Adrenocortical scavenger receptor class B type I deficiency exacerbates endotoxic shock and precipitates sepsis-induced mortality in mice

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 817-826

  Gilibert, Sophie ^a,b,c   Galle Treger, Lauriane ^a,b,c   Moreau, Martine ^a,b,c   Saint Charles, Flora ^a,b,c   Costa, Sara ^a,b,c   Ballaire, Raphaëlle ^a,b,c   Couvert, Philippe ^a,b,c,d   Carrié, Alain ^a,b,c,d   Lesnik, Philippe ^a,b,c,d   Huby, Thierry ^a,b,c,d  

^a INSERM   (France)

^b Université Pierre et Marie Curie 06 Unité Mixte de Recherche S 1166 ^*  (France)

^c Institute of Cardiometabolism and Nutrition   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPOPOLYSACCHARIDE; SCAVENGER RECEPTOR BI;

ACUTE DISEASE; ADRENAL CELL; ADRENAL CORTEX; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; BONE MARROW CELL; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DISEASE EXACERBATION; DISEASE MARKER; DISEASE SEVERITY; ENDOTHELIUM CELL; FEMALE; GENE ACTIVATION; INFLAMMATION; KNOCKOUT MOUSE; LETHALITY; LIPOPROTEIN BLOOD LEVEL; LIVER CELL; MALE; MORTALITY; MOUSE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; SEPSIS; SEPTIC SHOCK; STEROIDOGENESIS; STRESS; SYSTEMIC DISEASE; TISSUE SPECIFICITY;

ADRENAL CORTEX; ANIMALS; CHOLESTEROL, LDL; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GENE EXPRESSION; HEPATOCYTES; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE; MUSCLE, SKELETAL; MYELOID CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCAVENGER RECEPTORS, CLASS B; SEPSIS; SHOCK, SEPTIC; SPLEEN; SURVIVAL ANALYSIS; SURVIVAL RATE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904261696     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303164     Document Type: Article

References (38)

