Tryptophan 415 Is Critical for the Cholesterol Transport Functions of Scavenger Receptor BI

Biochemistry

Volumn 55, Issue 1, 2016, Pages 103-113

  Holme, Rebecca L ^a   Miller, James J ^a   Nicholson, Kay ^a   Sahoo, Daisy ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; ENZYME ACTIVITY; RESTORATION;

CELL SURFACE EXPRESSION; CHOLESTEROL OXIDASE; CHOLESTEROL TRANSPORT; CHOLESTERYL ESTERS; DESIGNED EXPERIMENTS; FREE CHOLESTEROLS; HIGH-DENSITY LIPOPROTEINS; SCAVENGER RECEPTOR;

CHOLESTEROL;

CHOLESTEROL; CHOLESTEROL ESTER; CHOLESTEROL OXIDASE; HIGH DENSITY LIPOPROTEIN; PHENYLALANINE; SCAVENGER RECEPTOR BI; TRYPTOPHAN 415; TRYPTOPHAN DERIVATIVE; UNCLASSIFIED DRUG; PROTEIN BINDING; SCARB1 PROTEIN, MOUSE; SCAVENGER RECEPTOR B; TRYPTOPHAN;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CHEMICAL BOND; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; COS 7 CELL LINE; HUMAN; HYPOTHESIS; LOSS OF FUNCTION MUTATION; MEDIATOR RELEASE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; SITE DIRECTED MUTAGENESIS; WILD TYPE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; GENETICS; METABOLISM; MUTATION; PROTEIN MULTIMERIZATION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CERCOPITHECUS AETHIOPS; CHOLESTEROL; COS CELLS; LIPOPROTEINS, HDL; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; SCAVENGER RECEPTORS, CLASS B; TRYPTOPHAN;

EID: 84954457161     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00804     Document Type: Article

References (56)

