Noncanonical role of the PDZ4 domain of the adaptor protein PDZK1 in the regulation of the hepatic high density lipoprotein receptor scavenger receptor class B, type i (SR-BI)

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19845-19860

  Tsukamoto, Kosuke ^a   Wales, Thomas E ^b   Daniels, Kathleen ^c   Pal, Rinku ^c   Sheng, Ren ^d   Cho, Wonhwa ^d   Stafford, Walter ^e   Engen, John R ^b   Krieger, Monty ^a   Kocher, Olivier ^c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b NORTHEASTERN UNIVERSITY   (United States)

^c BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^d UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^e BOSTON BIOMEDICAL RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTICAL ULTRACENTRIFUGATION; CELL SURFACE MEMBRANE; CONFORMATIONAL CHANGE; CYTOPLASMIC MEMBRANE; HIGH DENSITY LIPOPROTEIN; HYDROGEN-DEUTERIUM EXCHANGE; IMMUNOHISTOCHEMICAL STUDIES; SCAVENGER RECEPTOR;

CELL MEMBRANES; MASS SPECTROMETRY;

PEPTIDES;

ADAPTOR PROTEIN; PDZ PROTEIN; PDZ1 PROTEIN; PDZ2 PROTEIN; PDZ3 PROTEIN; PDZ4 PROTEIN; PROTEIN PDZK1; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; EXPRESSION VECTOR; GENETIC RECOMBINATION; HETEROZYGOSITY; HOMOZYGOSITY; IMMUNOHISTOCHEMISTRY; ISOTHERMAL TITRATION CALORIMETRY; MALE; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; SURFACE PLASMON RESONANCE; ULTRACENTRIFUGATION;

CHOLESTEROL METABOLISM; HIGH DENSITY LIPOPROTEIN (HDL); PROTEIN-PROTEIN INTERACTIONS; RECEPTORS; TRANSGENIC MICE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; CELL MEMBRANE; CELLS, CULTURED; DEUTERIUM EXCHANGE MEASUREMENT; HEPATOCYTES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MUTATION, MISSENSE; PDZ DOMAINS; PROTEIN BINDING; SCAVENGER RECEPTORS, CLASS B; SEQUENCE DELETION; SURFACE PLASMON RESONANCE;

EID: 84880062754     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.460170     Document Type: Article

References (55)

