Scavenger receptor class B, type I-mediated uptake of A1AT by pulmonary endothelial cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 309, Issue 4, 2015, Pages L425-L434

  Lockett, Angelia D ^a   Petrusca, Daniela N ^a   Justice, Matthew J ^a   Poirier, Christophe ^a   Serban, Karina A ^a   Rush, Natalia I ^a   Kamocka, Malgorzata ^a   Predescu, Dan ^b   Predescu, Sanda ^b   Petrache, Irina ^a,c  

^a INDIANA UNIVERSITY   (United States)

^b RUSH UNIVERSITY   (United States)

^c The Richard L Roudebush Veterans Affairs Medical Center   (India)

Author keywords

Antiproteinase; Cigarette smoke; Lipoprotein; Scavenger receptor; Serpin

Indexed keywords

CIGARETTE SMOKE; COLLOIDAL GOLD; HIGH DENSITY LIPOPROTEIN; LIPOPROTEIN; LOW DENSITY LIPOPROTEIN; NEUTRALIZING ANTIBODY; SCAVENGER RECEPTOR BI; ALPHA 1 ANTITRYPSIN; SCARB1 PROTEIN, HUMAN; SCAVENGER RECEPTOR B;

ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CAPILLARY ENDOTHELIAL CELL; CAVEOLA; CELL MEMBRANE; COATED VESICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENDOCYTOSIS; ENDOTHELIUM CELL; FEMALE; GENE; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LUNG ENDOTHELIUM; MALE; MEMBRANE BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SCARB1 GENE; TRANSMISSION ELECTRON MICROSCOPY; VASCULAR ENDOTHELIUM; WILD TYPE; ANIMAL; BINDING COMPETITION; C57BL MOUSE; CELL CULTURE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; SMOKING;

ALPHA 1-ANTITRYPSIN; ANIMALS; BINDING, COMPETITIVE; CELLS, CULTURED; ENDOCYTOSIS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; SCAVENGER RECEPTORS, CLASS B; SMOKING;

EID: 84939427799     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00376.2014     Document Type: Article

References (55)

