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Monocyte chemoattractant protein-1 polymorphism interaction with spirulina immunomodulatory effects in healthy Korean elderly: A 16-week, double-blind randomized clinical trial

  • Park, Hee Jung (Department of Foods and Nutrition, Kookmin University) ;
  • Lee, Hyun Sook (Department of Food Science and Nutrition, Dongseo University)
  • Received : 2017.02.07
  • Accepted : 2017.04.11
  • Published : 2017.08.01

Abstract

BACKGROUND/OBJECTIVES: Spirulina is a known a functional food related to lipid profiles, immune functions, and antioxidant capacity. Circulating monocyte chemoattractant protein-1 (MCP-1) level is associated with inflammation markers. Single nucleotide polymorphism in the MCP-1 promoter region -2518 have been identified and shown to affect gene transcription. Gene variation may also impact functional food supplementary effects. The current study investigated the interaction of MCP-1 -2518 polymorphism with spirulina supplements on anti-inflammatory capacity in Korean elderly. SUBJECTS/METHODS: After genotyping, healthy elderly subjects (n = 78) were included in a randomized, double blind, and placebo controlled study. Baseline characteristic, body composition, and dietary intake were measured twice (baseline vs. week 16). For 16 weeks, subjects consumed 8 g either spirulina or placebo daily. Plasma MCP-1, interleukin (IL) -2, IL-6, tumor necrosis factor (TNF)-${\alpha}$, complement (C) 3, immunoglobulin (Ig) G, and Ig A concentrations and lymphocyte proliferation rate (LPR) were analyzed as inflammatory markers. RESULTS: In the placebo group with A/A genotype, MCP-1 level was significantly increased, but the spirulina group with A/A genotype was unchanged. IL-2 was significantly increased only in subjects with spirulina supplementation. TNF-${\alpha}$ was significantly reduced in subjects with the G carrier. C3 was significantly increased in the placebo group, particularly when A/A increased more than G, but not when spirulina was ingested. LPR was significantly different only in subjects with A/A genotype; there was a significant increase in phytohemagglutinin and lipopolysaccharide induced LPR in the spirulina group. CONCLUSION: In healthy Korean elderly, spirulina supplementation may influence different inflammatory markers by the MCP-1 genotype. These results may be useful for customized dietary guidelines to improve immune function in Koreans.

Keywords

References

  1. Muller WA. Getting leukocytes to the site of inflammation. Vet Pathol 2013;50:7-22. https://doi.org/10.1177/0300985812469883
  2. Xu L, Rocnik E, Rahlpour R, Hunter N, Pickering G, Kelvin DJ. MCP-1 induces proliferation and migration of vascular smooth muscle cells. FASEB J 1996;10:A1932.
  3. Luster AD. Chemokines--chemotactic cytokines that mediate inflammation. N Engl J Med 1998;338:436-45. https://doi.org/10.1056/NEJM199802123380706
  4. Rossi D, Zlotnik A. The biology of chemokines and their receptors. Annu Rev Immunol 2000;18:217-42. https://doi.org/10.1146/annurev.immunol.18.1.217
  5. Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, Oppenheim JJ, Murphy WJ. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood 2000;96:34-40.
