Table of Contents Author Guidelines Submit a Manuscript
Oxidative Medicine and Cellular Longevity
Volume 2017 (2017), Article ID 6293740, 11 pages
https://doi.org/10.1155/2017/6293740
Research Article

Effect of Cocoa Polyphenolic Extract on Macrophage Polarization from Proinflammatory M1 to Anti-Inflammatory M2 State

1Department of Medicine, Campus Bio-Medico University of Rome, Via A. del Portillo 21, 00128 Roma, Italy
2Department of Biomedical, Dental Sciences and Morphological and Functional Images, University of Messina, Via Consolare Valeria, 98125 Messina, Italy
3European Center for Brain Research, Santa Lucia Foundation IRCCS, Rome, Italy
4Department of Basic Medical Sciences, Neurosciences and Sense Organs, University of Bari “Aldo Moro”, P.zza G. Cesare, 11, 70124 Bari, Italy

Correspondence should be addressed to Anna Maria Sardanelli; ti.abinu@illenadras.airamanna

Received 23 September 2016; Revised 22 November 2016; Accepted 20 April 2017; Published 28 June 2017

Academic Editor: Chung-Yen Oliver Chen

Copyright © 2017 Laura Dugo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. B. Bottazzi, A. Doni, C. Garlanda, and A. Mantovani, “An integrated view of humoral innate immunity: pentraxins as a paradigm,” Annual Review of Immunology, vol. 28, pp. 157–183, 2010. View at Google Scholar
  2. P. J. Murray and T. A. Wynn, “Protective and pathogenic functions of macrophage subsets,” Nature Reviews Immunology, vol. 11, no. 11, pp. 723–737, 2011. View at Google Scholar
  3. N. Kamada, T. Hisamatsu, S. Okamoto et al., “Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFN-gamma axis,” Journal of Clinical Investigation, vol. 118, no. 6, pp. 2269–2280, 2008. View at Google Scholar
  4. G. K. Hansson and A. Hermansson, “The immune system in atherosclerosis,” Nature Reviews Immunology, vol. 12, no. 3, pp. 204–212, 2011. View at Google Scholar
  5. S. Gordon, “Alternative activation of macrophages,” Nature Reviews Immunology, vol. 3, no. 1, pp. 23–35, 2003. View at Google Scholar
  6. A. Sica and A. Mantovani, “Macrophage plasticity and polarization: in vivo veritas,” Journal of Clinical Investigation, vol. 122, no. 3, pp. 787–795, 2012. View at Google Scholar
  7. F. O. Martinez, L. Helming, and S. Gordon, “Alternative activation of macrophages: an immunologic functional perspective,” Annual Review of Immunology, vol. 27, pp. 451–483, 2009. View at Google Scholar
  8. S. Gordon and P. R. Taylor, “Monocyte and macrophage heterogeneity,” Nature Reviews Immunology, vol. 5, no. 12, pp. 953–964, 2005. View at Google Scholar
  9. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica, “Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes,” Trends in Immunology, vol. 23, no. 11, pp. 549–555, 2002. View at Google Scholar
  10. T. Lawrence and G. Natoli, “Transcriptional regulation of macrophage polarization: enabling diversity with identity,” Nature Reviews Immunology, vol. 11, no. 11, pp. 750–761, 2011. View at Google Scholar
  11. N. Wang, H. Liang, and K. Zen, “Molecular mechanisms that influence the macrophage M1–M2 polarization balance,” Frontiers in Immunology, vol. 5, no. 614, pp. 1–9, 2014. View at Google Scholar
  12. T. Rőszer, “Understanding the mysterious M2 macrophage through activation markers and effector mechanisms,” Mediators of Inflammation, vol. 2015, Article ID 816460, 16 pages, 2015. View at Google Scholar
  13. P. J. Murray, J. E. Allen, S. K. Biswas et al., “Macrophage activation and polarization: nomenclature and experimental guidelines,” Immunity, vol. 41, no. 1, pp. 14–20, 2014. View at Google Scholar
