Hypothyroidism modifies lipid composition of polymorphonuclear leukocytes

Cellular Physiology and Biochemistry

Volumn 29, Issue 5-6, 2012, Pages 713-724

  Coria, Mariela J ^a   Viglianco, Yamila V Carmona ^a   Marra, Carlos A ^b   Gomez Mejiba, Sandra E ^c   Ramirez, Dario C ^c   Anzulovich, Ana C ^a   Gimenez, Maria S ^a  

^a UNIVERSIDAD NACIONAL DE SAN LUIS   (Argentina)

^b Facultad de Ciencias Médicas de la UNLP ^*  (Argentina)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

Cholesterol; HMGCoAR; Hypothyroidism; Triacylglycerides

Indexed keywords

ARACHIDONIC ACID; CHOLESTEROL; DIACYLGLYCEROL ACYLTRANSFERASE 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LINOLEIC ACID; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; MYRISTIC ACID; PALMITIC ACID; PHOSPHOLIPID; PROPYLTHIOURACIL; STEARIC ACID; STEROL REGULATORY ELEMENT BINDING PROTEIN 2; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; HYPOTHYROIDISM; LIPID COMPOSITION; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

EID: 84861413650     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000170987     Document Type: Article

References (69)

1. Martín-Zurro A: Patología tiroidea. Alteraciones del calcio; in Martín-Zurro A (eds): Atención Primaria, España: Elseiver, 2003, pp 1400-1456.
2. Dolphin PJ, Forsyth SJ: Nascent hepatic lipoproteins in hypothyroid rats. J Lipid Res 1983;24:541-551. (Pubitemid 13059190)
3. Diekman M J M, Anghelescu N, Endert E, Bakker O, Wiersinga WM: Changes in Plasma Low-Density Lipoprotein (LDL) - and High-Density Lipoprotein Cholesterol in Hypo-and Hyperthyroid Patients Are Related to Changes in Free Thyroxine, Not to Polymorphisms in LDL Receptor or Cholesterol Ester Transfer Protein Genes. J Clin Endocrinol Metab 2000;85:1857-1862. (Pubitemid 32269289)
4. Hapon MB, Varas SM, Jahn GA, Giménez MS: Effects of hypothyroidism on mammary and liver lipid metabolism in virgin and late-pregnant rats. J Lipid Res 2005;46:1320-1330. (Pubitemid 43109847)
5. Subudhi U, Das K, Paital B, Bhanja S, Chainy GB: Supplementation of curcumin and vitamin E enhances oxidative stress, but restores hepatic histoarchitecture in hypothyroid rats. Life Sci 2009;13:372-379.
6. Salter AM, Hayashi R, Al-seeni M, Brown NF, Bruce J, Sorensen O, Atkinson EA, Middleton B, Bleackley RC, Brindley DN: Effects of hypothyroidism and high-fat feeding on mRNA concentrations for the low-density-lipoprotein receptor and on acyl-CoA: cholesterol acyltransferase activities in rat liver Biochem J 1991;276:825-832.
7. Franco M, Castro G, Romero L, Regalado JC, Medina A, Huesca-Gómez C, Ramírez S, Montaño LF, Posadas-Romero C, Pérez- Méndez O: Decreased activity of lecithin: cholesterol acyltransferase and hepatic lipase in chronic hypothyroid rats: implications for reverse cholesterol transport. Mol Cell Biochem 2003;246:51-56. (Pubitemid 36798722)
8. Popovic L, Oreskovic K, Zupancic B, Petrunic M, Kunec-Vajic E: The relation between plasma lipid levels and pseudocholinesterase activity in hypothyroidism. Horm Metab Res 1998;30:137-140. (Pubitemid 28172520)
9. Apostolopoulos JJ, Howlett GJ, Fidge N: Effects of dietary cholesterol and hypothyroidism on rat apolipoprotein mRNA metabolism. J Lipid Res 1987;28:642-648. (Pubitemid 17085963)
10. Calder PC: n-3 fatty acids and mononuclear phagocyte function; in J. M. Kremer (ed): Medicinal Fatty Acids. Birkhauser, Basel, 1998, pp. 1-27.
11. Middleton J, Patterson AM, Gardner L, Schmutz C, Ashton BA: Leukocyte extravasation: chemokine transport and presentation by the endothelium. Blood 2002;100:3853-3860. (Pubitemid 35396849)