1. Glomset, J. A. (1968) The plasma lecithins:cholesterol acyltransferase reaction J. Lipid. Res. 9, 155-167
2. Ji, Y., Wang, N., Ramakrishnan, R., Sehayek, E., Huszar, D., Breslow, J. L., and Tall, A. R. (1999) Hepatic scavenger receptor BI promotes rapid clearance of high density lipoprotein free cholesterol and its transport into bile J. Biol. Chem. 274, 33398-33402 10.1074/jbc.274.47.33398
3. Glass, C. K. and Witztum, J. L. (2001) Atherosclerosis. the road ahead Cell 104, 503-516 10.1016/S0092-8674(01)00238-0
4. Acton, S., Rigotti, A., Landschulz, K. T., Xu, S., Hobbs, H. H., and Krieger, M. (1996) Identification of scavenger receptor SR-BI as a high density lipoprotein receptor Science 271, 518-520 10.1126/science.271.5248.518
5. Ueda, Y., Royer, L., Gong, E., Zhang, J., Cooper, P. N., Francone, O., and Rubin, E. M. (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 10.1074/jbc.274.11.7165
6. Ueda, Y., Gong, E., Royer, L., Cooper, P. N., Francone, O. L., and Rubin, E. M. (2000) Relationship between expression levels and atherogenesis in scavenger receptor class B, type I transgenics J. Biol. Chem. 275, 20368-20373 10.1074/jbc.M000730200
7. Kozarsky, K. F., Donahee, M. H., Rigotti, A., Iqbal, S. N., Edelman, E. R., and Krieger, M. (1997) Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels Nature 387, 414-417 10.1038/387414a0
8. Trigatti, B., Rayburn, H., Vinals, M., Braun, A., Miettinen, H., Penman, M., Hertz, M., Schrenzel, M., Amigo, L., Rigotti, A., and Krieger, M. (1999) Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology Proc. Natl. Acad. Sci. U. S. A. 96, 9322-9327 10.1073/pnas.96.16.9322
9. Braun, A., Trigatti, B. L., Post, M. J., Sato, K., Simons, M., Edelberg, J. M., Rosenberg, R. D., Schrenzel, M., and Krieger, M. (2002) 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 10.1161/hh0302.104462
10. Covey, S. D., Krieger, M., Wang, W., Penman, M., and Trigatti, B. L. (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 10.1161/01.ATV.0000083343.19940.A0
11. Brunham, L. R., Tietjen, I., Bochem, A. E., Singaraja, R. R., Franchini, P. L., Radomski, C., Mattice, M., Legendre, A., Hovingh, G. K., Kastelein, J. J., and Hayden, M. R. (2011) Novel mutations in scavenger receptor BI associated with high HDL cholesterol in humans Clin. Genet. 79, 575-581 10.1111/j.1399-0004.2011.01682.x
12. Vergeer, M., Korporaal, S. J., Franssen, R., Meurs, I., Out, R., Hovingh, G. K., Hoekstra, M., Sierts, J. A., Dallinga-Thie, G. M., Motazacker, M. M., Holleboom, A. G., Van Berkel, T. J., Kastelein, J. J., Van Eck, M., and Kuivenhoven, J. A. (2011) Genetic variant of the scavenger receptor BI in humans N. Engl. J. Med. 364, 136-145 10.1056/NEJMoa0907687
13. Chadwick, A. C. and Sahoo, D. (2012) Functional characterization of newly-discovered mutations in human SR-BI PLoS One 7, e45660 10.1371/journal.pone.0045660
14. Krieger, M. (1999) Charting the fate of the "good cholesterol": identification and characterization of the high-density lipoprotein receptor SR-BI Annu. Rev. Biochem. 68, 523-558 10.1146/annurev.biochem.68.1.523
15. Connelly, M. A., de la Llera-Moya, M., Monzo, P., Yancey, P. G., Drazul, D., Stoudt, G., Fournier, N., Klein, S. M., Rothblat, G. H., and Williams, D. L. (2001) Analysis of chimeric receptors shows that multiple distinct functional activities of scavenger receptor, class B, type I (SR-BI), are localized to the extracellular receptor domain Biochemistry 40, 5249-5259 10.1021/bi002825r
16. Temel, R. E., Trigatti, B., DeMattos, R. B., Azhar, S., Krieger, M., and Williams, D. L. (1997) Scavenger receptor class B, type I (SR-BI) is the major route for the delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells Proc. Natl. Acad. Sci. U. S. A. 94, 13600-13605 10.1073/pnas.94.25.13600
17. Connelly, M. A., Klein, S. M., Azhar, S., Abumrad, N. A., and Williams, D. L. (1999) Comparison of class B scavenger receptors, CD36 and scavenger receptor BI (SR-BI), shows that both receptors mediate high density lipoprotein-cholesteryl ester selective uptake but SR-BI exhibits a unique enhancement of cholesteryl ester uptake J. Biol. Chem. 274, 41-47 10.1074/jbc.274.1.41
18. Gu, X., Trigatti, B., Xu, S., Acton, S., Babitt, J., and Krieger, M. (1998) The efficient cellular uptake of high density lipoprotein lipids via scavenger receptor class B type I requires not only receptor-mediated surface binding but also receptor-specific lipid transfer mediated by its extracellular domain J. Biol. Chem. 273, 26338-26348 10.1074/jbc.273.41.26338
19. Connelly, M. A., De La Llera-Moya, M., Peng, Y., Drazul-Schrader, D., Rothblat, G. H., and Williams, D. L. (2003) Separation of lipid transport functions by mutations in the extracellular domain of scavenger receptor class B, type I J. Biol. Chem. 278, 25773-25782 10.1074/jbc.M302820200