  6. Inadera H, Egashira K, Takemoto M, Ouchi Y, Matsushima K. Increase in circulating levels of monocyte chemoattractant protein-1 with aging. J Interferon Cytokine Res 1999;19:1179-82. https://doi.org/10.1089/107999099313127
  7. Rovin BH, Lu L, Saxena R. A novel polymorphism in the MCP-1 gene regulatory region that influences MCP-1 expression. Biochem Biophys Res Commun 1999;259:344-8. https://doi.org/10.1006/bbrc.1999.0796
  8. Martin ES, Schneeberger EE, Aranda FM, Peres SW, Del Carmen Valerio M, de Los Angeles Correa M, Pra FD, Martinez L, Remondino G, de Larranaga G, Citera G. The -2518 A/G polymorphism in the monocyte chemoattractant protein 1 gene (MCP-1) is associated with an increased risk of rheumatoid arthritis in Argentine patients. Clin Rheumatol 2016;35:3057-61. https://doi.org/10.1007/s10067-016-3380-0
  9. Wang W, He M, Huang W. Association of monocyte chemoattractant protein-1 gene 2518A/G polymorphism with diabetic retinopathy in type 2 diabetes mellitus: a meta-analysis. Diabetes Res Clin Pract 2016;120:40-6. https://doi.org/10.1016/j.diabres.2016.07.016
  10. Niu J, Kolattukudy PE. Role of MCP-1 in cardiovascular disease: molecular mechanisms and clinical implications. Clin Sci (Lond) 2009;117:95-109. https://doi.org/10.1042/CS20080581
  11. Mansego ML, De Marco G, Ivorra C, Lopez-Izquierdo R, Morcillo S, Rojo-Martinez G, Gonzalez-Albert V, Martinez F, Soriguer F, Martin-Escudero JC, Redon J, Chaves FJ. The nutrigenetic influence of the interaction between dietary vitamin E and TXN and COMT gene polymorphisms on waist circumference: a case control study. J Transl Med 2015;13:286. https://doi.org/10.1186/s12967-015-0652-4
  12. Pase CS, Teixeira AM, Roversi K, Dias VT, Calabrese F, Molteni R, Franchi S, Panerai AE, Riva MA, Burger ME. Olive oil-enriched diet reduces brain oxidative damages and ameliorates neurotrophic factor gene expression in different life stages of rats. J Nutr Biochem 2015;26:1200-7. https://doi.org/10.1016/j.jnutbio.2015.05.013
  13. Pietropaolo S, Goubran MG, Joffre C, Aubert A, Lemaire-Mayo V, Crusio WE, Laye S. Dietary supplementation of omega-3 fatty acids rescues fragile X phenotypes in Fmr1-Ko mice. Psychoneuroendocrinology 2014;49:119-29. https://doi.org/10.1016/j.psyneuen.2014.07.002
  14. Nigam A, Talajic M, Roy D, Nattel S, Lambert J, Nozza A, Jones P, Ramprasath VR, O'Hara G, Kopecky S, Brophy JM, Tardif JC; AFFORD Investigators. Fish oil for the reduction of atrial fibrillation recurrence, inflammation, and oxidative stress. J Am Coll Cardiol 2014;64: 1441-8. https://doi.org/10.1016/j.jacc.2014.07.956
  15. Yanaka A, Fahey JW, Fukumoto A, Nakayama M, Inoue S, Zhang S, Tauchi M, Suzuki H, Hyodo I, Yamamoto M. Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in Helicobacter pylori-infected mice and humans. Cancer Prev Res (Phila) 2009;2:353-60. https://doi.org/10.1158/1940-6207.CAPR-08-0192
  16. Vicari E, La Vignera S, Castiglione R, Condorelli RA, Vicari LO, Calogero AE. Chronic bacterial prostatitis and irritable bowel syndrome: effectiveness of treatment with rifaximin followed by the probiotic VSL#3. Asian J Androl 2014;16:735-9. https://doi.org/10.4103/1008-682X.131064
  17. Ortega-Azorin C, Sorli JV, Asensio EM, Coltell O, Martinez-Gonzalez MA, Salas-Salvado J, Covas MI, Aros F, Lapetra J, Serra-Majem L, Gomez-Gracia E, Fiol M, Saez-Tormo G, Pinto X, Munoz MA, Ros E, Ordovas JM, Estruch R, Corella D. Associations of the FTO rs9939609 and the MC4R rs17782313 polymorphisms with type 2 diabetes are modulated by diet, being higher when adherence to the Mediterranean diet pattern is low. Cardiovasc Diabetol 2012;11:137. https://doi.org/10.1186/1475-2840-11-137
  18. Serrano JC, De Lorenzo D, Cassanye A, Martin-Gari M, Espinel A, Delgado MA, Pamplona R, Portero-Otin M. Vitamin D receptor BsmI polymorphism modulates soy intake and 25-hydroxyvitamin D supplementation benefits in cardiovascular disease risk factors profile. Genes Nutr 2013;8:561-9. https://doi.org/10.1007/s12263-013-0356-4
