, 16-25, 2016.

Organización Mundial de la Salud. (2018, Setiembre 12). Cáncer. [en línea]. Disponible en: https://www.who.int/es/news-room/fact-sheets/detail/cancer

R. de la Peña-López y Y. A. Remolina-Bonilla, “Cáncer,” Gaceta Médica De México, 152 (supl 1), 63-66, 2016.

S. M. Parizadeh, R. Jafarzadeh-Esfehani, S. M. Hassanian, S. M. R. Parizadeh, S. Vojdani, M. Ghandehari et al, “Targeting cancer stem cells as therapeutic approach in the treatment of colorectal cancer,” The International Journal of Biochemistry and Cell Biology, 110, 75-83, 2019.

F. Nasim, B. F. Sabath, and G. A. Eapen, “Lung Cancer,” Medical Clinics of North America, 103(3), 463-473, 2019.

D. Hanahan and R. A. Weinberg, “Hallmarks of Cancer: The Next Generation,” Cell, 144(5), 646-674, 2011.

F. Rodríguez Montero, “Cáncer gástrico: Su relación con Helicobacter pylori,” Revista Médica de Costa Rica y Centroamérica, 71(609), 5-7, 2014.

A. Ghosh, D. Ghartimagar, and S. Thapa, “Oncogenes – the basics,” Journal of Biomedical Sciences, 3(4), 35-37, 2016.

E. F. e Silva, F. da Silva Figueira, A. P. Lettnin, M. Carrett-Dias, D. M. V. B. Filgueira, S. Kalil et al, “C-Phycocyanin: Cellular targets, mechanisms of action and multi drug resistance in cancer,” Pharmacological Reports, 70(1), 75-80, 2017.

J. C. Arthur, E. Perez-Chanona, M. Mühlbauer, S. Tomkovich, J. M. Uronis, T. J. Fan et al, “Intestinal Inflammation Targets Cancer-Inducing Activity of the Microbiota,” Science, 338(6103), 120-123, 2012.

S. M. Crusz and F. R. Balkwill, “Inflammation and cancer: advances and new agents,” Nature Reviews Clinical Oncology, 12(10), 584-596, 2015.

L. Zitvogel, F. Pietrocola, and G. Kroemer, “Nutrition, inflammation and cancer,” Nature Immunology, 18(8), 843-850, 2017.

L. Zamai, C. Ponti, P. Mirandola, G. Gobbi, S. Papa, L. Galeotti et al, “NK Cells and Cancer,” The Journal of Immunology, 178(7), 4011-4016, 2007.

S. M. A. Mahmoud, E. C. Paish, D. G. Powe, R. D. Macmillan, M. J. Grainge, A. H. S. Lee et al, “Tumor-Infiltrating CD8+ Lymphocytes Predict Clinical Outcome in Breast Cancer,” Journal of Clinical Oncology, 29(15), 1949- 1955, 2011.

J. Hamanishi, M. Mandai, M. Iwasaki, T. Okazaki, Y. Tanaka, K. Yamaguchi et al, “Programmed cell death

ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer,” Proceedings of the National Academy of Sciences of the United States od America, 104(9), 3360-3365, 2007.2006.

Instituto Nacional del Cáncer. (2019). Tipos de tratamiento. [en línea]. Disponible en: https://www.cancer.gov/espanol/cancer/tratamiento/tipos

Instituto Nacional del Cáncer. (2019). Diccionario de cáncer. [en línea]. Disponible en: https://www.cancer.gov/espanol/publicaciones/diccionario/def/inmunoterapia

D. L. Stanculeanu, Z. Daniela, A. Lazescu, R. Bunghez, and R. Anghel, “Development of new immunotherapy treatments in different cancer types,” Journal of Medicine and Life, 9(3), 240-248, 2016.

S. Arshad, D. Baleanu, J. Huang, Y. Tang, and M. M. Al Qurashi. “Dynamical analysis of fractional order model of immunogenic tumors,” Advances in Mechanical Engineering, 8(7), 1-13, 2016.

O. Fuge, N. Vasdev, P. Allchorne P, and J. Green, “Immunotherapy for bladder cancer,” Research and Reports in Urology, 7, 65-79, 2015.

National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, “Eliminación de la TB, Vacuna BCG,” Center for Disease Control and Prevention, Georgia, 2011.