  14. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Google Scholar
  15. A. Sica and V. Bronte, “Altered macrophage differentiation and immune dysfunction in tumor development,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1155–1166, 2007. View at Google Scholar
  16. C. He and A. B. Carter, “The metabolic prospective and redox regulation of macrophage polarization,” Journal of Clinical & Cellular Immunology, vol. 6, no. 6, 2015. View at Google Scholar
  17. D. Duluc, M. Corvaisier, S. Blanchard et al., “Interferon-gamma reverses the immunosuppressive and protumoral properties and prevents the generation of human tumor-associated macrophages,” International Journal of Cancer, vol. 125, no. 2, pp. 367–373, 2009. View at Google Scholar
  18. T. Hagemann, T. Lawrence, I. McNeish et al., ““re-educating” tumor-associated macrophages by targeting NF-kappaB,” The Journal of Experimental Medicine, vol. 205, no. 6, pp. 1261–1268, 2008. View at Google Scholar
  19. A. Saccani, T. Schioppa, C. Porta et al., “p50 nuclear factor-kappaB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance,” Cancer Research, vol. 66, no. 23, pp. 11432–11440, 2006. View at Google Scholar
  20. S. Aharoni, Y. Lati, M. Aviram, and B. Fuhrman, “Pomegranate juice polyphenols induce a phenotypic switch in macrophage polarization favoring a M2 anti-inflammatory state,” BioFactors, vol. 41, no. 1, pp. 44–51, 2015. View at Google Scholar
  21. C. Fanali, L. Dugo, G. Tripodo, and L. Santi, “Cocoa polyphenols: chemistry, bioavailability and effects on cardiovascular performance,” Current Medicinal Chemistry, vol. 23, 2016. View at Google Scholar
  22. S. J. Crozier, A. G. Preston, J. W. Hurst et al., “Cacao seeds are a “super fruit”: a comparative analysis of various fruit powders and products,” Chemistry Central Journal, vol. 5, p. 5, 2011. View at Google Scholar
  23. A. Othman, A. Ismail, N. Abdul Ghani, and I. Adenan, “Antioxidant capacity and phenolic content of cocoa beans,” Food Chemistry, vol. 100, no. 4, pp. 1523–1530, 2007. View at Google Scholar
  24. C. Pantano, N. L. Reynaert, A. van der Vliet, and Y. M. Janssen-Heininger, “Redox-sensitive kinases of the nuclear factor-kappaB signaling pathway,” Antioxidand and Redox Signal, vol. 8, no. 9-10, pp. 1791–1806, 2006. View at Google Scholar
  25. E. Ramiro, A. Franch, C. Castellote, C. Andrés-Lacueva, M. Izquierdo-Pulido, and M. Castell, “Effect of Theobroma cacao flavonoids on immune activation of a lymphoid cell line,” British Journal of Nutrition, vol. 93, no. 6, pp. 859–866, 2005. View at Google Scholar
  26. R. di Giuseppe, A. Di Castelnuovo, F. Centritto et al., “Regular consumption of dark chocolate is associated with low serum concentrations of C-reactive protein in a healthy Italian population,” The Journal of Nutrition, vol. 138, no. 10, pp. 1939–1945, 2008. View at Google Scholar
  27. M. Monagas, N. Khan, C. Andres-Lacueva et al., “Effect of cocoa powder on the modulation of inflammatory biomarkers in patients at high risk of cardiovascular disease,” The American Journal of Clinical Nutrition, vol. 90, no. 5, pp. 1144–1150, 2009. View at Google Scholar
  28. B. Buijsse, E. J. Feskens, F. J. Kok, and D. Kromhout, “Cocoa intake, blood pressure, and cardiovascular mortality: the Zutphen Elderly Study,” Archives of Internal Medicine, vol. 166, no. 4, pp. 411–417, 2006. View at Google Scholar
