Skip to main content Accessibility help
×
×
Home

Virgin olive oil and its phenol fraction modulate monocyte/macrophage functionality: a potential therapeutic strategy in the treatment of systemic lupus erythematosus

  • Marina Aparicio-Soto (a1), Sergio Montserrat-de la Paz (a2) (a3), Marina Sanchez-Hidalgo (a1), Ana Cardeno (a1), Beatriz Bermudez (a1) (a4), Francisco J. G. Muriana (a2) and Catalina Alarcon-de-la-Lastra (a1)...
Abstract

Monocytes and macrophages are critical effectors and regulators of inflammation and innate immune response, which appear altered in different autoimmune diseases such as systemic lupus erythematosus (SLE). Recent studies suggested that virgin olive oil (VOO) and particularly its phenol compounds might possess preventive effects on different immune-inflammatory diseases, including SLE. Here, we evaluated the effects of VOO (and sunflower oil) on lipopolysaccharide (LPS)-activated peritoneal macrophages from a model of pristane-induced SLE in BALB/c mice, as well as those of the phenol fraction (PF) from VOO on the immune-inflammatory activity and plasticity in monocytes and monocyte-derived macrophages from healthy volunteers. The release of nitrite and inflammatory cytokines was lower in LPS-treated peritoneal macrophages from pristane-SLE mice fed the VOO diet when compared with the sunflower oil diet. PF from VOO similarly decreased the secretion of nitrite and inflammatory cytokines and expression of inducible nitric oxide, PPARγ and Toll-like receptor 4 in LPS-treated human monocytes. PF from VOO also prevented the deregulation of human monocyte subset distribution by LPS and blocked the genetic signature of M1 macrophages while favouring the phenotype of M2 macrophages upon canonical polarisation of naïve human macrophages. For the first time, our study provides several lines of in vivo and in vitro evidence that VOO and PF from VOO target and counteract inflammatory pathways in the monocyte–macrophage lineage of mice with pristane-induced SLE and of healthy subjects, which is a meaningful foundation for further development and application in preclinical and clinical use of PF from VOO in patients with SLE.