20. Pittman, R. C., Knecht, T. P., Rosenbaum, M. S., and Taylor, C. A., Jr. (1987) A nonendocytotic mechanism for the selective uptake of high density lipoprotein-associated cholesterol esters J. Biol. Chem. 262, 2443-2450
21. Liu, T., Krieger, M., Kan, H. Y., and Zannis, V. I. (2002) The effects of mutations in helices 4 and 6 of ApoA-I on scavenger receptor class B type I (SR-BI)-mediated cholesterol efflux suggest that formation of a productive complex between reconstituted high density lipoprotein and SR-BI is required for efficient lipid transport J. Biol. Chem. 277, 21576-21584 10.1074/jbc.M112103200
22. Sahoo, D., Darlington, Y. F., Pop, D., Williams, D. L., and Connelly, M. A. (2007) Scavenger receptor class B Type I (SR-BI) assembles into detergent-sensitive dimers and tetramers Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 1771, 807-817 10.1016/j.bbalip.2006.03.003
23. Sahoo, D., Peng, Y., Smith, J. R., Darlington, Y. F., and Connelly, M. A. (2007) Scavenger receptor class B, type I (SR-BI) homo-dimerizes via its C-terminal region: fluorescence resonance energy transfer analysis Biochim. Biophys. Acta, Mol. Cell Biol. Lipids 1771, 818-829 10.1016/j.bbalip.2007.04.019
24. Rodrigueza, W. V., Thuahnai, S. T., Temel, R. E., Lund-Katz, S., Phillips, M. C., and Williams, D. L. (1999) Mechanism of scavenger receptor class B type I-mediated selective uptake of cholesteryl esters from high density lipoprotein to adrenal cells J. Biol. Chem. 274, 20344-20350 10.1074/jbc.274.29.20344
25. Yu, M., Lau, T. Y., Carr, S. A., and Krieger, M. (2012) Contributions of a disulfide bond and a reduced cysteine side chain to the intrinsic activity of the high-density lipoprotein receptor SR-BI Biochemistry 51, 10044-10055 10.1021/bi301203x
26. Papale, G. A., Hanson, P. J., and Sahoo, D. (2011) Extracellular disulfide bonds support scavenger receptor class B type I-mediated cholesterol transport Biochemistry 50, 6245-6454 10.1021/bi2005625
27. Papale, G. A., Nicholson, K., Hanson, P. J., Pavlovic, M., Drover, V. A., and Sahoo, D. (2010) Extracellular hydrophobic regions in scavenger receptor BI play a key role in mediating HDL-cholesterol transport Arch. Biochem. Biophys. 496, 132-139 10.1016/j.abb.2010.02.011
28. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent J. Biol. Chem. 193, 265-275
29. Peng, Y., Akmentin, W., Connelly, M. A., Lund-Katz, S., Phillips, M. C., and Williams, D. L. (2003) Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein Mol. Biol. Cell 15, 384-396 10.1091/mbc.E03-06-0445
30. de la Llera-Moya, M., Rothblat, G. H., Connelly, M. A., Kellner-Weibel, G., Sakr, S. W., Phillips, M. C., and Williams, D. L. (1999) Scavenger receptor BI (SR-BI) mediates free cholesterol flux independently of HDL tethering to the cell surface J. Lipid Res. 40, 575-580
31. Ji, Y., Jian, B., Wang, N., Sun, Y., Moya, M. L., Phillips, M. C., Rothblat, G. H., Swaney, J. B., and Tall, A. R. (1997) Scavenger receptor BI promotes high density lipoprotein-mediated cellular cholesterol efflux J. Biol. Chem. 272, 20982-20985 10.1074/jbc.272.34.20982
32. Jian, B., de la Llera-Moya, M., Ji, Y., Wang, N., Phillips, M. C., Swaney, J. B., Tall, A. R., and Rothblat, G. H. (1998) Scavenger receptor class B type I as a mediator of cellular cholesterol efflux to lipoproteins and phospholipid acceptors J. Biol. Chem. 273, 5599-55606 10.1074/jbc.273.10.5599
33. Kellner-Weibel, G., de La Llera-Moya, M., Connelly, M. A., Stoudt, G., Christian, A. E., Haynes, M. P., Williams, D. L., and Rothblat, G. H. (2000) Expression of scavenger receptor BI in COS-7 cells alters cholesterol content and distribution Biochemistry 39, 221-229 10.1021/bi991666c
34. Reaven, E., Cortez, Y., Leers-Sucheta, S., Nomoto, A., and Azhar, S. (2004) Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues J. Lipid Res. 45, 513-528
35. Ramjeesingh, M., Huan, L. J., Garami, E., and Bear, C. E. (1999) Novel method for evaluation of the oligomeric structure of membrane proteins Biochem. J. 342 (Pt 1) 119-123 10.1042/bj3420119
36. de La Llera-Moya, M., Connelly, M. A., Drazul, D., Klein, S. M., Favari, E., Yancey, P. G., Williams, D. L., and Rothblat, G. H. (2001) Scavenger receptor class B type I affects cholesterol homeostasis by magnifying cholesterol flux between cells and HDL J. Lipid Res. 42, 1969-1978
37. Kartz, G. A., Holme, R. L., Nicholson, K., and Sahoo, D. (2014) SR-BI/CD36 chimeric receptors define extracellular subdomains of SR-BI critical for cholesterol transport Biochemistry 53, 6173-6182 10.1021/bi500706x