1. Acton, S., A. Rigotti, K. T. Landschulz, S. Xu, H. H. Hobbs, and M. Krieger. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271: 518-520.
2. Ueda, Y., L. Royer, E. Gong, J. Zhang, P. N. Cooper, O. Francone, and E. M. Rubin. 1999. Lower plasma levels and accelerated clearance of high density lipoprotein (HDL) and non-HDL cholesterol in scavenger receptor class B type I transgenic mice. J. Biol. Chem. 274: 7165-7171.
3. 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)
4. 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)
5. Out, R., M. Hoekstra, J. A. Spijkers, J. K. Kruijt, M. van Eck, I. S. Bos, J. Twisk, and T. J. Van Berkel. 2004. Scavenger receptor class B type I is solely responsible for the selective uptake of cholesteryl esters from HDL by the liver and the adrenals in mice. J. Lipid Res. 45: 2088-2095. (Pubitemid 40990903)
6. Vergeer, M., S. J. Korporaal, R. Franssen, I. Meurs, R. Out, G. K. Hovingh, M. Hoekstra, J. A. Sierts, G. M. Dallinga-Thie, M. M. Motazacker, et al. 2011. Genetic variant of the scavenger receptor BI in humans. N. Engl. J. Med. 364: 136-145.
7. 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.
8. 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.
9. 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.
10. 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)
11. 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, and P. W. Shaul. 2001. High-density lipoprotein binding to scavenger receptor-BI activates endothelial nitric oxide synthase. Nat. Med. 7: 853-857. (Pubitemid 32691642)
12. Bocharov, A. V., I. N. Baranova, T. G. Vishnyakova, A. T. Remaley, G. Csako, F. Thomas, A. P. Patterson, and T. L. Eggerman. 2004. Targeting of scavenger receptor class B type I by synthetic amphipathic alpha-helical- containing peptides blocks lipopolysaccharide (LPS) uptake and LPS-induced proinflammatory cytokine responses in THP-1 monocyte cells. J. Biol. Chem. 279: 36072-36082. (Pubitemid 39100615)
13. 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)
14. 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)
15. Watanabe, K., E. K. Shin, M. Hashino, M. Tachibana, and M. Watarai. 2010. Toll-like receptor 2 and class B scavenger receptor type I are required for bacterial uptake by trophoblast giant cells. Mol. Immunol. 47: 1989-1996.
16. Cai, L., Z. Wang, J. M. Meyer, A. Ji, and D. R. van der Westhuyzen. 2012. Macrophage SR-BI regulates LPS-induced pro-inflammatory signaling in mice and isolated macrophages. J. Lipid Res. 53: 1472-1481.
17. Leelahavanichkul, A., A. V. Bocharov, R. Kurlander, I. N. Baranova, T. G. Vishnyakova, A. C. Souza, X. Hu, K. Doi, B. Vaisman, M. Amar, et al. 2012. Class B scavenger receptor types I and II and CD36 targeting improves sepsis survival and acute outcomes in mice. J. Immunol. 188: 2749-2758.
18. El Bouhassani, M., S. Gilibert, M. Moreau, F. Saint-Charles, M. Tréguier, 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.
19. Postic, C., and M. A. Magnuson. 2000. DNA excision in liver by an albumin-Cre transgene occurs progressively with age. Genesis 26: 149-150. (Pubitemid 30158104)
20. Kisanuki, Y. Y., R. E. Hammer, J. Miyazaki, S. C. Williams, J. A. Richardson, and M. Yanagisawa. 2001. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230: 230-242. (Pubitemid 32171420)
21. Bingham, N. C., S. Verma-Kurvari, L. F. Parada, and K. L. Parker. 2006. Development of a steroidogenic factor 1/Cre transgenic mouse line. Genesis 44: 419-424. (Pubitemid 44454047)
22. Pène, F., E. Courtine, F. Ouaaz, B. Zuber, B. Sauneuf, G. Sirgo, C. Rousseau, J. Toubiana, V. Balloy, M. Chignard, et al. 2009. Toll-like receptors 2 and 4 contribute to sepsis-induced depletion of spleen dendritic cells. Infect. Immun. 77: 5651-5658.
23. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
24. Tréguier, M., C. Doucet, M. Moreau, C. Dachet, J. Thillet, M. J. Chapman, and T. Huby. 2004. Transcription factor sterol regulatory element binding protein 2 regulates scavenger receptor Cla-1 gene expression. Arterioscler. Thromb. Vasc. Biol. 24: 2358-2364. (Pubitemid 39658042)
25. -/- mice reveals a role for fractalkine in atherogenesis. J. Clin. Invest. 111: 333-340.
26. Hildebrand, R. B., B. Lammers, I. Meurs, S. J. Korporaal, W. De Haan, Y. Zhao, J. K. Kruijt, D. Praticò, 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.
27. Gomes, A. L., T. Carvalho, J. Serpa, C. Torre, and S. Dias. 2010. Hypercholesterolemia promotes bone marrow cell mobilization by perturbing the SDF-1: CXCR4 axis. Blood 115: 3886-3894.
28. Feng, Y., S. Schouteden, R. Geenens, V. Van Duppen, P. Herijgers, P. Holvoet, P. P. Van Veldhoven, and C. M. Verfaillie. 2012. Hematopoietic stem/progenitor cell proliferation and differentiation is differentially regulated by high-density and low-density lipoproteins in mice. PLoS ONE 7: e47286.
29. Suehiro, J., T. Hamakubo, T. Kodama, W. C. Aird, and T. Minami. 2010. Vascular endothelial growth factor activation of endothelial cells is mediated by early growth response-3. Blood 115: 2520-2532.
30. Aldridge, A. J. 2002. Role of the neutrophil in septic shock and the adult respiratory distress syndrome. Eur. J. Surg. 168: 204-214. (Pubitemid 34879391)
31. Dal Secco, D., J. A. Paron, S. H. de Oliveira, S. H. Ferreira, J. S. Silva, and Q. Cunha Fde. 2003. Neutrophil migration in inflammation: nitric oxide inhibits rolling, adhesion and induces apoptosis. Nitric Oxide 9: 153-164.
32. Schakman, O., S. Kalista, C. Barbé, A. Loumaye, and J. P. Thissen. 2013. Glucocorticoid-induced skeletal muscle atrophy. Int. J. Biochem. Cell Biol. 45: 2163-2172.
33. Li, W., J. S. Moylan, M. A. Chambers, J. Smith, and M. B. Reid. 2009. Interleukin-1 stimulates catabolism in C2C12 myotubes. Am. J. Physiol. Cell Physiol. 297: C706-C714.
34. Li, Y. P., Y. Chen, J. John, J. Moylan, B. Jin, D. L. Mann, and M. B. Reid. 2005. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J. 19: 362-370. (Pubitemid 40316524)
35. Doyle, A., G. Zhang, E. A. Abdel Fattah, N. T. Eissa, and Y. P. Li. 2011. Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways. FASEB J. 25: 99-110.
36. Braun, T. P., X. Zhu, M. Szumowski, G. D. Scott, A. J. Grossberg, P. R. Levasseur, K. Graham, S. Khan, S. Damaraju, W. F. Colmers, et al. 2011. Central nervous system inflammation induces muscle atrophy via activation of the hypothalamic-pituitary-adrenal axis. J. Exp. Med. 208: 2449-2463.
37. Komori, H., H. Arai, T. Kashima, T. Huby, T. Kita, and Y. Ueda. 2008. Coexpression of CLA-1 and human PDZK1 in murine liver modulates HDL cholesterol metabolism. Arterioscler. Thromb. Vasc. Biol. 28: 1298-1303.
38. Teslovich, T. M., K. Musunuru, A. V. Smith, A. C. Edmondson, I. M. Stylianou, M. Koseki, J. P. Pirruccello, S. Ripatti, D. I. Chasman, C. J. Willer, et al. 2010. Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466: 707-713.