  29. R. Corti, A. J. Flammer, N. K. Hollenberg, and T. F. Lüscher, “Cocoa and cardiovascular health,” Circulation, vol. 119, no. 10, pp. 1433–1441, 2009. View at Google Scholar
  30. K. Davison and P. R. C. Howe, “Potential implications of dose and diet for the effects of cocoa flavanols on cardiometabolic function,” Journal of Agricultural and Food Chemistry, vol. 63, no. 45, pp. 9942–9947, 2015. View at Google Scholar
  31. L. Goya, M. Martín, B. Sarriá, S. Ramos, R. Mateos, and L. Bravo, “Effect of cocoa and its flavonoids on biomarkers of inflammation: studies of cell culture, animals and humans,” Nutrients, vol. 8, no. 4, p. 212, 2016. View at Google Scholar
  32. T. Perez-Berezo, A. Franch, C. Castellote, M. Castell, and F. J. Pérez-Cano, “Mechanisms involved in down-regulation of intestinal IgA in rats by high cocoa intake,” The Journal of Nutritional Biochemistry, vol. 23, no. 7, pp. 838–844, 2012. View at Google Scholar
  33. S. Ramos-Romero, F. J. Perez-Cano, E. Ramiro-Puig, A. Franch, and M. Castell, “Cocoa intake attenuates oxidative stress associated with rat adjuvant arthritis,” Pharmacological Research, vol. 66, no. 3, pp. 207–212, 2012. View at Google Scholar
  34. M. Massot-Cladera, A. Franch, F. J. Perez-Cano, and M. Castell, “Cocoa and cocoa fibre differentially modulate IgA and IgM production at mucosal sites,” British Journal of Nutrition, vol. 115, no. 9, pp. 1539–1546, 2016. View at Google Scholar
  35. M. Comalada, D. Camuesco, S. Sierra et al., “In vivo quercitrin anti-inflammatory effect involves release of quercetin, which inhibits inflammation through down-regulation of the NF-kappaB pathway,” European Journal of Immunology, vol. 35, no. 2, pp. 584–592, 2005. View at Google Scholar
  36. Y. C. Park, G. Rimbach, C. Saliou, G. Valacchi, and L. Packer, “Activity of monomeric, dimeric, and trimeric flavonoids on NO production, TNF-alpha secretion, and NF-kappaB-dependent gene expression in RAW 264.7 macrophages,” FEBS Letters, vol. 465, no. 2-3, pp. 93–97, 2000. View at Google Scholar
  37. N. J. Kang, K. W. Lee, D. E. Lee et al., “Cocoa procyanidins suppress transformation by inhibiting mitogen-activated protein kinase kinase,” The Journal of Biological Chemistry, vol. 283, no. 30, pp. 20664–20673, 2008. View at Google Scholar
  38. G. Muthian and J. J. Bright, “Quercetin, a flavonoid phytoestrogen, ameliorates experimental allergic encephalomyelitis by blocking IL-12 signaling through JAK-STAT pathway in T lymphocyte,” Journal of Clinical Immunology, vol. 24, no. 5, pp. 542–552, 2004. View at Google Scholar
  39. V. L. Singleton, R. Orthofer, and R. M. Lamuela-Raventós, “Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent,” Methods in Enzymology, vol. 299, pp. 152–178, 1999, Academic Press. View at Google Scholar
  40. C. Fanali, M. G. Belluomo, M. Cirilli et al., “Antioxidant activity evaluation and HPLC-photodiode array/MS polyphenols analysis of pomegranate juice from selected Italian cultivars: a comparative study,” Electrophoresis, vol. 37, no. 13, pp. 1947–1955, 2016. View at Google Scholar
  41. G. Lopez-Castejon, A. Baroja-Mazo, and P. Pelegrin, “Novel macrophage polarization model: from gene expression to identification of new anti-inflammatory molecules,” Cellular and Molecular Life Sciences, vol. 68, no. 18, pp. 3095–3107, 2011. View at Google Scholar
  42. C. Piccoli, A. Sardanelli, R. Scrima et al., “Mitochondrial respiratory dysfunction in familiar parkinsonism associated with PINK1 mutation,” Neurochemical Research, vol. 33, no. 12, pp. 2565–2574, 2008. View at Google Scholar
