Deletion of serum amyloid A3 improves high fat high sucrose diet-induced adipose tissue inflammation and hyperlipidemia in female mice

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Den Hartigh, Laura J ^a   Wang, Shari ^a   Goodspeed, Leela ^a   Ding, Yilei ^a   Averill, Michelle ^a   Subramanian, Savitha ^a   Wietecha, Tomasz ^a   O'Brien, Kevin D ^a   Chait, Alan ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; LIPOPROTEIN; TRIACYLGLYCEROL; SAA3 PROTEIN, MOUSE; SERUM AMYLOID A; SUGAR INTAKE;

ADIPOSE TISSUE INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BODY COMPOSITION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEMALE; GENE; GENE DELETION; GENE EXPRESSION; GENE FUNCTION; GLUCOSE METABOLISM; HYPERLIPIDEMIA; INFLAMMATION; LIPOPROTEIN BLOOD LEVEL; MACROPHAGE; MALE; MOUSE; NONHUMAN; OBESITY; RESTING METABOLIC RATE; SAA1 GENE; SAA2 GENE; SERUM AMYLOID A3 GENE; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN; ADIPOSE TISSUE; ADMINISTRATION AND DOSAGE; ANIMAL; C57BL MOUSE; GENETICS; LIPID DIET; LIVER; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SUGAR INTAKE; TRANSGENIC MOUSE;

MUS;

ADIPOSE TISSUE; ANIMALS; DIET, HIGH-FAT; DIETARY SUCROSE; FEMALE; HYPERLIPIDEMIAS; INFLAMMATION; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SERUM AMYLOID A PROTEIN; WEIGHT GAIN;

EID: 84907486570     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0108564     Document Type: Article

References (64)