  19. Giacconi R, Costarelli L, Malavolta M, Cardelli M, Galeazzi R, Piacenza F, Gasparini N, Basso A, Mariani E, Fulop T, Rink L, Dedoussis G, Herbein G, Jajte J, Provinciali M, Busco F, Mocchegiani E. Effect of ZIP2 Gln/Arg/Leu (rs2234632) polymorphism on zinc homeostasis and inflammatory response following zinc supplementation. Biofactors 2015;41:414-23. https://doi.org/10.1002/biof.1247
  20. Park S, Zhang X, Lee NR, Jin HS. TRPV1 gene polymorphisms are associated with type 2 diabetes by their interaction with fat consumption in the Korean genome epidemiology study. J Nutrigenet Nutrigenomics 2016;9:47-61. https://doi.org/10.1159/000446499
  21. Thengodkar RR, Sivakami S. Degradation of Chlorpyrifos by an alkaline phosphatase from the cyanobacterium Spirulina platensis. Biodegradation 2010;21:637-44. https://doi.org/10.1007/s10532-010-9331-6
  22. Lee JB, Srisomporn P, Hayashi K, Tanaka T, Sankawa U, Hayashi T. Effects of structural modification of calcium spirulan, a sulfated polysaccharide from Spirulina platensis, on antiviral activity. Chem Pharm Bull (Tokyo) 2001;49:108-10. https://doi.org/10.1248/cpb.49.108
  23. Marcel AK, Ekali LG, Eugene S, Arnold OE, Sandrine ED, von der Weid D, Gbaguidi E, Ngogang J, Mbanya JC. The effect of Spirulina platensis versus soybean on insulin resistance in HIV-infected patients: a randomized pilot study. Nutrients 2011;3:712-24. https://doi.org/10.3390/nu3070712
  24. Nkengfack G, Torimiro J, Ngogang J, Heike E. Effects of nutritional education and lifestyle modification on the nutritional status of HIV positive patients: results of a cluster randomized intervention over a period of six months. Glob Epidemi Obes 2013;1:5. https://doi.org/10.7243/2052-5966-1-5
  25. Moura LP, Puga GM, Beck WR, Teixeira IP, Ghezzi AC, Silva GA, Mello MA. Exercise and Spirulina control non-alcoholic hepatic steatosis and lipid profile in diabetic Wistar rats. Lipids Health Dis 2011;10:77. https://doi.org/10.1186/1476-511X-10-77
  26. Layam A, Reddy CL. Antidiabetic property of Spirulina. Diabetol Croat 2007;35:29-33.
  27. Hayashi O, Katoh T, Okuwaki Y. Enhancement of antibody production in mice by dietary Spirulina platensis. J Nutr Sci Vitaminol (Tokyo) 1994;40:431-41. https://doi.org/10.3177/jnsv.40.431
  28. Watanuki H, Ota K, Tassakka AC, Kato T, Sakai M. Immunostimulant effects of dietary Spirulina platensis on carp, Cyprinus carpio. Aquaculture 2006;258:157-63. https://doi.org/10.1016/j.aquaculture.2006.05.003
  29. Qureshi MA, Kidd MT, Ali RA. Spirulina platensis extract enhances chicken macrophages functions after in vitro exposure. J Nutr Immunol 1996;3:35-45.
  30. Hirahashi T, Matsumoto M, Hazeki K, Saeki Y, Ui M, Seya T. Activation of the human innate immune system by Spirulina: augmentation of interferon production and NK cytotoxicity by oral administration of hot water extract of Spirulina platensis. Int Immunopharmacol 2002;2:423-34. https://doi.org/10.1016/S1567-5769(01)00166-7
  31. Selmi C, Leung PS, Fischer L, German B, Yang CY, Kenny TP, Cysewski GR, Gershwin ME. The effects of Spirulina on anemia and immune function in senior citizens. Cell Mol Immunol 2011;8:248-54. https://doi.org/10.1038/cmi.2010.76
  32. Park HJ, Lee YJ, Ryu HK, Kim MH, Chung HW, Kim WY. A randomized double-blind, placebo-controlled study to establish the effects of Spirulina in elderly Koreans. Ann Nutr Metab 2008;52:322-8. https://doi.org/10.1159/000151486
  33. Park HJ, Lee HS. The influence of obesity on the effects of Spirulina supplementation in the human metabolic response of Korean elderly. Nutr Res Pract 2016;10:418-23. https://doi.org/10.4162/nrp.2016.10.4.418
  34. The Korean Nutrition Society. CAN-Pro 4.0: nutritional assessment program. Seoul: The Korean Nutrition Society; 2010.