12. Baggiolini M, Boulay F, Badwey JA, Curnutte JT: Activation of neutrophil leukocytes: chemoattractant receptors and respiratory burst. FASEB J 1993;7:1004-1010. (Pubitemid 23243441)
13. Li S, Sun Y, Liang CP, Thorp EB, Han S, Jehle AW, Saraswathi V, Pridgen B, Kanter JE, Li R, Welch CL, Hasty AH, Bornfeldt KE, Breslow JL, Tabas I, Tall AR: Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet. Circ Res 2009;20:1072-1082.
14. Mutungi G, Torres-Gonzalez M, McGrane MM, Volek JS, Fernandez ML: Carbohydrate restriction and dietary cholesterol modulate the expression of HMG-CoA reductase and the LDL receptor in mononuclear cells from adult men. Lipids Health Dis 2007;28:6-34.
15. Lara LL, Rivera H, Perez-P C, Blanca I, Bianco NE, De Sanctis JB: Low density lipoprotein receptor expression and function in human polymorphonuclear leukocytes. Clin Exp Immunol 1997;107:205-212. (Pubitemid 27019831)
16. Bonneau C, Couderc R, Roch-Arveiller M, Giroud JP, Raichvarg D: Effects of low-density lipoproteins on polymorphonuclear leukocyte function in-vitro. J Lipid Mediat Cell Signal 1997;10:203-212.
17. Baillif RN, Kimbrough C: Studies on leucocyte granules after staining with sudan black B and May-Grünwald Giemsa. J Lab Clin Med 1947;32:155-166.
18. Guo RF, Sun L, Gao H, Shi KX, Rittirsch D, Sarma VJ, Zetoune FS, Ward PA: In vivo regulation of neutrophil apoptosis by C5a during sepsis. J Leukoc Biol 2006;80:1575-1583. (Pubitemid 44904996)
19. Juaregui HO, Hayner NT, Driscoll JL, Williams-Holland R, Lipsky MH, Galletti PM: Trypan blue dye uptake and lactate dehydrogenase in adult rat hepatocytes freshly isolated cells, cell suspensions, and primary monolayer cultures. In vitro 1981;17:1100-1110. (Pubitemid 12119617)
20. 2+ /dextran sulfate and its enzymatic measurement. Clin Chem 1978;24:931-933. (Pubitemid 8357907)
21. Friedewald WT, Levy RI, Fredrickson DS: Estimation of the concentration of lowdensity lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18:499-502.
22. Folch J, Less M, Sloane-Stanley GH: A simple method for the isolation and purification of total lipid from animal tissues. J Biol Chem 1968;226:497-509.
23. Malins DC, Mangold HK: Analysis of complex lipid mixtures by thin layer chromatography and complementary methods. J Am Oil Chem Soc 1960;37:576-582.
24. Fiske CH, Subbarow Y: Phosphorus compounds of muscle and liver. Science 1929;18:381-382.
25. Zack B, Moss N, Boyle AS, Zlatkis A: Reaction of certain unsaturated steroids with acid iron reagent. Anal Chem 1954;26:776-777.
26. Ellis BA, Poynten A, Lowy AJ, Furler SM, Chisholm DJ, Kraegen EW, Cooney GJ: Long-chain acyl-CoA esters as indicators of lipid metabolism and insulin sensitivity in rat and human muscle. Am J Physiol Endocrinol Metab 2000;279:554-560.
27. Sardesai VM, Manning JA: Determination of triglycerides in plasma and tissues. Clin Chem 1968;14:156-161.
28. Marra CA, de Alaniz M J T: Influence of Testosterone Administration on the Biosynthesis of Unsaturated Fatty Acids in Male and Female Rats. Lipids 1989;24:1014-1019. (Pubitemid 20027375)
29. Balkin MS, Buchholtz M, Ortiz J, Green AJ: Propylthiouracil (PTU)-induced agranulocytosis treated with recombinant human granulocyte colony-stimulating factor (G-CSF). Thyroid 1993;3:305-309. (Pubitemid 24015325)
30. Kariya K, Lee E, Hirouchi M: Relationship between leukopenia and bone marrow myeloperoxidase in the rat treated with propylthiouracil. Jpn J Pharmacol 1984;36:217-222. (Pubitemid 14044555)
31. Serebriakova OV, Govorin AV, Prosianik VI, Baksheeva EV: Fatty acid composition of the blood serum and erythrocyte membrane lipids in patients with hypothyroidism and left ventricular diastolic dysfunction. Klin Med (Mosk) 2008;86:40-43.