1. Acton S, Rigotti A, Landschulz KT, Xu S, Hobbs HH, Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271: 518-520, 1996.
2. Aldonyte R, Hutchinson ET, Jin B, Brantly M, Block E, Patel J, Zhang J. Endothelial alpha-1-antitrypsin attenuates cigarette smoke induced apoptosis in vitro. COPD 5: 153-162, 2008.
3. Arai T, Wang N, Bezouevski M, Welch C, Tall AR. Decreased atherosclerosis in heterozygous low density lipoprotein receptor-deficient mice expressing the scavenger receptor BI transgene. J Biol Chem 274: 2366-2371, 1999.
4. Babitt J, Trigatti B, Rigotti A, Smart EJ, Anderson RG, Xu S, Krieger M. Murine SR-BI, a high density lipoprotein receptor that mediates selective lipid uptake, is N-glycosylated and fatty acylated and colocalizes with plasma membrane caveolae. J Biol Chem 272: 13242-13249, 1997.
5. Braun A, Trigatti BL, Post MJ, Sato K, Simons M, Edelberg JM, Rosenberg RD, Schrenzel M, Krieger M. Loss of SR-BI expression leads to the early onset of occlusive atherosclerotic coronary artery disease, spontaneous myocardial infarctions, severe cardiac dysfunction, and premature death in apolipoprotein E-deficient mice. Circ Res 90: 270-276, 2002.
6. Cirillo DJ, Agrawal Y, Cassano PA. Lipids and pulmonary function in the Third National Health and Nutrition Examination Survey. Am J Epidemiol 155: 842-848, 2002.
7. Cruickshank-Quinn CI, Mahaffey S, Justice MJ, Hughes G, Armstrong M, Bowler RP, Reisdorph R, Petrache I, Reisdorph N. Transient and persistent metabolomic changes in plasma following chronic cigarette smoke exposure in a mouse model. PLoS One 9: 101855, 2014.
8. Dollery CM, Owen CA, Sukhova GK, Krettek A, Shapiro SD, Libby P. Neutrophil elastase in human atherosclerotic plaques: production by macrophages. Circulation 107: 2829-2836, 2003.
9. Eckhardt ER, Cai L, Shetty S, Zhao Z, Szanto A, Webb NR, van der Westhuyzen DR. High density lipoprotein endocytosis by scavenger receptor SR-BII is clathrin-dependent and requires a carboxyl-terminal dileucine motif. J Biol Chem 281: 4348-4353, 2006.
10. Eckhardt ER, Cai L, Sun B, Webb NR, van der Westhuyzen DR. High density lipoprotein uptake by scavenger receptor SR-BII. J Biol Chem 279: 14372-14381, 2004.
11. Feng H, Guo L, Wang D, Gao H, Hou G, Zheng Z, Ai J, Foreman O, Daugherty A, Li XA. Deficiency of SR-BI leads to impaired lymphocyte homeostasis and autoimmune disorders in mice. Arterioscler Thromb Vasc Biol 31: 2543-2551, 2011.
12. Goldstein JL, Ho YK, Basu SK, Brown MS. Binding site on macrophages that mediates uptake and degradation of acetylated low density lipoprotein, producing massive cholesterol deposition. Proc Natl Acad Sci USA 76: 333-337, 1979.
13. Gordon DJ, Rifkind BM. High-density lipoprotein-the clinical implications of recent studies. N Engl J Med 321: 1311-1316, 1989.
14. Gowdy KM, Madenspacher JH, Azzam KM, Gabor KA, Janardhan KS, Aloor JJ, Fessler MB. Key role for scavenger receptor B-I in the integrative physiology of host defense during bacterial pneumonia. Mu-cosal Immunol 8: 559-571, 2015.
15. Hubbard RC, Ogushi F, Fells GA, Cantin AM, Jallat S, Courtney M, Crystal RG. Oxidants spontaneously released by alveolar macrophages of cigarette smokers can inactivate the active site of alpha 1-antitrypsin, rendering it ineffective as an inhibitor of neutrophil elastase. J Clin Invest 80: 1289-1295, 1987.
16. Janciauskiene S, Moraga F, Lindgren S. C-terminal fragment of a1-antitrypsin activates human monocytes to a pro-inflammatory state through interactions with the CD36 scavenger receptor and LDL receptor. Atherosclerosis 158: 41-51, 2001.
17. Kartz GA, Holme RL, Nicholson K, Sahoo D. SR-BI/CD36 chimeric receptors define extracellular subdomains of SR-BI critical for cholesterol transport. Biochemistry 53: 6173-6182, 2014.
18. Krieger M. Scavenger receptor class B type I is a multiligand HDL receptor that influences diverse physiologic systems. J Clin Invest 108: 793-797, 2001.