  35. Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.
  36. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 1983;65:55-63. https://doi.org/10.1016/0022-1759(83)90303-4
  37. Bielinski SJ, Pankow JS, Miller MB, Hopkins PN, Eckfeldt JH, Hixson J, Liu Y, Register T, Myers RH, Arnett DK. Circulating MCP-1 levels shows linkage to chemokine receptor gene cluster on chromosome 3: the NHLBI family heart study follow-up examination. Genes Immun 2007;8:684-90. https://doi.org/10.1038/sj.gene.6364434
  38. Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 2009;29:313-26. https://doi.org/10.1089/jir.2008.0027
  39. Yamamoto T, Eckes B, Mauch C, Hartmann K, Krieg T. Monocyte chemoattractant protein-1 enhances gene expression and synthesis of matrix metalloproteinase-1 in human fibroblasts by an autocrine IL-1 alpha loop. J Immunol 2000;164:6174-9. https://doi.org/10.4049/jimmunol.164.12.6174
  40. Xia M, Sui Z. Recent developments in CCR2 antagonists. Expert Opin Ther Pat 2009;19:295-303. https://doi.org/10.1517/13543770902755129
  41. Rollins BJ. Chemokines. Blood 1997;90:909-28.
  42. de Lemos JA, Morrow DA, Sabatine MS, Murphy SA, Gibson CM, Antman EM, McCabe CH, Cannon CP, Braunwald E. Association between plasma levels of monocyte chemoattractant protein-1 and long-term clinical outcomes in patients with acute coronary syndromes. Circulation 2003;107:690-5. https://doi.org/10.1161/01.CIR.0000049742.68848.99
  43. Deo R, Khera A, McGuire DK, Murphy SA, Meo Neto Jde P, Morrow DA, de Lemos JA. Association among plasma levels of monocyte chemoattractant protein-1, traditional cardiovascular risk factors, and subclinical atherosclerosis. J Am Coll Cardiol 2004;44:1812-8. https://doi.org/10.1016/j.jacc.2004.07.047
  44. Navratilova Z. Polymorphisms in CCL2&CCL5 chemokines/chemokine receptors genes and their association with diseases. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 2006;150:191-204. https://doi.org/10.5507/bp.2006.028
  45. Szalai C, Kozma GT, Nagy A, Bojszko A, Krikovszky D, Szabo T, Falus A. Polymorphism in the gene regulatory region of MCP-1 is associated with asthma susceptibility and severity. J Allergy Clin Immunol 2001;108:375-81. https://doi.org/10.1067/mai.2001.117930
  46. Arakelyan A, Zakharyan R, Hambardzumyan M, Petrkova J, Olsson MC, Petrek M, Boyajyan A. Functional genetic polymorphisms of monocyte chemoattractant protein 1 and C-C chemokine receptor type 2 in ischemic stroke. J Interferon Cytokine Res 2014;34:100-5. https://doi.org/10.1089/jir.2013.0030
  47. Bjarnadottir K, Eiriksdottir G, Aspelund T, Gudnason V. Examination of genetic effects of polymorphisms in the MCP-1 and CCR2 genes on MI in the Icelandic population. Atherosclerosis 2006;188:341-6. https://doi.org/10.1016/j.atherosclerosis.2005.11.014
  48. Angeles-Martinez J, Posadas-Sanchez R, Alvarez-Leon E, Villarreal-Molina T, Cardoso-Saldana G, Fragoso JM, Juarez-Rojas JG, Medina-Urrutia A, Posadas-Romero C, Vargas-Alarcon G. Monocyte chemoattractant protein-1 gene (MCP-1) polymorphisms are associated with risk of premature coronary artery disease in Mexican patients from the Genetics of Atherosclerotic Disease (GEA) study. Immunol Lett 2015;167:125-30. https://doi.org/10.1016/j.imlet.2015.08.003
  49. Xu J, Liao YF, Zhou WP, Ming HL, Wang QH. The MCP-1 gene A-2518G polymorphism confers an increased risk of vascular complications in type 2 diabetes mellitus patients. Genet Test Mol Biomarkers 2015;19:411-7. https://doi.org/10.1089/gtmb.2014.0325
  50. Hou S, Yang P, Du L, Jiang Z, Mao L, Shu Q, Zhou H, Kijlstra A. Monocyte chemoattractant protein-1 -2518 A/G single nucleotide polymorphism in Chinese Han patients with ocular Behcet's disease. Hum Immunol 2010;71:79-82. https://doi.org/10.1016/j.humimm.2009.09.354
  51. Zuo S, Wang H, Wang B. Association of monocyte chemoattractant protein-1-2518A/G polymorphism and risk of coronary artery disease among the Chinese population: a meta-analysis. Int J Clin Exp Med 2015;8:15182-9.
