Macrophage SR-BI regulates LPS-induced pro-inflammatory signaling in mice and isolated macrophages

Journal of Lipid Research

Volumn 53, Issue 8, 2012, Pages 1472-1481

  Cai, Lei ^a,b,c   Wang, Zhen ^c,d   Meyer, Jason M ^b,c   Ji, Ailing ^a,b,c   Van Der Westhuyzen, Deneys R ^a,b,c  

^a LEXINGTON VA MEDICAL CENTER   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

^d SHANDONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Inflammation; Lipopolysaccharide; Scavenger receptor

Indexed keywords

CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; SCAVENGER RECEPTOR BI; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; INFLAMMATION; LIPID RAFT; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD36; BIOLOGICAL TRANSPORT; BONE MARROW TRANSPLANTATION; CELL SEPARATION; CHOLESTEROL; CYTOKINES; GENE DELETION; GENE EXPRESSION REGULATION; INFLAMMATION; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIPOPOLYSACCHARIDES; MACROPHAGES; MALE; MICE; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 84863799417     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M023234     Document Type: Article

References (42)

1. Russell, J. A. 2006. Management of sepsis. N. Engl. J. Med. 355: 1699-1713. (Pubitemid 44583960)
2. Cohen, J. 2002. The immunopathogenesis of sepsis. Nature. 420: 885-891. (Pubitemid 36019643)
3. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature. 406: 782-787.
4. Trinchieri, G., and A. Sher. 2007. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7: 179-190.
5. Rittirsch, D., M. A. Flierl, and P. A. Ward. 2008. Harmful molecular mechanisms in sepsis. Nat. Rev. Immunol. 8: 776-787.
6. Philips, J. A., E. J. Rubin, and N. Perrimon. 2005. Drosophila RNAi screen reveals CD36 family member required for mycobacterial infection. Science. 309: 1251-1253. (Pubitemid 41170920)
7. Vishnyakova, T. G., A. V. Bocharov, I. N. Baranova, Z. Chen, A. T. Remaley, G. Csako, T. L. Eggerman, and A. P. Patterson. 2003. Binding and internalization of lipopolysaccharide by Cla-1, a human orthologue of rodent scavenger receptor B1. J. Biol. Chem. 278: 22771-22780. (Pubitemid 36830338)
8. Vishnyakova, T. G., R. Kurlander, A. V. Bocharov, I. N. Baranova, Z. Chen, M. S. Abu-Asab, M. Tsokos, D. Malide, F. Basso, A. Remaley, et al. 2006. CLA-1 and its splicing variant CLA-2 mediate bacterial adhesion and cytosolic bacterial invasion in mammalian cells. Proc. Natl. Acad. Sci. USA. 103: 16888-16893. (Pubitemid 44737348)
9. Cai, L., A. Ji, F. C. de Beer, L. R. Tannock, and D. R. van der Westhuyzen. 2008. SR-BI protects against endotoxemia in mice through its roles in glucocorticoid production and hepatic clearance. J. Clin. Invest. 118: 364-375.
10. Li, X. A., L. Guo, R. Asmis, M. Nikolova-Karakashian, and E. J. Smart. 2006. Scavenger receptor BI prevents nitric oxide-induced cytotoxicity and endotoxin-induced death. Circ. Res. 98: e60-e65.
11. Guo, L., Z. Song, M. Li, Q. Wu, D. Wang, H. Feng, P. Bernard, A. Daugherty, B. Huang, and X. A. Li. 2009. Scavenger receptor BI protects against septic death through its role in modulating inflammatory response. J. Biol. Chem. 284: 19826-19834.
12. Rigotti, A., H. E. Miettinen, and M. Krieger. 2003. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr. Rev. 24: 357-387. (Pubitemid 36724375)
13. Chinetti, G., F. G. Gbaguidi, S. Griglio, Z. Mallat, M. Antonucci, P. Poulain, J. Chapman, J. C. Fruchart, A. Tedgui, J. Najib-Fruchart, et al. 2000. CLA-1/SR-BI is expressed in atherosclerotic lesion macrophages and regulated by activators of peroxisome proliferatoractivated receptors. Circulation. 101: 2411-2417. (Pubitemid 30329133)