32. van Doormaal JJ, Muskiet FA, Martini IA, Doorenbos H: Changes in fatty acid profiles of plasma, erythrocytes and polymorphonuclear leukocytes in induced hypothyroidism in man: indirect evidence for altered delta 6 desaturase activity. Clin Chim Acta 1986;15:299-313.
33. Bakan E, Yildirim A, Kurtul N, Polat MF, Dursun H, Cayir K: Effects of type 2 diabetes mellitus on plasma fatty acid composition and cholesterol content of erythrocyte and leukocyte membranes. Acta Diabetol 2006;43:109-113. (Pubitemid 46072205)
34. Berlin RD, Fera JP: Changes in membrane microviscosity associated with phagocytosis: effects of colchicine. Proc Natl Acad Sci U S A 1977;74:1072-1076. (Pubitemid 8065673)
35. Gomes MG, Serakides R, Nunes VA, Da Silva CM, Carneiro RA, Ocarino NM: Perfil Hematológico de Ratas Adultas Hipotireóideas Castradas e Não Castradas. Arq Bras Endocrinol Metanol 2004;48:294-298.
36. Perello M, Friedman T, Paez-Espinosa V, Shen X, Stuart RC, Nillni EA: Thyroid Hormones Selectively Regulate the Posttranslational Processing of Prothyrotropin-Releasing Hormone in the Paraventricular Nucleus of the Hypothalamus. Endocrinology 2006;147:2705-2716. (Pubitemid 43764607)
37. Duntas LH: Thyroid Disease and Lipids. Thyroid 2002;12:287-293. (Pubitemid 34438931)
38. Byers SO, Rosenman RH, Friedman M, Biggs MW: Rate of cholesterol synthesis in hypo-and hyperthyroid rats. J Exp Med 1952;96:513-516.
39. Dory L, Roheim PS: Rat plasma lipoproteins and apolipoproteins in experimental hypothyroidism. J Lipid Res 1981;22:287-296. (Pubitemid 11125133)
40. Sample CE, Pendleton LC, Ness GC: Regulation of 3-hydroxy-3- methylglutaryl coenzyme A reductase levels by Ltriiodothyronine. Biochemistry 1987;26:727-731. (Pubitemid 17021048)
41. Cachefo A, Boucher P, Vidon C, Dusserre E, Diraison F, Beylot M: Hepatic Lipogenesis and Cholesterol Synthesis in Hyperthyroid Patients. J Clin Endocrinol Metab 2001;86:5353-5357. (Pubitemid 33070259)
42. Ness GC, Lopez D, Chambers CM, Newsome WP, Cornelius P, Long CA, Harwood HJ Jr: Effects of LTriiodothyronine and the Thyromimetic L-94901 on Serum Lipoprotein Levels and Hepatic Low-Density Lipoprotein Receptor, 3-Hydroxy-3-methylglutaryl Coenzyme A Reductase, and Apo A-I Gene Expression. Biochem Pharmacol 1998;56:121-129. (Pubitemid 28477459)
43. Kuo P, Weinfeld M, Loscalzo J: Effect of membrane fatty acyl composition on LDL metabolism in Hep G2 hepatocytes. Biochemistry 1990;17:6626-6632. (Pubitemid 20223557)
44. Horton JD, Goldstein JL, Brown MS: SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest 2002;109:1125-1131. (Pubitemid 34496588)
45. Shin DJ, Osborne TF: Thyroid Hormone Regulation and Cholesterol Metabolism Are Connected through Sterol Regulatory Element-binding Protein-2 (SREBP-2). J Biol Chem 2003;278:34114-34118. (Pubitemid 37553251)
46. Weller PF, Ackerman SI, Nicholson-Weller A, Dvorak AM: Cytoplasmic lipid bodies of human neutrophilic leukocytes. Am J Pathol 1989;135:947-959. (Pubitemid 20009505)
47. Weller PF, Dvorak AM: Arachidonic acid incorporation by cytoplasmic lipid bodies of human eosinophils. Blood 1985;65:269-1274.
48. Bandeira-Melo C, Phoofolo M, Weller PF: Extranuclear lipid bodies, elicited by CCR3-mediated signaling pathways, are the sites of chemokine-enhanced leukotriene C4 production in eosinophils and basophils. J Biol Chem 2001;22:22779-22787.