N. González Sánchez, Z. Armada Esmores, L. Llópiz Casanova. “Propiedades de los interferones y su acción antitumoral,” Medicentro Electrónica, 21(3), 192-198, 2017.

A. A. Tarhini, H. Gogas, and J. M. Kirkwood, “IFN-α in the Treatment of Melanoma,” The Journal of Immunology, 189(8), 3789-3793, 2012.

T. Jiang, C. Zhou, and S. Ren, “Role of IL-2 in cancer immunotherapy,” Oncoimmunology, 5(6), e1163462, 2016.

D. A. Mata-Espinosa y R. Hernández-Pando, “Interferón gamma: aspectos básicos, importancia clínica y usos terapéuticos,” Revista de Investigación Clínica, 60(5), 421-431, 2008.

J. M. Fragoso, G. Vargas Alarcón, S. Jiménez Morales, O. D. Reyes Hernández y J. Ramírez Bello, “El factor de necrosis tumoral α (TNF-α) en las enfermedades autoinmunes (EA): biología molecular y genética,” Gaceta Médica de México, 150(4), 334-344, 2014.

V. H. Bermúdez-Morales, O. Peralta-Zaragoza y V Madrid-Marina, “Terapia génica con citocinas contra cáncer cervicouterino,” Salud Pública de México, 47(6), 458-468, 2005.

T. Chinen, A. K. Kannan, A. G. Levine, X. Fan, U. Klein, Y. Zheng et al, “An essential role for the IL-2 receptor in Treg cell function,” Nature Immunology, 17(11), 1322-1333, 2016.

Chemocare. IL-2 (2019). Chemocare. [en línea]. Disponible en: http://chemocare.com/es/chemotherapy/drug-info/IL-2.aspx

F. Ferriols Lisart, R. Ferriols Lisart y J. Colomina Rodríguez, “Inmunoterapia Tumoral. Vacunas y Terapia Génica,” Farmacia Hospitalaria, 21(3), 166-170, 1997.

M. J. de Prado Hidalgo y A. Llanos Méndez. Seguridad y eficacia de los virus oncolíticos en el cáncer avanzado, Agencia de Evaluación de Tecnologías Sanitarias de Andalucía, Sevilla, Informes de Evaluación de Tecnologías Sanitarias, AETSA 2011 / 2-3, 2012.

L. Lerma, “Virus oncolíticos: un nuevo aliado en la lucha contra el cáncer,” Sociedad Española de Bioquímica y Biología Molecular, 2019.

G. Köhler, “Derivation and Diversification of Monoclonal Antibodies,” Physiology or Medicine, 228-243, 1984.

I. Dávila González, “Generalidades del tratamiento con anticuerpos monoclonales,” Monografías de Archivos de Bronconeumología, 4(1), 2017.

G. Falero, B. L. Rodríguez, I. Rodríguez, E. Suzarte, O. Otero, N. Núñez et al, “Generación de hibridomas productores de anticuerpos monoclonales contra la proteína de membrana externa U (OmpU) de Vibrio cholerae,” Revista CENIC Ciencias Biológicas, 38(3), 224-227, 2006.

S. Escrivá-de-Romaní, M. Arumí, M. Bellet, and C. Saura, “HER2-positive breast cancer: Current and new therapeutic strategies,” The Breast, 39, 80-88, 2018.

T. Vu, F. X. Claret, “Trastuzumab: Updated Mechanisms of Action and Resistance in Breast Cancer,” Frontiers

in Oncology, 2:62, 2012.

R. Muthuswamy, L. Wang, J. Pitteroff, J. R. Gingrich, and P. Kalinski. Combination of IFNα and poly-I:C reprograms bladder cancer microenvironment for enhanced CTL attraction. Journal for ImmunoTherapy of Cancer, 3(6), 2015.