1. Müller S, Martin S, Koenig W, Hanifi-Moghaddam P, Rathmann W, et al. (2002) Impaired glucose tolerance is associated with increased serum concentrations of interleukin 6 and co-regulated acute-phase proteins but not TNF-alpha or its receptors. Diabetologia 45: 805-812.
2. Poitou C, Viguerie N, Cancello R, De Matteis R, Cinti S, et al. (2005) Serum amyloid A: production by human white adipocyte and regulation by obesity and nutrition. Diabetologia 48: 519-528.
3. Lewis KE, Kirk EA, McDonald TO, Wang S, Wight TN, et al. (2004) Increase in serum amyloid a evoked by dietary cholesterol is associated with increased atherosclerosis in mice. Circulation 110: 540-545.
4. Scheja L, Heese B, Zitzer H, Michael MD, Siesky AM, et al. (2008) Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp Diabetes Res 2008: 230837.
5. McAdam KP, Sipe JD (1976) Murine model for human secondary amyloidosis: genetic variability of the acute-phase serum protein SAA response to endotoxins and casein. J Exp Med 144: 1121-1127.
6. Migita K, Eguchi K, Tsukada T, Kawabe Y, Takashima H, et al. (1996) Increased circulating serum amyloid A protein derivatives in rheumatoid arthritis patients with secondary amyloidosis. Lab Invest 75: 371-375.
7. O'Hara R, Murphy EP, Whitehead AS, FitzGerald O, Bresnihan B (2000) Acute-phase serum amyloid A production by rheumatoid arthritis synovial tissue. Arthritis Res 2: 142-144.
8. Fyfe AI, Rothenberg LS, DeBeer FC, Cantor RM, Rotter JI, et al. (1997) Association between serum amyloid A proteins and coronary artery disease: evidence from two distinct arteriosclerotic processes. Circulation 96: 2914-2919.
9. Johnson BD, Kip KE, Marroquin OC, Ridker PM, Kelsey SF, et al. (2004) Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women's Ischemia Syndrome Evaluation (WISE). Circulation 109: 726-732.
10. van Dielen FM, van't Veer C, Schols AM, Soeters PB, Buurman WA, et al. (2001) Increased leptin concentrations correlate with increased concentrations of inflammatory markers in morbidly obese individuals. Int J Obes Relat Metab Disord 25: 1759-1766.
11. Benditt EP, Eriksen N (1977) Amyloid protein SAA is associated with high density lipoprotein from human serum. Proc Natl Acad Sci U S A 74: 4025-4028.
12. Meek RL, Benditt EP (1986) Amyloid A gene family expression in different mouse tissues. J Exp Med 164: 2006-2017.
13. Benditt EP, Meek RL (1989) Expression of the third member of the serum amyloid A gene family in mouse adipocytes. J Exp Med 169: 1841-1846.
14. Chiba T, Han CY, Vaisar T, Shimokado K, Kargi A, et al. (2009) Serum amyloid A3 does not contribute to circulating SAA levels. J Lipid Res 50: 1353-1362.
15. Reigstad CS, Lundén GO, Felin J, Bäckhed F (2009) Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PLoS One 4: e5842.
16. Kluve-Beckerman B, Drumm ML, Benson MD (1991) Nonexpression of the human serum amyloid A three (SAA3) gene. DNA Cell Biol 10: 651-661.
17. Uhlar CM, Whitehead AS (1999) Serum amyloid A, the major vertebrate acute-phase reactant. Eur J Biochem 265: 501-523.
18. Badolato R, Johnston JA, Wang JM, McVicar D, Xu LL, et al. (1995) Serum amyloid A induces calcium mobilization and chemotaxis of human monocytes by activating a pertussis toxin-sensitive signaling pathway. J Immunol 155: 4004-4010.
19. Liang TS, Wang JM, Murphy PM, Gao JL (2000) Serum amyloid A is a chemotactic agonist at FPR2, a low-affinity N-formylpeptide receptor on mouse neutrophils. Biochem Biophys Res Commun 270: 331-335.
20. Su SB, Gong W, Gao JL, Shen W, Murphy PM, et al. (1999) A seven-transmembrane, G protein-coupled receptor, FPRL1, mediates the chemotactic activity of serum amyloid A for human phagocytic cells. J Exp Med 189: 395-402.
21. Lindhorst E, Young D, Bagshaw W, Hyland M, Kisilevsky R (1997) Acute inflammation, acute phase serum amyloid A and cholesterol metabolism in the mouse. Biochim Biophys Acta 1339: 143-154.
22. Kisilevsky R, Subrahmanyan L (1992) Serum amyloid A changes high density lipoprotein's cellular affinity. A clue to serum amyloid A's principal function. Lab Invest 66: 778-785.