14. Ji, Y., B. Jian, N. Wang, Y. Sun, M. L. Moya, M. C. Phillips, G. H. Rothblat, J. B. Swaney, and A. R. Tall. 1997. Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux. J. Biol. Chem. 272: 20982-20985. (Pubitemid 27373951)
15. Yancey, P. G., W. G. Jerome, H. Yu, E. E. Griffin, B. E. Cox, V. R. Babaev, S. Fazio, and M. F. Linton. 2007. Severely altered cholesterol homeostasis in macrophages lacking apoE and SR-BI. J. Lipid Res. 48: 1140-1149. (Pubitemid 46708681)
16. Ji, A., J. M. Meyer, L. Cai, A. Akinmusire, M. C. de Beer, N. R. Webb, and D. R. van der Westhuyzen. 2011. Scavenger receptor SR-BI in macrophage lipid metabolism. Atherosclerosis. 217: 106-112.
17. Covey, S. D., M. Krieger, W. Wang, M. Penman, and B. L. Trigatti. 2003. Scavenger receptor class B type I-mediated protection against atherosclerosis in LDL receptor-negative mice involves its expression in bone marrow-derived cells. Arterioscler. Thromb. Vasc. Biol. 23: 1589-1594. (Pubitemid 37108202)
18. Van Eck, M., I. S. Bos, R. B. Hildebrand, B. T. Van Rij, and T. J. Van Berkel. 2004. Dual role for scavenger receptor class B, type I on bone marrow-derived cells in atherosclerotic lesion development. Am. J. Pathol. 165: 785-794. (Pubitemid 39129286)
19. Zhang, W., P. G. Yancey, Y. R. Su, V. R. Babaev, Y. Zhang, S. Fazio, and M. F. Linton. 2003. Inactivation of macrophage scavenger receptor class B type I promotes atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation. 108: 2258-2263. (Pubitemid 37363044)
20. 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.
21. Yvan-Charvet, L., C. Welch, T. A. Pagler, M. Ranalletta, M. Lamkanfi, S. Han, M. Ishibashi, R. Li, N. Wang, and A. R. Tall. 2008. Increased inflammatory gene expression in ABC transporter-deficient macrophages: free cholesterol accumulation, increased signaling via toll-like receptors, and neutrophil infiltration of atherosclerotic lesions. Circulation. 118: 1837-1847.
22. Rigotti, A., B. L. Trigatti, M. Penman, H. Rayburn, J. Herz, and M. Krieger. 1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role in HDL metabolism. Proc. Natl. Acad. Sci. USA. 94: 12610-12615. (Pubitemid 27492576)
23. Huang, Z. H., and T. Mazzone. 2002. ApoE-dependent sterol efflux from macrophages is modulated by scavenger receptor class B type I expression. J. Lipid Res. 43: 375-382. (Pubitemid 34252267)
24. King, V. L., S. J. Szilvassy, and A. Daugherty. 2002. Interleukin-4 deficiency decreases atherosclerotic lesion formation in a site-specific manner in female LDL receptor -/- mice. Arterioscler. Thromb. Vasc. Biol. 22: 456-461. (Pubitemid 34218754)
25. Powers, K. A., K. Szaszi, R. G. Khadaroo, P. S. Tawadros, J. C. Marshall, A. Kapus, and O. D. Rotstein. 2006. Oxidative stress generated by hemorrhagic shock recruits Toll-like receptor 4 to the plasma membrane in macrophages. J. Exp. Med. 203: 1951-1961. (Pubitemid 44188469)
26. Collins, T. J. 2007. ImageJ for microscopy. Biotechniques. 43: 25-30.
27. Koseki, M., K. Hirano, D. Masuda, C. Ikegami, M. Tanaka, A. Ota, J. C. Sandoval, Y. Nakagawa-Toyama, S. B. Sato, T. Kobayashi, et al. 2007. Increased lipid rafts and accelerated lipopolysaccharide-induced tumor necrosis factor-alpha secretion in Abca1-deficient macrophages. J. Lipid Res. 48: 299-306. (Pubitemid 46220596)
28. Hoebe, K., P. Georgel, S. Rutschmann, X. Du, S. Mudd, K. Crozat, S. Sovath, L. Shamel, T. Hartung, U. Zahringer, et al. 2005. CD36 is a sensor of diacylglycerides. Nature. 433: 523-527. (Pubitemid 40204309)
29. Stuart, L. M., J. Deng, J. M. Silver, K. Takahashi, A. A. Tseng, E. J. Hennessy, R. A. Ezekowitz, and K. J. Moore. 2005. Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain. J. Cell Biol. 170: 477-485. (Pubitemid 41126946)