Cancer.net. Qué es la inmunoterapia. (2019, Enero). American Society of Clinical Oncology. [en línea]. Disponible en: https://www.cancer.net/es/desplazarse-por-atenci%C3%B3n-del-c%C3%A1ncer/c%C3%B3mo-se-trata-el-c%C3%A1ncer/inmunoterapia/qu%C3%A9-es-la-inmunoterapia

Instituto Nacional del Cáncer. La terapia con células T y CAR ha sido aprobada para algunos niños y adultos jóvenes con leucemia. (2017, Octubre 19). Instituto Nacional del Cáncer. en línea]. Disponible en: https://www. cancer.gov/espanol/noticias/temas-y-relatos-blog/2017/tisagenlecleucel-fda-leucemia-infantil

M. Gato, T. Liechtenstein, I. Blanco-Luquín, M. I. Zudaire, G. Kochan y D. Escors. “Inmunoterapia genética con

células dendríticas para el tratamiento del cáncer,” Anales del Sistema Sanitario de Navarra, 38(2), 279-288, 2015.

V. K. Kannaujiya, D. Kumar, J. Pathak, and R. P. Sinha, “Phycobiliproteins and Their Commercial Significance,”Cyanobacteria: From Basic Science to Applications, A. K. Mishra, D. N. Tiwari, and A. N. Rai, Ed. Londres: Academic Press, 2019.

X. J. Wu, H. Yang, Y. T. Chen, and P. P. Li, “Biosynthesis of Fluorescent β Subunits of C-Phycocyanin from Spirulina subsalsa in Escherichia coli, and Their Antioxidant Properties,” Molecules, 23(6), 1369, 2018.

E. Manirafasha, T. Ndikubwimana, X. Zeng, Y. Lu, and K. Jing. Phycobiliprotein: Potential microalgae derived

pharmaceutical and biological reagent. Biochemical Engineering Journal, 109, 282-296, 2016.

B. Fernández-Rojas, J. Hernández-Juárez, and J. Pedraza-Chaverri, “Nutraceutical properties of phycocyan- in,” Journal of Functional Foods, 11, 375-392, 2014.

X. Q. Wang, L. N. Li, W. R. Chang, J. P. Zhang, L. L. Gui, B. J. Guo et al, “Structure of C-phycocyanin from Spirulina platensis at 2.2 Å resolution: a novel monoclinic crystal form for phycobiliproteins in phycobilisomes,” Acta Crystallographica Section D Biological crystallography, 57(Pt 6), 784–792, 2001

N. T. Eriksen, “Production of phycocyanin — a pigment with applications in biology, biotechnology, foods and medicine,” Applied Microbiology Biotechnology, 80(1), 1-14, 2008.

M. Kuddus, P. Singh, G. Thomas, and A. Al-Hazimi, “Recent Developments in Production and Biotechnological Applications of C-Phycocyanin,” BioMed Research International, 2013, 742859, 2013.

C. Nemoto-Kawamura, T. Hirahashi, T. Nagai, H. Yamada, T. Katoh, and O. Hayashi, “Phycocyanin enhances secretary IgA antibody response and suppresses allergic IgE antibody response in mice immunized with antigen-entrapped biodegradable microparticles,” Journal of Nutritional Science and Vitaminology, 50(2), 129- 136, 2004.

Q. Liu, Y. Huang, R. Zhang, T. Cai y Y. Cai, “Medical Application of Spirulina platensis Derived C-Phycocianin,”Evidence-Based Complementary and Alternative Medicine, 2016, 7803846, 2016.

G. Díaz Domínguez, V. Marsán Suárez y L. O. del Valle Pérez, “Principales propiedades inmunomodulado- ras y antinflamatorias de la ficobiliproteína C-ficocianina,” Revista Cubana de Hematología, Inmunología y Hemoterapia, 32(4), 447-454, 2016.

Ch. Romay, R. Gonzalez, N. Ledon, D. Remirez, and V. Rimbau, “C-Phycocyanin: A Biliprotein with Antioxidant, Anti-Inflammatory and Neuroprotective Effects,” Current Protein and Peptide Science, 4(3), 207-216, 2003.

S. Agarwal, G. V. Reddy, and P. Reddanna, “Eicosanoids in inflammation and cancer: the role of COX-2,” Expert Review of Clinical Immunology, 5(2), 145-165, 2009.

G. Ding, F. Liu, C. Feng, J. Xu, and Q. Ding, “Asociación entre los polimorfismos de genes de mieloperoxidasa y la susceptibilidad a cáncer de próstata: un estudio caso-control en la población de nacionalidad china,” Actas Urológicas Españolas, 37(2), 79-82, 2013.

A. Soni, M. Dubey, M. Verma, R. Dhankhar, V. Kaushal, R. et al, “Revisiting the Role of Phycocyanin in Current Clinical Practice,” International Journal of Pharmaceutical Sciences and Research, 6(11), 4588-4600, 2015.