23. Tsun JG, Shiu SW, Wong Y, Yung S, Chan TM, et al. (2013) Impact of serum amyloid A on cellular cholesterol efflux to serum in type 2 diabetes mellitus. Atherosclerosis 231: 405-410.
24. Artl A, Marsche G, Lestavel S, Sattler W, Malle E (2000) Role of serum amyloid A during metabolism of acute-phase HDL by macrophages. Arterioscler Thromb Vasc Biol 20: 763-772.
25. Banka CL, Yuan T, de Beer MC, Kindy M, Curtiss LK, et al. (1995) Serum amyloid A (SAA): influence on HDL-mediated cellular cholesterol efflux. J Lipid Res 36: 1058-1065.
26. Uhlar CM, Burgess CJ, Sharp PM, Whitehead AS (1994) Evolution of the serum amyloid A (SAA) protein superfamily. Genomics 19: 228-235.
27. Lowell CA, Potter DA, Stearman RS, Morrow JF (1986) Structure of the murine serum amyloid A gene family. Gene conversion. J Biol Chem 261: 8442-8452.
28. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, et al. (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808.
29. Han C, Subramanian S, Chan C, Omer M, Chiba T, et al. (2007) Adipocyte-derived serum amyloid A3 and hyaluronan play a role in monocyte recruitment and adhesion. Diabetes 56: 2260-2273.
30. Lin Y, Rajala MW, Berger JP, Moller DE, Barzilai N, et al. (2001) Hyperglycemia-induced production of acute phase reactants in adipose tissue. J Biol Chem 276: 42077-42083.
31. Badolato R, Wang JM, Murphy WJ, Lloyd AR, Michiel DF, et al. (1994) Serum amyloid A is a chemoattractant: induction of migration, adhesion, and tissue infiltration of monocytes and polymorphonuclear leukocytes. J Exp Med 180: 203-209.
32. Subramanian S, Han C, Chiba T, McMillen T, Wang S, et al. (2008) Dietary cholesterol worsens adipose tissue macrophage accumulation and atherosclerosis in obese LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol 28: 685-691.
33. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, et al. (2006) CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 116: 115-124.
34. Matsen ME, Thaler JP, Wisse BE, Guyenet SJ, Meek TH, et al. (2013) In uncontrolled diabetes, thyroid hormone and sympathetic activators induce thermogenesis without increasing glucose uptake in brown adipose tissue. Am J Physiol Endocrinol Metab 304: E734-746.
35. Morton GJ, Kaiyala KJ, Fisher JD, Ogimoto K, Schwartz MW, et al. (2011) Identification of a physiological role for leptin in the regulation of ambulatory activity and wheel running in mice. Am J Physiol Endocrinol Metab 300: E392-401.
36. McLean J, Tobin G (1987) Animal and Human Calorimetry. Cambridge, UK: Cambridge Univ. Press.
37. Schreyer SA, Vick C, Lystig TC, Mystkowski P, LeBoeuf RC (2002) LDL receptor but not apolipoprotein E deficiency increases diet-induced obesity and diabetes in mice. Am J Physiol Endocrinol Metab 282: E207-214.
38. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
39. Subramanian S, Goodspeed L, Wang S, Kim J, Zeng L, et al. (2011) Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice. J Lipid Res 52: 1626-1635.
40. Subramanian V, Ferrante AW (2009) Obesity, inflammation, and macrophages. Nestle Nutr Workshop Ser Pediatr Program 63: 151-159; discussion 159-162, 259-168.
41. Han CY, Subramanian S, Chan CK, Omer M, Chiba T, et al. (2007) Adipocyte-derived serum amyloid A3 and hyaluronan play a role in monocyte recruitment and adhesion. Diabetes 56: 2260-2273.
42. Denis GV, Obin MS (2013) 'Metabolically healthy obesity': origins and implications. Mol Aspects Med 34: 59-70.
43. Kramer CK, Zinman B, Retnakaran R (2013) Are metabolically healthy overweight and obesity benign conditions?: A systematic review and meta-analysis. Ann Intern Med 159: 758-769.
44. Alam I, Ng TP, Larbi A (2012) Does inflammation determine whether obesity is metabolically healthy or unhealthy? The aging perspective. Mediators Inflamm 2012: 456456.
45. Lee HY, Kim SD, Shim JW, Kim HJ, Yun J, et al. (2010) A pertussis toxin sensitive G-protein-independent pathway is involved in serum amyloid A-induced formyl peptide receptor 2-mediated CCL2 production. Exp Mol Med 42: 302-309.
46. Li Y, Cai L, Wang H, Wu P, Gu W, et al. (2011) Pleiotropic regulation of macrophage polarization and tumorigenesis by formyl peptide receptor-2. Oncogene 30: 3887-3899.
47. Lee HY, Kim SD, Shim JW, Lee SY, Lee H, et al. (2008) Serum amyloid A induces CCL2 production via formyl peptide receptor-like 1-mediated signaling in human monocytes. J Immunol 181: 4332-4339.
48. Liverton NJ, Butcher JW, Claiborne CF, Claremon DA, Libby BE, et al. (1999) Design and synthesis of potent, selective, and orally bioavailable tetrasubstituted imidazole inhibitors of p38 mitogen-activated protein kinase. J Med Chem 42: 2180-2190.
49. Hollenbach E, Neumann M, Vieth M, Roessner A, Malfertheiner P, et al. (2004) Inhibition of p38 MAP kinase- and RICK/NF-kappaB-signaling suppresses inflammatory bowel disease. FASEB J 18: 1550-1552.
50. Ando H, Kurita S, Takamura T (2004) The specific p38 mitogen-activated protein kinase pathway inhibitor FR167653 keeps insulitis benign in nonobese diabetic mice. Life Sci 74: 1817-1827.
51. Krementsov DN, Noubade R, Dragon JA, Otsu K, Rincon M, et al. (2014) Sex-specific control of central nervous system autoimmunity by p38 mitogen-activated protein kinase signaling in myeloid cells. Ann Neurol 75: 50-66.
52. Pettersson US, Waldén TB, Carlsson PO, Jansson L, Phillipson M (2012) Female mice are protected against high-fat diet induced metabolic syndrome and increase the regulatory T cell population in adipose tissue. PLoS One 7: e46057.
53. Davis KE, D'Neinast M, Sun K, M Skiles W, D'Bills J, et al. (2013) The sexually dimorphic role of adipose and adipocyte estrogen receptors in modulating adipose tissue expansion, inflammation, and fibrosis. Mol Metab 2: 227-242.
54. Register TC, Cann JA, Kaplan JR, Williams JK, Adams MR, et al. (2005) Effects of soy isoflavones and conjugated equine estrogens on inflammatory markers in atherosclerotic, ovariectomized monkeys. J Clin Endocrinol Metab 90: 1734-1740.
55. Christodoulakos GE, Lambrinoudaki IV, Economou EV, Papadias C, Vitoratos N, et al. (2007) Circulating chemoattractants RANTES, negatively related to endogenous androgens, and MCP-1 are differentially suppressed by hormone therapy and raloxifene. Atherosclerosis 193: 142-150.
56. Sjöholm K, Lundgren M, Olsson M, Eriksson JW (2009) Association of serum amyloid A levels with adipocyte size and serum levels of adipokines: differences between men and women. Cytokine 48: 260-266.
57. Shoelson SE, Herrero L, Naaz A (2007) Obesity, inflammation, and insulin resistance. Gastroenterology 132: 2169-2180.
58. Montes VN, Turner MS, Subramanian S, Ding Y, Hayden-Ledbetter M, et al. (2013) T cell activation inhibitors reduce CD8+ T cell and pro-inflammatory macrophage accumulation in adipose tissue of obese mice. PLoS One 8: e67709.
59. Ahlin S, Olsson M, Olsson B, Svensson PA, Sjöholm K (2013) No Evidence for a Role of Adipose Tissue-Derived Serum Amyloid A in the Development of Insulin Resistance or Obesity-Related Inflammation in hSAA1(+/-) Transgenic Mice. PLoS One 8: e72204.
60. Ahlin S, Olsson M, Wilhelmson AS, Skålén K, Borén J, et al. (2014) Adipose Tissue-Derived Human Serum Amyloid A Does Not Affect Atherosclerotic Lesion Area in hSAA1+/-/ApoE-/- Mice. PLoS One 9: e95468.
61. De Beer MC, Wroblewski JM, Noffsinger VP, Rateri DL, Howatt DA, et al. (2014) Deficiency of endogenous acute phase serum amyloid A does not affect atherosclerotic lesions in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 34: 255-261.
62. Ryan AS, Ge S, Blumenthal JB, Serra MC, Prior SJ, et al. (2014) Aerobic exercise and weight loss reduce vascular markers of inflammation and improve insulin sensitivity in obese women. J Am Geriatr Soc 62: 607-614.
63. Poitou C, Coussieu C, Rouault C, Coupaye M, Cancello R, et al. (2006) Serum amyloid A: a marker of adiposity-induced low-grade inflammation but not of metabolic status. Obesity (Silver Spring) 14: 309-318.
64. Sjöholm K, Palming J, Olofsson LE, Gummesson A, Svensson PA, et al. (2005) A microarray search for genes predominantly expressed in human omental adipocytes: adipose tissue as a major production site of serum amyloid A. J Clin Endocrinol Metab 90: 2233-2239.