  43. C. Pacelli, D. De Rasmo, A. Signorile et al., “Mitochondrial defect and PGC-1α dysfunction in parkin-associated familial Parkinson’s disease,” Biochimica et Biophysyca Acta- Molecular Basis of Disease, vol. 1812, no. 8, pp. 1041–1053, 2011. View at Google Scholar
  44. A. Carpentieri, E. Cozzoli, M. Scimeca, E. Bonanno, A. M. Sardanelli, and A. Gambacurta, “Differentiation of human neuroblastoma cells toward the osteogenic lineage by mTOR inhibitor,” Cell Death and Disease, vol. 6, article e1974, 2015. View at Google Scholar
  45. F. J. Pérez-Cano and M. Castell, “Flavonoids, inflammation and immune system,” Nutrients, vol. 8, no. 10, 2016. View at Google Scholar
  46. A. Spadafranca, C. Martinez Conesa, S. Sirini, and G. Testolin, “Effect of dark chocolate on plasma epicatechin levels, DNA resistance to oxidative stress and total antioxidant activity in healthy subjects,” British Journal of Nutrition, vol. 103, no. 7, pp. 1008–1014, 2010. View at Google Scholar
  47. M. Urpi-Sarda, M. Monagas, N. Khan et al., “Targeted metabolic profiling of phenolics in urine and plasma after regular consumption of cocoa by liquid chromatography-tandem mass spectrometry,” Journal of Chromatography. A, vol. 1216, no. 43, pp. 7258–7267, 2009. View at Google Scholar
  48. F. A. Tomas-Barberan, E. Cienfuegos-Jovellanos, A. Marín et al., “A new process to develop a cocoa powder with higher flavonoid monomer content and enhanced bioavailability in healthy humans,” Journal of Agricultural and Food Chemistry, vol. 55, no. 10, pp. 3926–3935, 2007. View at Google Scholar
  49. A. Serra, A. Macià, L. Rubió et al., “Distribution of procyanidins and their metabolites in rat plasma and tissues in relation to ingestion of procyanidin-enriched or procyanidin-rich cocoa creams,” European Journal of Clinical Nutrition, vol. 52, no. 3, pp. 1029–1038, 2013. View at Google Scholar
  50. T. Cifuentes-Gomez, A. Rodriguez-Mateos, I. Gonzalez-Salvador, M. E. Alañon, and J. P. Spencer, “Factors affecting the absorption, metabolism, and excretion of cocoa flavanols in humans,” Journal of Agricultural and Food Chemistry, vol. 63, no. 35, pp. 7615–7623, 2015. View at Google Scholar
  51. R. R. Holt, S. A. Lazarus, M. C. Sullards et al., “Procyanidin dimer B2 [epicatechin-(4beta-8)-epicatechin] in human plasma after the consumption of a flavanol-rich cocoa,” The American Journal of Clinical Nutrition, vol. 76, no. 4, pp. 798–804, 2002. View at Google Scholar
  52. M. Urpi-Sarda, E. Ramiro-Puig, N. Khan et al., “Distribution of epicatechin metabolites in lymphoid tissues and testes of young rats with a cocoa-enriched diet,” British Journal of Nutrition, vol. 103, no. 10, pp. 1393–1397, 2010. View at Google Scholar
  53. M. Margalef, Z. Pons, F. I. Bravo, B. Muguerza, and A. Arola-Arnal, “Tissue distribution of rat flavanol metabolites at different doses,” The Journal of Nutritional Biochemistry, vol. 26, no. 10, pp. 987–995, 2015. View at Google Scholar
  54. J.-E. Kim, J. E. Son, S. K. Jung et al., “Cocoa polyphenols suppress TNF-α-induced vascular endothelial growth factor expression by inhibiting phosphoinositide 3-kinase (PI3K) and mitogen-activated protein kinase kinase-1 (MEK1) activities in mouse epidermal cells,” British Journal of Nutrition, vol. 104, no. 7, pp. 957–964, 2010. View at Google Scholar
  55. E. Ramiro, À. Franch, C. Castellote et al., “Flavonoids from Theobroma cacao down-regulate inflammatory mediators,” Journal of Agricultural and Food Chemistry, vol. 53, no. 22, pp. 8506–8511, 2005. View at Google Scholar