R. Raja and S. Hemaiswarya, “Microalgae and Immune Potential” Dietary Components and Immune Function, R. Watson, S. Zibadi, and V. Preedy, Ed. Nueva Jersey: Humana Press, 2010.

H. W. Chen, T. S. Yang, M. J. Chen, Y. C. Chang, I. Eugene, C. Wang et al, “Purification and immunomodulating activity of C-phycocyanin from Spirulina platensis cultured using power plant flue gas, Process Biochemistry, 49(8), 1337-1344, 2014.

L. Jiang, Y. Wang, Q. Yin, G. Liu, H. Liu, Y. Huang et al, Phycocyanin: A Potential Drug for Cancer Treatment, Journal of Cancer, 8(17), 3416-3429, 2017.

H. Wang, Y. Liu, X. Gao, C. L. Carter, and Z. R. Liu, “The recombinant β subunit of C-phycocyanin inhibits cell proliferation and induces apoptosis,” Cancer letters, 247(1), 150-158, 2007.

S. Viñas Domínguez, “Enfermedades de tubulinas,” tesis, Universidad de Cantabria, Cantabria, España, 2016.

A. Iddar, F. Valverde, O. Assobhei, A. Serrano, A. Soukri, “Widespread occurrence of non-phosphorylating glyceraldehyde-3-phosphate dehydrogenase among gram-positive bacteria,” International Microbiology, 8(4), 252-258, 2005.

M. M. Esparza-Jiménez Morán, “Calpaínas,” Revista Médica MD, 1(2).

O. Díaz Horta, “El ion calcio: su regulación y función en la célula ß pancreática,” Revista Cubana de Endocrinología, 14(3), 2003. [Internet]. 2003 [citado 2019 Jun 22]; 14(3).

M. K. Saini and S. N. Sanyal, “Piroxicam and c-phycocyanin prevent colon carcinogenesis by inhibition of membrane fluidity and canonical Wnt/β-catenin signaling while up-regulating ligand dependent transcription factor PPARγ,” Biomedicine & Pharmacotherapy, 68(5), 537-550. 2014;68(5):537-50.

M. K. Saini and S. N. Sanyal, “Targeting angiogenic pathway for chemoprevention of experimental colon cancer using C-phycocyanin as cyclooxygenase-2 inhibitor,” Biochemistry and Cell Biology, 92(3), 206-218, 2014.

E. Fernandes e Silva, F. S. Figueira, A. D. Cañedo, K. S. Machado, M. T. S. F. Salgado, T. K. Silva et al, “C-phycocyanin to overcome the multidrug resistance phenotype in human erythroleukemias with or without interaction with ABC transporters,” Biomedicine & Pharmacotherapy, 106, 532-542, 2018.

G. Pentón-Rol, J. Marín-Prida, and Falcón-Cama, “C-Phycocyanin and Phycocyanobilin as Remyelination Therapies for Enhancing Recovery in Multiple Sclerosis and Ischemic Stroke: A Preclinical Perspective,” Behavioral Sciences, 8(1), 15, 2018.

N. B. Gdara, A. Belgacem, I. Khemiri, S. Mannai, and L. Bitri, “Protective effects of phycocyanin on ischemia/reperfusion liver injuries,” Biomedicine & Pharmacotherapy, 102, 196-202, 2018.

M. Ichimura, S. Kato, K. Tsuneyama, S. Matsutake, M. Kamogawa, E. Hirao et al, “Phycocyanin prevents hyper- ¿tension and low serum adiponectin level in a rat model of metabolic syndrome,” Nutrition Research, 33(5), 397-405, 2013.

X. Li, L. Ma, W. Zheng, and T. Chen, “Inhibition of islet amyloid polypeptide fibril formation by selenium-contai- ning phycocyanin and prevention of beta cell apoptosis,” Biomaterials, 35(30), 8596-8604, 2014.

R. J. Fayyad, A. N. M. Ali, A. S. Dwaish, A. K. A. Al-Abboodi, “Anticancer Activity of Spirulina platensis Methanolic Extracts Against L20B and MCF7 Human Cancer Cell Lines, Plant Archives, 19(Suppl 1), 1419- 1426, 2019.

Most read articles by the same author(s)