19. Leclercq A, Houard X, Philippe M, Ollivier V, Sebbag U, Meilhac O, Michel JB. Involvement of intraplaque hemorrhage in atherothrombosis evolution via neutrophil protease enrichment. J Leukoc Biol 82: 1420-1429, 2007.
20. Lockett AD, Brown MB, Santos-Falcon N, Rush NI, Oueini H, Oberle AJ, Bolanis E, Fragoso MA, Petrusca DN, Serban KA, Schweitzer KS, Presson RG Jr, Campos M, Petrache I. Active trafficking of alpha 1 antitrypsin across the lung endothelium. PLoS One 9: 93979, 2014.
21. Lockett AD, Kimani S, Ddungu G, Wrenger S, Tuder RM, Jan-ciauskiene SM, Petrache I. od-Antitrypsin modulates lung endothelial cell inflammatory responses to TNF-o. Am J Respir Cell Mol Biol 49: 143-50, 2013.
22. Lockett AD, Van Demark M, Gu Y, Schweitzer KS, Sigua N, Kamocki K, Fijalkowska I, Garrison J, Fisher AJ, Serban K, Wise RA, Flotte TR, Mueller C, Presson RG Jr, Petrache HI, Tuder RM, Petrache I. Effect of cigarette smoke exposure and structural modifications on the α-1 antitrypsin interaction with caspases. Mol Med 18: 445-454, 2012.
23. Martineau C, Martin-Falstrault L, Brissette L, Moreau R. Gender-and region-specific alterations in bone metabolism in Scarbi-null female mice. J Endocrinol 222: 277-288, 2014.
24. Mashiba S, Wada Y, Takeya M, Sugiyama A, Hamakubo T, Naka-mura A, Noguchi N, Niki E, Izumi A, Kobayashi M, Uchida K, Kodama T. In vivo complex formation of oxidized α 1-antitrypsin and LDL. Arterioscler Thromb Vasc Biol 21: 1801-1808, 2001.
25. Moore KJ, Freeman MW. Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol 26: 1702-1711, 2006.
26. Mulcahy JV, Riddell DR, Owen JS. Human scavenger receptor class B type II (SR-BII) and cellular cholesterol efflux. Biochem J 377: 741-747, 2004.
27. O'Connell BJ, Denis M, Genest J. Cellular physiology of cholesterol efflux in vascular endothelial cells. Circulation 110: 2881-2888, 2004.
28. Ogushi F, Fells GA, Hubbard RC, Straus SD, Crystal RG. Z-type alpha 1-antitrypsin is less competent than M1-type alpha 1-antitrypsin as an inhibitor of neutrophil elastase. J Clin Invest 80: 1366-1374, 1987.
29. Ohar JA, Hamilton RF Jr, Zheng S, Sadeghnejad A, Sterling DA, Xu J, Meyers DA, Bleecker ER, Holian A. COPD is associated with a macrophage scavenger receptor-1 gene sequence variation. Chest 137: 1098-1107, 2010.
30. Ortiz-Munoz G, Houard X, Martin-Ventura JL, Ishida BY, Loyau S, Rossignol P, Moreno JA, Kane JP, Chalkley RJ, Burlingame AL, Michel JB, Meilhac O. HDL antielastase activity prevents smooth muscle cell anoikis, a potential new antiatherogenic property. FASEB J 23: 3129-3139, 2009.
31. Palade GE. A study of fixation for electron microscopy. J Exp Med 95: 285-298, 1952.
32. Petrache I, Fijalkowska I, Medler TR, Skirball J, Cruz P, Zhen L, Petrache HI, Flotte TR, Tuder RM. α-1 Antitrypsin inhibits caspase-3 activity, preventing lung endothelial cell apoptosis. Am J Pathol 169: 1155-1166, 2006.
33. Petrache I, Fijalkowska I, Zhen L, Medler TR, Brown E, Cruz P, Choe KH, Taraseviciene-Stewart L, Scerbavicius R, Shapiro L, Zhang B, Song S, Hicklin D, Voelkel NF, Flotte T, Tuder RM. A novel antiapoptotic role for α 1 antitrypsin in the prevention of pulmonary emphysema. Am J Respir Crit Care Med 173: 1222-1228, 2006.
34. Predescu D, Predescu S, McQuistan T, Palade GE. Transcytosis of alpha1-acidic glycoprotein in the continuous microvascular endothelium. Proc Natl Acad Sci USA 95: 6175-6180, 1998.
35. Rabassa AA, Schwartz MR, Ertan A. Alpha 1-antitrypsin deficiency and chronic pancreatitis. Dig Dis Sci 40: 1997-2001, 1995.
36. Rigotti A, Trigatti B, Babitt J, Penman M, Xu S, Krieger M. Scavenger receptor BI-a cell surface receptor for high density lipoprotein. Curr Opin Lipidol 8: 181-188, 1997.
37. Rigotti A, Trigatti BL, Penman M, Rayburn H, Herz J, Krieger M. 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, 1997.