Copyright
Corresponding author
*Corresponding author: Professor Dr C. Alarcon-de-la-Lastra, fax +34 954 55 6074, email calarcon@us.es
References
Hide All
1. Helmick, CG, Felson, DT, Lawrence, RC, et al. (2008) Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I. Arthritis Rheum 58, 1525.
2. Peng, SL (2009) Altered T and B lymphocyte signaling pathways in lupus. Autoimmun Rev 8, 179183.
3. Geissmann, F, Manz, MG, Jung, S, et al. (2010) Development of monocytes, macrophages, and dendritic cells. Science 327, 656661.
4. Tugal, D, Liao, X & Jain, MK (2013) Transcriptional control of macrophage polarization. Arterioscler Thromb Vasc Biol 33, 11351144.
5. Kavai, M & Szegedi, G (2007) Immune complex clearance by monocytes and macrophages in systemic lupus erythematosus. Autoimmun Rev 6, 497502.
6. Rönnblom, L, Eloranta, ML & Alm, GV (2006) The type I interferon system in systemic lupus erythematosus. Arthritis Rheum 54, 408420.
7. Sestak, AL, Fürnrohr, BG, Harley, JB, et al. (2011) The genetics of systemic lupus erythematosus and implications for targeted therapy. Ann Rheum Dis 70, Suppl. 1, i37i43.
8. Satoh, M & Reeves, WH (1994) Induction of lupus-associated autoantibodies in BALB/c mice by intraperitoneal injection of pristane. J Exp Med 180, 23412346.
9. Satoh, M, Yamagata, H, Watanabe, F, et al. (1995) Development of anti-Sm and anti-DNA antibodies followed by clinical manifestation of systemic lupus erythematosus in an elderly woman with long-standing Sjögren's syndrome. Lupus 4, 6365.
10. Shaheen, VM, Satoh, M, Richards, HB, et al. (1999) Immunopathogenesis of environmentally induced lupus in mice. Environ Health Perspect 107, Suppl. 5, 723727.
11. De Rosa, V, Galgani, M, Santopaolo, M, et al. (2015) Nutritional control of immunity: balancing the metabolic requirements with an appropriate immune function. Semin Immunol 27, 300309.
12. Aparicio-Soto, M, Sanchez-Hidalgo, M & Alarcon-de-la-Lastra, C (2017) An update on diet and nutritional factors in systemic lupus erythematosus management. Nutr Res Rev 30, 118137.
13. Buckland, G, Mayen, AL, Agudo, A, et al. (2012) Olive oil intake and mortality within the Spanish population (EPIC-Spain). Am J Clin Nutr 96, 142149.
14. Alarcon de la Lastra, C, Barranco, MD, Motilva, V, et al. (2001) Mediterranean diet and health: biological importance of olive oil. Curr Pharm Des 7, 933950.
15. Cardeno, A, Sanchez-Hidalgo, M & Alarcon-de-la-Lastra, C (2013) An up-date of olive oil phenols in inflammation and cancer: molecular mechanisms and clinical implications. Curr Med Chem 20, 47584776.
16. Cardeno, A, Sanchez-Hidalgo, M, Aparicio-Soto, M, et al. (2014) Extra virgin olive oil polyphenolic extracts downregulate inflammatory responses in LPS-activated murine peritoneal macrophages suppressing NF kappa B and MAPK signalling pathways. Food Funct 5, 12701277.
17. Sanchez-Fidalgo, S, Cardeno, A, Sanchez-Hidalgo, M, et al. (2013) Dietary extra virgin olive oil polyphenols supplementation modulates DSS-induced chronic colitis in mice. J Nutr Biochem 24, 14011413.
18. Aparicio-Soto, M, Sanchez-Hidalgo, M, Cardeno, A, et al. (2016) Dietary extra virgin olive oil attenuates kidney injury in pristane-induced SLE model via activation of HO-1/Nrf-2 antioxidant pathway and suppression of JAK/STAT, NF-κB and MAPK activation. J Nutr Biochem 27, 278288.
19. Rosillo, MA, Sanchez-Hidalgo, M, Sanchez-Fidalgo, S, et al. (2016) Dietary extra-virgin olive oil prevents inflammatory response and cartilage matrix degradation in murine collagen-induced arthritis. Eur J Nutr 5, 315325.
20. Sanchez-Fidalgo, S, Villegas, I, Cardeno, A, et al. (2010) Extra-virgin olive oil-enriched diet modulates DSS-colitis-associated colon carcinogenesis in mice. Clin Nutr 29, 663673.
21. Aparicio-Soto, M, Sanchez-Hidalgo, M, Cardeno, A, et al. (2017) The phenolic fraction of extra virgin olive oil modulates the activation and the inflammatory response of T cells from patients with systemic lupus erythematosus and healthy donors. Mol Nutr Food Res 61, 18.
22. Aparicio-Soto, M, Alarcon-de-la-Lastra, C, Cardeno, A, et al. (2014) Melatonin modulates microsomal PGE synthase 1 and NF-E2-related factor-2-regulated antioxidant enzyme expression in LPS-induced murine peritoneal macrophages. Br J Pharmacol 171, 134144.
23. Kilkenny, C, Browne, WJ, Cuthill, IC, et al. (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. J Pharmacol Pharmacother 1, 9499.
24. McGrath, JC, Drummond, GB, McLachlan, EM, et al. (2010) Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160, 15731576.