49. Galli SJ, Dvorak AM, Peters SP, Schulman ES, MacGlashan DW, Isomura T, Pyne K, Harvey VS, Hammel I, Lichtenstein LM, Dvorak HF: Lipid Bodies. Widely distributed cytoplasmic structures that represent preferential nonmembrane repositories of exogenous [3H] arachidonic acid incorporated by mast cells, macrophages, and other cell types; in Bailey JM (ed): Prostaglandins, Leukotrienes, and Lipoxins, Plenum, 1985, pp 221-239.
50. Lutas EM, Zucker-Franklin D: Formation of lipid inclusions in normal human leukocytes. Blood 1977;49:309-320. (Pubitemid 8032564)
51. Johnson MM, Vaughn B, Triggiani M, Swan DD, Fonteh AN, Chilton FH: Role of Arachidonyl Triglycerides within Lipid Bodies in Eicosanoid Formation by Human Polymorphonuclear Cells. J Respir Cell Mol Biol 1999;21:253-258. (Pubitemid 129502224)
52. Bozza PT, Magalhães KG, Weller PF: Leukocyte lipid bodies - Biogenesis and functions in inflammation. Biochim Biophys Acta 2009;1791:540-551.
53. Coleman RA, Douglas PL: Enzymes of triacylglycerol synthesis and their regulation. Prog Lipid Res 2004;43:134-176. (Pubitemid 37492937)
54. Coleman RA, Lewin TM, Muoio DM: Physiological and nutritional regulation of enzymes of triacylglycerol synthesis. Ann Rev Nutr 2000;20:77-103.
55. Akesson B: Composition of rat liver triacylglycerols and diacylglycerols. Eur J Biochem 1969;9:463-477.
56. Dircks L, Sul HS: Acyltransferases of de novo glycerophospholipid biosynthesis. Prog Lipid Res 1999;38:461-479.
57. van Doormaal JJ, Muskiet FA, Martini IA, Doorenbos H: Changes in fatty acid profiles of plasma, erythrocytes and polymorphonuclear leukocytes in induced hypothyroidism in man: indirect evidence for altered delta 6 desaturase activity. Clin Chim Acta 1986;15:299-313.
58. Faas FH, Carter WJ: Fatty acid desaturation and microsomal lipid fatty acid composition in experimental hypothyroidism. Biochem J 1982;207:29-35. (Pubitemid 13255213)
59. Landriscina C, Gnoni GV, Quagliariello E: Effect of thyroid hormones on microsomal fatty acid chain elongation synthesis in rat liver. Eur J Biochem 1976;71:135-143. (Pubitemid 8001903)
60. Chini B, Parenti M: G-protein coupled receptors in lipid rafts and caveolae: how, when and why do they go there? J Mol Endocrinol 2004;32:325-348.
61. Filippov A, Oradd G, Lindblom G: Lipid lateral diffusion in ordered and disordered phases in raft mixtures. Biophys J 2004;86:891-896. (Pubitemid 38209533)
62. Keller SL, Anderson TG, McConnell HM: Miscibility critical pressures in monolayers of ternary lipid mixtures. Biophys J 2000;79:2033-2042.
63. Radhakrishnan A, McConnell H: Condensed complexes in vesicles containing cholesterol and phospholipids. Proc Natl Acad Sci 2005;102:12662-12666. (Pubitemid 41279421)
64. 2+ Entry and Respiratory Burst: Correlations with Calcium Channel Raft Trafficking. J Immunol 2007;178:5253-5261. (Pubitemid 46595310)
65. 2+ influx in human neutrophils occurs via store operated mechanisms. J. Leukocyte Biol 2001;69:63-68. (Pubitemid 32095118)
66. Axelband F, Dias J, Ferrão FM, Einicker-Lamas M: Nongenomic signaling pathways triggered by thyroid hormones and their metabolite 3-iodothyronamine on the cardiovascular system. J Cell Physiol 2011;226:221-28.
67. Bergh JJ, Lin HY, Lansing L, Mohamed SN, Davis FB, Mousa S, Davis PJ: Integrin aVb3 contains a cell surface receptor site for thyroid hormones that is linked to activation of mitogen-activated protein kinase and induction of angiogenesis. Endocrinology 2005;146:2864-2871. (Pubitemid 41002793)
68. De Vito P, Incerpi S, Pedersen JZ, Luly P, Davis FB, Davis PJ: Thyroid Hormones as Modulators of Immune Activities at the Cellular Level. Thyroid 2011;21:879-890.
69. Oh H, Mohler ER, Tian A, Baumgart T, Diamond SL: Membrane Cholesterol Is a Biomechanical Regulator of Neutrophil Adhesion. Arterioscler Thromb Vasc Biol 2009;29:1290-1297.