38. Sandstrom CS, Ohlsson B, Melander O, Westin U, Mahadeva R, Janciauskiene S. An association between type 2 diabetes and alpha-antitrypsin deficiency. Diabet Med 25: 1370-1373, 2008.
39. Shapiro L, Pott GB, Ralston AH. Alpha-1-antitrypsin inhibits human immunodeficiency virus type 1. FASEB J 15: 115-122, 2001.
40. Sohrab S, Petrusca DN, Lockett AD, Schweitzer KS, Rush NI, Gu Y, Kamocki K, Garrison J, Petrache I. Mechanism of α-1 antitrypsin endocytosis by lung endothelium. FASEB J 23: 3149-3158, 2009.
41. Stephen SL, Freestone K, Dunn S, Twigg MW, Homer-Vanniasinkam S, Walker JH, Wheatcroft SB, Ponnambalam S. Scavenger receptors and their potential as therapeutic targets in the treatment of cardiovascular disease. Int J Hypertens 2010: 646929, 2010.
42. Sticozzi C, Belmonte G, Pecorelli A, Arezzini B, Gardi C, Maioli E, Miracco C, Toscano M, Forman HJ, Valacchi G. Cigarette smoke affects keratinocytes SRB1 expression and localization via H2O2 production and HNE protein adducts formation. PLoS One 7: 33592, 2012.
43. Taggart C, Cervantes-Laurean D, Kim G, McElvaney NG, Wehr N, Moss J, Levine RL. Oxidation of either methionine 351 or methionine 358 in α 1-antitrypsin causes loss of anti-neutrophil elastase activity. J Biol Chem 275: 27258-27265, 2000.
44. Tall AR. Plasma high density lipoproteins. Metabolism and relationship to atherogenesis. J Clin Invest 86: 379-384, 1990.
45. Tall AR, Y van-Charv. Cholesterol, inflammation and innate immunity. Nat Rev Immunol 15: 104-116, 2015.
46. Toldo S, Seropian IM, Mezzaroma E, Van Tassell BW, Salloum FN, Lewis EC, Voelkel N, Dinarello CA, Abbate A. Alpha-1 antitrypsin inhibits caspase-1 and protects from acute myocardial ischemia-reperfu-sion injury. J Mol Cell Cardiol 51: 244-251, 2011.
47. Turino GM, Seniorrm Garg BD, Keller S, Levi MM, Mandl I. Serum elastase inhibitor deficiency and alpha 1-antitrypsin deficiency in patients with obstructive emphysema. Science 165: 709-711, 1969.
48. Valacchi G, Davis PA, Khan EM, Lanir R, Maioli E, Pecorelli A, Cross CE, Goldkorn T. Cigarette smoke exposure causes changes in scavenger receptor B1 level and distribution in lung cells. Int J Biochem Cell Biol 43: 1065-1070, 2011.
49. Valacchi G, Vasu VT, Yokohama W, Corbacho AM, Phung A, Lim Y, Aung HH, Cross CE, Davis PA. Lung vitamin E transport processes are affected by both age and environmental oxidants in mice. Toxicol Appl Pharmacol 222: 227-234, 2007.
50. Vergeer M, Korporaal SJA, Franssen R, Meurs I, Out R, Hovingh GK, Hoekstra M, Sierts JA, Dallinga-Thie GM, Motazacker MM, Holleboom AG, Van Berkel TJC, Kastelein JJP, Van Eck M, Kuiv-enhoven JA. Genetic variant of the scavenger receptor BI in humans. N Engl J Med 364: 136-145, 2011.
51. Wang W, Xu H, Shi Y, Nandedkar S, Zhang H, Gao H, Feroah T, Weihrauch D, Schulte ML, Jones DW, Jarzembowski J, Sorci-Thomas M, Pritchard KA Jr. Genetic deletion of apolipoprotein A-I increases airway hyperresponsiveness, inflammation, and collagen deposition in the lung. J Lipid Res 51: 2560-2570, 2010.
52. Yamada Y, Doi T, Hamakubo T, Kodama T. Scavenger receptor family proteins: roles for atherosclerosis, host defence and disorders of the central nervous system. Cell Mol Life Sci 54: 628-640, 1998.
53. Ye J, Liao YT, Jian YQ, Zhang XD, Wei P, Qi H, Deng CY, Li FR. Alpha-1-antitrypsin for the improvement of autoimmunity and allograft rejection in beta cell transplantation. Immunol Lett 150: 61-68, 2013.
54. Yeh YC, Hwang GY, Liu IP, Yang VC. Identification and expression of scavenger receptor SR-BI in endothelial cells and smooth muscle cells of rat aorta in vitro and in vivo. Atherosclerosis 161: 95-103, 2002.
55. Zhang B, Lu Y, Campbell-Thompson M, Spencer T, Wasserfall C, Atkinson M, Song S. α1-Antitrypsin protects ß-cells from apoptosis. Diabetes 56: 1316-1323, 2007.