  52. Jemaa R, Rojbani H, Kallel A, Ben Ali S, Feki M, Chabrak S, Elasmi M, Taieb SH, Sanhaji H, Souheil O, Mechmeche R, Kaabachi N. Association between the -2518G/A polymorphism in the monocyte chemoattractant protein-1 (MCP-1) gene and myocardial infarction in Tunisian patients. Clin Chim Acta 2008;390:122-5. https://doi.org/10.1016/j.cca.2008.01.004
  53. Kaur R, Matharoo K, Arora P, Bhanwer AJ. Association of -2518A>G promoter polymorphism in the monocyte chemoattractant protein-1 (MCP-1) gene with type 2 diabetes and coronary artery disease. Genet Test Mol Biomarkers 2013;17:750-5. https://doi.org/10.1089/gtmb.2013.0227
  54. Okopien B, Haberka M, Cwalina L, Kowalski J, Belowski D, Madej A, Zielinski M, Krysiak R, Labuzek K, Kalina Z, Herman ZS. Plasma cytokines as predictors of coronary heart disease. Res Commun Mol Pathol Pharmacol 2002;112:5-15.
  55. Gao HH, Gao LB, Wen JM. Correlations of MCP-1 -2518A>G polymorphism and serum levels with cerebral infarction risk: a meta-analysis. DNA Cell Biol 2014;33:522-30. https://doi.org/10.1089/dna.2013.2263
  56. Park HJ. Association of MCP-1 polymorphism with cardiovascular disease risk factors in Korean elderly. J Nutr Health 2013;46:511-20. https://doi.org/10.4163/jnh.2013.46.6.511
  57. Nelken NA, Coughlin SR, Gordon D, Wilcox JN. Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest 1991;88:1121-7. https://doi.org/10.1172/JCI115411
  58. Nikolich-Zugich J. T cell aging: naive but not young. J Exp Med 2005;201:837-40. https://doi.org/10.1084/jem.20050341
  59. Halkes CJ, van Dijk H, de Jaegere PP, Plokker HW, van Der Helm Y, Erkelens DW, Castro Cabezas M. Postprandial increase of complement component 3 in normolipidemic patients with coronary artery disease: effects of expanded-dose simvastatin. Arterioscler Thromb Vasc Biol 2001;21:1526-30. https://doi.org/10.1161/hq0901.095276
  60. Muscari A, Bozzoli C, Puddu GM, Sangiorgi Z, Dormi A, Rovinetti C, Descovich GC, Puddu P. Association of serum C3 levels with the risk of myocardial infarction. Am J Med 1995;98:357-64. https://doi.org/10.1016/S0002-9343(99)80314-3
  61. Hoskinson CD, Chew BP, Wong TS. Age-related changes in mitogeninduced lymphocyte proliferation and polymorphonuclear neutrophil function in the piglet. J Anim Sci 1990;68:2471-8. https://doi.org/10.2527/1990.6882471x

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