30. 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.
31. Mukhopadhyay, S., A. Varin, Y. Chen, B. Liu, K. Tryggvason, and S. Gordon. 2011. SR-A/MARCO-mediated ligand delivery enhances intracellular TLR and NLR function, but ligand scavenging from cell surface limits TLR4 response to pathogens. Blood. 117: 1319-1328.
32. Al-Jarallah, A., and B. L. Trigatti. 2010. A role for the scavenger receptor, class B type I in high density lipoprotein dependent activation of cellular signaling pathways. Biochim. Biophys. Acta. 1801: 1239-1248.
33. Saddar, S., C. Mineo, and P. W. Shaul. 2010. Signaling by the high-affinity HDL receptor scavenger receptor B type I. Arterioscler. Thromb. Vasc. Biol. 30: 144-150.
34. Yuhanna, I. S., Y. Zhu, B. E. Cox, L. D. Hahner, S. Osborne-Lawrence, P. Lu, Y. L. Marcel, R. G. Anderson, M. E. Mendelsohn, H. H. Hobbs, et al. 2001. High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 7: 853-857. (Pubitemid 32691642)
35. Zhu, W., S. Saddar, D. Seetharam, K. L. Chambliss, C. Longoria, D. L. Silver, I. S. Yuhanna, P. W. Shaul, and C. Mineo. 2008. The scavenger receptor class B type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ. Res. 102: 480-487. (Pubitemid 351651102)
36. Zhang, Y., A. M. Ahmed, N. McFarlane, C. Capone, D. R. Boreham, R. Truant, S. A. Igdoura, and B. L. Trigatti. 2007. Regulation of SR-BI-mediated selective lipid uptake in Chinese hamster ovary-derived cells by protein kinase signaling pathways. J. Lipid Res. 48: 405-416. (Pubitemid 46220607)
37. Kimura, T., H. Tomura, C. Mogi, A. Kuwabara, A. Damirin, T. Ishizuka, A. Sekiguchi, M. Ishiwara, D. S. Im, K. Sato, et al. 2006. Role of scavenger receptor class B type I and sphingosine 1-phosphate receptors in high density lipoprotein-induced inhibition of adhesion molecule expression in endothelial cells. J. Biol. Chem. 281: 37457-37467. (Pubitemid 46042049)
38. Li, Y., R. F. Schwabe, T. DeVries-Seimon, P. M. Yao, M. C. Gerbod-Giannone, A. R. Tall, R. J. Davis, R. Flavell, D. A. Brenner, and I. Tabas. 2005. Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-alpha and interleukin-6: model of NF-kappaB- and map kinase-dependent inflammation in advanced atherosclerosis. J. Biol. Chem. 280: 21763-21772. (Pubitemid 40827824)
39. Van Eck, M., M. Pennings, M. Hoekstra, R. Out, and T. J. Van Berkel. 2005. Scavenger receptor BI and ATP-binding cassette transporter A1 in reverse cholesterol transport and atherosclerosis. Curr. Opin. Lipidol. 16: 307-315. (Pubitemid 40839760)
40. Huby, T., C. Doucet, C. Dachet, B. Ouzilleau, Y. Ueda, V. Afzal, E. Rubin, M. J. Chapman, and P. Lesnik. 2006. Knockdown expression and hepatic deficiency reveal an atheroprotective role for SR-BI in liver and peripheral tissues. J. Clin. Invest. 116: 2767-2776. (Pubitemid 44511640)
41. Hildebrand, R. B., B. Lammers, I. Meurs, S. J. Korporaal, W. De Haan, Y. Zhao, J. K. Kruijt, D. Pratico, A. W. Schimmel, A. G. Holleboom, et al. 2010. Restoration of high-density lipoprotein levels by cholesteryl ester transfer protein expression in scavenger receptor class B type I (SR-BI) knockout mice does not normalize pathologies associated with SR-BI deficiency. Arterioscler. Thromb. Vasc. Biol. 30: 1439-1445.
42. El Bouhassani, M., S. Gilibert, M. Moreau, F. Saint-Charles, M. Treguier, F. Poti, M. J. Chapman, W. Le Goff, P. Lesnik, and T. Huby. 2011. Cholesteryl ester transfer protein expression partially attenuates the adverse effects of SR-BI receptor deficiency on cholesterol metabolism and atherosclerosis. J. Biol. Chem. 286: 17227-17238.