38. Parathath, S., Darlington, Y. F., de la Llera Moya, M., Drazul-Schrader, D., Williams, D. L., Phillips, M. C., Rothblat, G. H., and Connelly, M. A. (2007) Effects of amino acid substitutions at glycine 420 on SR-BI cholesterol transport function J. Lipid Res. 48, 1386-1395 10.1194/jlr.M700086-JLR200
39. Gaidukov, L., Nager, A. R., Xu, S., Penman, M., and Krieger, M. (2011) Glycine dimerization motif in the N-terminal transmembrane domain of the high density lipoprotein receptor SR-BI required for normal receptor oligomerization and lipid transport J. Biol. Chem. 286, 18452-18464 10.1074/jbc.M111.229872
40. Russ, W. P. and Engelman, D. M. (2000) The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296, 911-919 10.1006/jmbi.1999.3489
41. Fink, A., Sal-Man, N., Gerber, D., and Shai, Y. (2012) Transmembrane domains interactions within the membrane milieu: principles, advances and challenges Biochim. Biophys. Acta, Biomembr. 1818, 974-983 10.1016/j.bbamem.2011.11.029
42. Connelly, M. A., Parathath, S., Sahoo, D., Darlington, Y. F., Collins, H. L., Rothblat, G. H., and Williams, D. L. (2004) Glycine 420 near the C-terminal transmembrane domain of SR-BI is critical for proper delivery and metabolism of HDL cholesteryl ester Arterioscler. Thromb. Vasc. Biol. 24, E1
43. Parathath, S., Sahoo, D., Darlington, Y. F., Peng, Y., Collins, H. L., Rothblat, G. H., Williams, D. L., and Connelly, M. A. (2004) Glycine 420 near the C-terminal transmembrane domain of SR-BI is critical for proper delivery and metabolism of high density lipoprotein cholesteryl ester J. Biol. Chem. 279, 24976-24985 10.1074/jbc.M402435200
44. Saddar, S., Carriere, V., Lee, W. R., Tanigaki, K., Yuhanna, I. S., Parathath, S., Morel, E., Warrier, M., Sawyer, J. K., Gerard, R. D., Temel, R. E., Brown, J. M., Connelly, M., Mineo, C., and Shaul, P. W. (2013) Scavenger receptor class B type I is a plasma membrane cholesterol sensor Circ. Res. 112, 140-151 10.1161/CIRCRESAHA.112.280081
45. Endemann, G., Stanton, L. W., Madden, K. S., Bryant, C. M., White, R. T., and Protter, A. A. (1993) CD36 is a receptor for oxidized low density lipoprotein J. Biol. Chem. 268, 11811-11816
46. Reczek, D., Schwake, M., Schroder, J., Hughes, H., Blanz, J., Jin, X., Brondyk, W., Van Patten, S., Edmunds, T., and Saftig, P. (2007) LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of beta-glucocerebrosidase Cell 131, 770-783 10.1016/j.cell.2007.10.018
47. Armesilla, A. L. and Vega, M. A. (1994) Structural organization of the gene for human CD36 glycoprotein J. Biol. Chem. 269, 18985-18991
48. Neculai, D., Schwake, M., Ravichandran, M., Zunke, F., Collins, R. F., Peters, J., Neculai, M., Plumb, J., Loppnau, P., Pizarro, J. C., Seitova, A., Trimble, W. S., Saftig, P., Grinstein, S., and Dhe-Paganon, S. (2013) Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36 Nature 504, 172-176 10.1038/nature12684
49. Wu, L., McElheny, D., Takekiyo, T., and Keiderling, T. A. (2010) Geometry and efficacy of cross-strand Trp/Trp, Trp/Tyr, and Tyr/Tyr aromatic interaction in a beta-hairpin peptide Biochemistry 49, 4705-4714 10.1021/bi100491s
50. Vinals, M., Xu, S., Vasile, E., and Krieger, M. (2003) Identification of the N-linked glycosylation sites on the high density lipoprotein (HDL) receptor SR-BI and assessment of their effects on HDL binding and selective lipid uptake J. Biol. Chem. 278, 5325-5332 10.1074/jbc.M211073200
51. de Jesus, A. J. and Allen, T. W. (2013) The role of tryptophan side chains in membrane protein anchoring and hydrophobic mismatch Biochim. Biophys. Acta, Biomembr. 1828, 864-876 10.1016/j.bbamem.2012.09.009
52. Killian, J. A. and von Heijne, G. (2000) How proteins adapt to a membrane-water interface Trends Biochem. Sci. 25, 429-434 10.1016/S0968-0004(00)01626-1
53. Yau, W. M., Wimley, W. C., Gawrisch, K., and White, S. H. (1998) The preference of tryptophan for membrane interfaces Biochemistry 37, 14713-14718 10.1021/bi980809c
54. Gao, X., Zeng, Y., Liu, S., and Wang, S. (2013) Acute stress show great influences on liver function and the expression of hepatic genes associated with lipid metabolism in rats Lipids Health Dis. 12, 118 10.1186/1476-511X-12-118
55. Al-Jarallah, A., Chen, X., Gonzalez, L., and Trigatti, B. L. (2014) High density lipoprotein stimulated migration of macrophages depends on the scavenger receptor class B, type I, PDZK1 and Akt1 and is blocked by sphingosine 1 phosphate receptor antagonists PLoS One 9, e106487 10.1371/journal.pone.0106487
56. Fiser, A. and Sali, A. (2003) Modeller: generation and refinement of homology-based protein structure models Methods Enzymol. 374, 461-491 10.1016/S0076-6879(03)74020-8