25. Moorcroft, MJ, Davis, J & Compton, RG (2001) Detection and determination of nitrate and nitrite: a review. Talanta 54, 785803.
26. Vazquez Roncero, A, Janet del Valle, M & Janet del Valle, L (1976) Componentes fenolicos de la aceituna. III, Polifenoles del aceite (Phenolic compounds from olives. III, Oil polyphenols). Grasas aceites (B Aires) 27, 185191.
27. Denizot, F & Lang, R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods 89, 271277.
28. Sanchez-Hidalgo, M, Martin, AR, Villegas, I, et al. (2005) Rosiglitazone, an agonist of peroxisome proliferator-activated receptor gamma, reduces chronic colonic inflammation in rats. Biochem Pharmacol 69, 17331744.
29. Bradford, MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248254.
30. Feng, GJ, Goodridge, HS, Harnett, MM, et al. (1999) Extracellular signal-related kinase (ERK) and p38 mitogen-activated protein (MAP) kinases differentially regulate the lipopolysaccharide-mediated induction of inducible nitric oxide synthase and IL-12 in macrophages: Leishmania phosphoglycans subvert macrophage IL-12 production by targeting ERK MAP kinase. J Immunol 163, 64036412.
31. Chow, JC, Young, DW, Golenbock, DT, et al. (1999) Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J Biol Chem 274, 1068910692.
32. Cole, JE, Georgiou, E & Monaco, C (2010) The expression and functions of Toll-like receptors in atherosclerosis. Mediators Inflamm 2010, 393946.
33. Ziegler-Heitbrock, L (2014) Monocyte subsets in man and other species. Cell Immunol 289, 135139.
34. Li, Y, Lee, PY & Reeves, WH (2010) Monocyte and macrophage abnormalities in systemic lupus erythematosus. Arch Immunol Ther Exp (Warsz) 58, 355364.
35. Unanue, ER (1978) The regulation of lymphocyte functions by the macrophage. Immunol Rev 40, 227255.
36. Katsiari, CG, Liossis, SN & Sfikakis, PP (2010) The pathophysiologic role of monocytes and macrophages in systemic lupus erythematosus: a reappraisal. Semin Arthritis Rheum 39, 491503.
37. van Vollenhoven, RF, Parodis, I & Levitsky, A (2013) Biologics in SLE: towards new approaches. Best Pract Res Clin Rheumatol 27, 341349.
38. Sukkar, SG & Rossi, E (2004) Oxidative stress and nutritional prevention in autoimmune rheumatic diseases. Autoimmun Rev 3, 199206.
39. Oates, JC & Gilkeson, GS (2006) The biology of nitric oxide and other reactive intermediates in systemic lupus erythematosus. Clin Immunol 121, 243250.
40. Rosillo, MA, Alcaraz, MJ, Sanchez-Hidalgo, M, et al. (2014) Anti-inflammatory and joint protective effects of extra-virgin olive-oil polyphenol extract in experimental arthritis. J Nutr Biochem 25, 12751281.
41. Chen, L, Yang, S, Zumbrun, EE, et al. (2015) Resveratrol attenuates lipopolysaccharide-induced acute kidney injury by suppressing inflammation driven by macrophages. Mol Nutr Food Res 59, 853864.
42. Venegas-Pont, M, Sartori-Valinotti, JC, Maric, C, et al. (2009) Rosiglitazone decreases blood pressure and renal injury in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol 296, R1282R1289.
43. Chinetti, G, Fruchart, JC & Staels, B (2000) Peroxisome proliferator-activated receptors (PPARs): nuclear receptors at the crossroads between lipid metabolism and inflammation. Inflamm Res 49, 497505.
44. Martin, H (2009) Role of PPAR-gamma in inflammation. Prospects for therapeutic intervention by food components. Mutat Res 669, 17.
45. Perez-Jimenez, F, Alvarez de Cienfuegos, G, Badimon, L, et al. (2005) International conference on the healthy effect of virgin olive oil. Eur J Clin Invest 35, 421424.
46. Burbano, C, Vasquez, G & Rojas, M (2014) Modulatory effects of CD14+CD16++ monocytes on CD14++CD16monocytes: a possible explanation of monocyte alterations in systemic lupus erythematosus. Arthritis Rheumatol 66, 33713381.
47. Moser, KL, Kelly, JA, Lessard, CJ, et al. (2009) Recent insights into the genetic basis of systemic lupus erythematosus. Genes Immun 10, 373379.
48. Yang, J, Zhang, L, Yu, C, et al. (2014) Monocyte and macrophage differentiation: circulation inflammatory monocyte as biomarker for inflammatory diseases. Biomark Res 2, 1.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

British Journal of Nutrition
  • ISSN: 0007-1145
  • EISSN: 1475-2662
  • URL: /core/journals/british-journal-of-nutrition
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
WORD
Supplementary materials

Aparicio-Soto et al. supplementary material
Aparicio-Soto et al. supplementary material 1

 Word (79 KB)
79 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed