Myeloid cell-specific ABCA1 deletion does not worsen insulin resistance in HF diet-induced or genetically obese mouse models

Journal of Lipid Research

Volumn 54, Issue 10, 2013, Pages 2708-2717

  Zhu, Xuewei ^a   Chung, Soonkyu ^a,b   Bi, Xin ^a   Chuang, Chia Chi ^a   Brown, Amanda L ^a   Liu, Mingxia ^a   Seo, Jeongmin ^a   Cuffe, Helen ^a   Gebre, Abraham K ^a   Boudyguina, Elena ^a   Parks, John S ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cholesterol; High fat; Inflammation; Macrophage; Obesity

Indexed keywords

ABC TRANSPORTER A1; ARGINASE 1; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARGINASE 1 GENE; ARTICLE; CELL INFILTRATION; CH313 GENE; CONTROLLED STUDY; DISEASE EXACERBATION; FATTY LIVER; GENE EXPRESSION; HYPERCHOLESTEROLEMIA; IL 6 GENE; INSULIN RESISTANCE; MACROPHAGE ACTIVATION; MALE; MCP 1 GENE; MOLECULAR PATHOLOGY; MOUSE; NONHUMAN; OBESITY; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; TNF ALPHA GENE; UPREGULATION; WILD TYPE;

CHOLESTEROL; HIGH-FAT; INFLAMMATION; MACROPHAGE; OBESITY;

ADIPOSE TISSUE, WHITE; ANIMALS; ATP BINDING CASSETTE TRANSPORTER 1; CELLS, CULTURED; CHEMOKINES; CHOLESTEROL; DIET, HIGH-FAT; EPIDIDYMIS; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; MICE, TRANSGENIC; OBESITY;

EID: 84884146156     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M038943     Document Type: Article

References (39)

1. Hotamisligil, G. S., P. Arner, J. F. Caro, R. L. Atkinson, and B. M. Spiegelman. 1995. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J. Clin. Invest. 95: 2409-2415.
2. Kanda, H., S. Tateya, Y. Tamori, K. Kotani, K. Hiasa, R. Kitazawa, S. Kitazawa, H. Miyachi, S. Maeda, K. Egashira, et al. 2006. MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J. Clin. Invest. 116: 1494-1505.
3. Hotamisligil, G. S., P. Peraldi, A. Budavari, R. Ellis, M. F. White, and B. M. Spiegelman. 1996. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science. 271: 665-668.
4. Wellen, K. E., and G. S. Hotamisligil. 2003. Obesity-induced inflammatory changes in adipose tissue. J. Clin. Invest. 112: 1785-1788.
5. Hwang, D. 2001. Modulation of the expression of cyclooxygenase-2 by fatty acids mediated through toll-like receptor 4-derived signaling pathways. FASEB J. 15: 2556-2564.
6. Lee, J. Y., K. H. Sohn, S. H. Rhee, and D. Hwang. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276: 16683-16689.
7. Shi, H., M. V. Kokoeva, K. Inouye, I. Tzameli, H. Yin, and J. S. Flier. 2006. TLR4 links innate immunity and fatty acid-induced insulin resistance. J. Clin. Invest. 116: 3015-3025.
8. Saberi, M., N. B. Woods, C. de Luca, S. Schenk, J. C. Lu, G. Bandyopadhyay, I. M. Verma, and J. M. Olefsky. 2009. Hematopoietic cell-specific deletion of toll-like receptor 4 ameliorates hepatic and adipose tissue insulin resistance in high-fat-fed mice. Cell Metab. 10: 419-429.
9. Solinas, G., C. Vilcu, J. G. Neels, G. K. Bandyopadhyay, J. L. Luo, W. Naugler, S. Grivennikov, A. Wynshaw-Boris, M. Scadeng, J. M. Olefsky, et al. 2007. JNK1 in hematopoietically derived cells contributes to diet-induced inflammation and insulin resistance without affecting obesity. Cell Metab. 6: 386-397.
10. Arkan, M. C., A. L. Hevener, F. R. Greten, S. Maeda, Z. W. Li, J. M. Long, A. Wynshaw-Boris, G. Poli, J. Olefsky, and M. Karin. 2005. IKK-beta links inflammation to obesity-induced insulin resistance. Nat. Med. 11: 191-198.
11. Attie, A. D., J. P. Kastelein, and M. R. Hayden. 2001. Pivotal role of ABCA1 in reverse cholesterol transport influencing HDL levels and susceptibility to atherosclerosis. J. Lipid Res. 42: 1717-1726.
12. Oram, J. F., and R. M. Lawn. 2001. ABCA1. The gatekeeper for eliminating excess tissue cholesterol. J. Lipid Res. 42: 1173-1179.
13. Bodzioch, M., E. Orso, J. Klucken, T. Langmann, A. Bottcher, W. Diederich, W. Drobnik, S. Barlage, C. Buchler, M. Porsch- Ozcurumez, et al. 1999. The gene encoding ATP-binding cassette transporter 1 is mutated in Tangier disease. Nat. Genet. 22: 347-351.
14. Brooks-Wilson, A., M. Marcil, S. M. Clee, L. H. Zhang, K. Roomp, M. van Dam, L. Yu, C. Brewer, J. A. Collins, H. O. Molhuizen, et al. 1999. Mutations in ABC1 in Tangier disease and familial high-density lipoprotein deficiency. Nat. Genet. 22: 336-345.
15. Rust, S., M. Rosier, H. Funke, J. Real, Z. Amoura, J. C. Piette, J. F. Deleuze, H. B. Brewer, N. Duverger, P. Denefle, et al. 1999. Tangier disease is caused by mutations in the gene encoding ATP-binding cassette transporter 1. Nat. Genet. 22: 352-355.
16. Serfaty-Lacrosniere, C., F. Civeira, A. Lanzberg, P. Isaia, J. Berg, E. D. Janus, M. P. Smith, Jr ., P. H. Pritchard, J. Frohlich, and R. S. Lees. 1994. Homozygous Tangier disease and cardiovascular disease. Atherosclerosis. 107: 85-98.
17. Daimon, M., T. Kido, M. Baba, T. Oizumi, Y. Jimbu, W. Kameda, H. Yamaguchi, H. Ohnuma, M. Tominaga, M. Muramatsu, et al. 2005. Association of the ABCA1 gene polymorphisms with type 2 DM in a Japanese population. Biochem. Biophys. Res. Commun. 329: 205-210.
18. Porchay, I., F. Pean, N. Bellili, B. Royer, J. Cogneau, M. C. Chesnier, A. Caradec, J. Tichet, B. Balkau, M. Marre, et al. 2006. ABCA1 single nucleotide polymorphisms on high-density lipoprotein-cholesterol and overweight: the D.E.S.I.R. study. Obesity (Silver Spring). 14: 1874-1879.
19. Villarreal-Molina, M. T., C. A. Aguilar-Salinas, M. Rodriguez-Cruz, D. Riano, M. Villalobos-Comparan, R. Coral-Vazquez, M. Menjivar, P. Yescas-Gomez, M. Konigsoerg-Fainstein, S. Romero-Hidalgo, et al. 2007. The ATP-binding cassette transporter A1 R230C variant affects HDL cholesterol levels and BMI in the Mexican population: association with obesity and obesity-related comorbidities. Diabetes. 56: 1881-1887.
20. Villarreal-Molina, M. T., M. T. Flores-Dorantes, O. Arellano- Campos, M. Villalobos-Comparan, M. Rodriguez-Cruz, A. Miliar- Garcia, A. Huertas-Vazquez, M. Menjivar, S. Romero-Hidalgo, N. H. Wacher, et al. 2008. Association of the ATP-binding cassette transporter A1 R230C variant with early-onset type 2 diabetes in a Mexican population. Diabetes. 57: 509-513.
21. Patel, D. C., C. Albrecht, D. Pavitt, V. Paul, C. Pourreyron, S. P. Newman, I. F. Godsland, J. Valabhji, and D. G. Johnston. 2011. Type 2 diabetes is associated with reduced ATP-binding cassette transporter A1 gene expression, protein and function. PLoS ONE. 6: e22142.
22. Albrecht, C., I. Simon-Vermot, J. I. Elliott, C. F. Higgins, D. G. Johnston, and J. Valabhji. 2004. Leukocyte ABCA1 gene expression is associated with fasting glucose concentration in normoglycemic men. Metabolism. 53: 17-21.
23. Brunham, L. R., J. K. Kruit, T. D. Pape, J. M. Timmins, A. Q. Reuwer, Z. Vasanji, B. J. Marsh, B. Rodrigues, J. D. Johnson, J. S. Parks, et al. 2007. Beta-cell ABCA1 influences insulin secretion, glucose homeostasis and response to thiazolidinedione treatment. Nat. Med. 13: 340-347.
24. Zhu, X., J. Y. Lee, J. M. Timmins, J. M. Brown, E. Boudyguina, A. Mulya, A. K. Gebre, M. C. Willingham, E. M. Hiltbold, N. Mishra, et al. 2008. Increased cellular free cholesterol in macrophage-specific Abca1 knock-out mice enhances pro-inflammatory response of macrophages. J. Biol. Chem. 283: 22930-22941.
25. Zhu, X., J. S. Owen, M. D. Wilson, H. Li, G. L. Griffiths, M. J. Thomas, E. M. Hiltbold, M. B. Fessler, and J. S. Parks. 2010. Macrophage ABCA1 reduces MyD88-dependent Toll-like receptor trafficking to lipid rafts by reduction of lipid raft cholesterol. J. Lipid Res. 51: 3196-3206.
26. Zhu, X., M. M. Westcott, X. Bi, M. Liu, K. M. Gowdy, J. Seo, Q. Cao, A. K. Gebre, M. B. Fessler, E. M. Hiltbold, et al. 2012. Myeloid cellspecific ABCA1 deletion protects mice from bacterial infection. Circ. Res. 111: 1398-1409.
27. Brown, J. M., Y. D. Halvorsen, Y. R. Lea-Currie, C. Geigerman, and M. McIntosh. 2001. Trans-10, cis-12, but not cis-9, trans-11, conjugated linoleic acid attenuates lipogenesis in primary cultures of stromal vascular cells from human adipose tissue. J. Nutr. 131: 2316-2321.
28. Stewart, C. R., L. M. Stuart, K. Wilkinson, J. M. van Gils, J. Deng, A. Halle, K. J. Rayner, L. Boyer, R. Zhong, W. A. Frazier, et al. 2010. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat. Immunol. 11: 155-161.
29. Weisberg, S. P., D. McCann, M. Desai, M. Rosenbaum, R. L. Leibel, and A. W. Ferrante, Jr. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112: 1796-1808.
30. Xu, H., G. T. Barnes, Q. Yang, G. Tan, D. Yang, C. J. Chou, J. Sole, A. Nichols, J. S. Ross, L. A. Tartaglia, et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112: 1821-1830.
31. Lumeng, C. N., J. L. Bodzin, and A. R. Saltiel. 2007. Obesity induces a phenotypic switch in adipose tissue macrophage polarization. J. Clin. Invest. 117: 175-184.
32. Hotamisligil, G. S. 2006. Inflammation and metabolic disorders. Nature. 444: 860-867.
33. Aiello, R. J., D. Brees, P. A. Bourassa, L. Royer, S. Lindsey, T. Coskran, M. Haghpassand, and O. L. Francone. 2002. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler. Thromb. Vasc. Biol. 22: 630-637.
34. van Eck, M., I. S. Bos, W. E. Kaminski, E. Orsó, G. Rothe, J. Twisk, A. Böttcher, E. S. Van Amersfoort, T. A. Christiansen-Weber, W. P. Fung-Leung, et al. 2002. Leukocyte ABCA1 controls susceptibility to atherosclerosis and macrophage recruitment into tissues. Proc. Natl. Acad. Sci. USA. 99: 6298-6303.
35. Yvan-Charvet, L., M. Ranalletta, N. Wang, S. Han, N. Terasaka, R. Li, C. Welch, and A. R. Tall. 2007. Combined deficiency of ABCA1 and ABCG1 promotes foam cell accumulation and accelerates atherosclerosis in mice. J. Clin. Invest. 117: 3900-3908.
36. Han, M. S., D. Y. Jung, C. Morel, S. A. Lakhani, J. K. Kim, R. A. Flavell, and R. J. Davis. 2013. JNK expression by macrophages promotes obesity-induced insulin resistance and inflammation. Science. 339: 218-222.
37. Vijay-Kumar, M., J. D. Aitken, F. A. Carvalho, T. R. Ziegler, A. T. Gewirtz, and V. Ganji. 2011. Loss of function mutation in toll-like receptor-4 does not offer protection against obesity and insulin resistance induced by a diet high in trans fat in mice. J. Inflamm. (Lond.). 8: 2.
38. Hosoi, T., S. Yokoyama, S. Matsuo, S. Akira, and K. Ozawa. 2010. Myeloid differentiation factor 88 (MyD88)-deficiency increases risk of diabetes in mice. PLoS ONE. 5: e12537.
39. Erridge, C., and N. J. Samani. 2009. Saturated fatty acids do not directly stimulate Toll-like receptor signaling. Arterioscler. Thromb. Vasc. Biol. 29: 1944-1949.