1. Pawson, T., and Nash, P. (2003) Assembly of cell regulatory systems through protein interaction domains. Science 300, 445-452
2. Kocher, O., and Krieger, M. (2009) Role of the adaptor protein PDZK1 in controlling the HDL receptor SR-BI. Curr. Opin. Lipidol. 20, 236-241
3. van Ham, M., and Hendriks, W. (2003) PDZ domains-glue and guide. Mol. Biol. Rep. 30, 69-82
4. Doyle, D. A., Lee, A., Lewis, J., Kim, E., Sheng, M., and MacKinnon, R. (1996) Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 85, 1067-1076
5. Kocher, O., Comella, N., Tognazzi, K., and Brown, L. F. (1998) Identification and partial characterization of PDZK1: a novel protein containing PDZ interaction domains. Lab. Invest. 78, 117-125
6. Yesilaltay, A., Kocher, O., Rigotti, A., and Krieger, M. (2005) Regulation of SR-BI-mediated high-density lipoprotein metabolism by the tissue-specific adaptor protein PDZK1. Curr. Opin. Lipidol. 16, 147-152
7. Ikemoto, M., Arai, H., Feng, D., Tanaka, K., Aoki, J., Dohmae, N., Takio, K., Adachi, H., Tsujimoto, M., and Inoue, K. (2000) Identification of a PDZdomain-containing protein that interacts with the scavenger receptor class B type I. Proc. Natl. Acad. Sci. U.S.A. 97, 6538-6543
8. Kocher, O., Yesilaltay, A., Cirovic, C., Pal, R., Rigotti, A., and Krieger, M. (2003) Targeted disruption of the PDZK1 gene in mice causes tissuespecific depletion of the high density lipoprotein receptor scavenger receptor class B type I and altered lipoprotein metabolism. J. Biol. Chem. 278, 52820-52825
9. Nakamura, T., Shibata, N., Nishimoto-Shibata, T., Feng, D., Ikemoto, M., Motojima, K., Iso-O, N., Tsukamoto, K., Tsujimoto, M., and Arai, H. (2005) Regulation of SR-BI protein levels by phosphorylation of its associated protein, PDZK1. Proc. Natl. Acad. Sci. U.S.A. 102, 13404-13409
10. Rigotti, A., Miettinen, H. E., and Krieger, M. (2003) The role of the highdensity lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr. Rev. 24, 357-387
11. 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
12. Morrison, J. R., Silvestre, M. J., and Pittman, R. C. (1994) Cholesteryl ester transfer between high density lipoprotein and phospholipid bilayers. J. Biol. Chem. 269, 13911-13918
13. Rigotti, A., Trigatti, B. L., Penman, M., Rayburn, H., Herz, J., and Krieger, M. (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. U.S.A. 94, 12610-12615
14. Plump, A. S., Smith, J. D., Hayek, T., Aalto-Setälä, K., Walsh, A., Verstuyft, J. G., Rubin, E. M., and Breslow, J. L. (1992) Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71, 343-353
15. Zhang, S. H., Reddick, R. L., Piedrahita, J. A., and Maeda, N. (1992) Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258, 468-471
16. 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
17. Trigatti, B., Rayburn, H., Viñals, 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
18. Kocher, O., Birrane, G., Tsukamoto, K., Fenske, S., Yesilaltay, A., Pal, R., Daniels, K., Ladias, J. A., and Krieger, M. (2010) In vitro and in vivo analysis of the binding of the C terminus of the HDL receptor scavenger receptor class B, type I (SR-BI), to the PDZ1 domain of its adaptor protein PDZK1. J. Biol. Chem. 285, 34999-35010
19. Kocher, O., Birrane, G., Yesilaltay, A., Shechter, S., Pal, R., Daniels, K., and Krieger, M. (2011) Identification of the PDZ3 domain of the adaptor protein PDZK1 as a second, physiologically functional binding site for the C terminus of the high density lipoprotein receptor scavenger receptor class B type I. J. Biol. Chem. 286, 25171-25186
20. Pawson, T., and Scott, J. D. (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080
21. Kocher, O., Yesilaltay, A., Shen, C. H., Zhang, S., Daniels, K., Pal, R., Chen, J., and Krieger, M. (2008) Influence of PDZK1 on lipoprotein metabolism and atherosclerosis. Biochim. Biophys. Acta 1782, 310-316
22. Zhu, W., Saddar, S., Seetharam, D., Chambliss, K. L., Longoria, C., Silver, D. L., Yuhanna, I. S., Shaul, P. W., and Mineo, C. (2008) The scavenger receptor class B type I adaptor protein PDZK1 maintains endothelial monolayer integrity. Circ. Res. 102, 480-487
23. Fenske, S. A., Yesilaltay, A., Pal, R., Daniels, K., Barker, C., Quiñones, V., Rigotti, A., Krieger, M., and Kocher, O. (2009) Normal hepatic cell surface localization of the high density lipoprotein receptor, scavenger receptor class B, type I, depends on all four PDZ domains of PDZK1. J. Biol. Chem. 284, 5797-5806
24. Fenske, S. A., Yesilaltay, A., Pal, R., Daniels, K., Rigotti, A., Krieger, M., and Kocher, O. (2008) Overexpression of the PDZ1 domain of PDZK1 blocks the activity of hepatic scavenger receptor, class B, type I by altering its abundance and cellular localization. J. Biol. Chem. 283, 22097-22104
25. Simonet, W. S., Bucay, N., Lauer, S. J., and Taylor, J. M. (1993) A fardownstream hepatocyte-specific control region directs expression of the linked human apolipoprotein E and C-I genes in transgenic mice. J. Biol. Chem. 268, 8221-8229
26. Stafford, W. (1994) Methods in Enzymology, Numerical computer methods, Part B, pp. 478-501, Academic Press, Orlando
27. Stafford, W. (2000) Analysis of reversibly interacting macromolecular systems by time derivative sedimentation velocity. Methods Enzymol. 323, 302-325
28. Stafford, W. F., and Sherwood, P. J. (2004) Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants. Biophys. Chem. 108, 231-243
29. Stafford, W. F. (1992) Boundary analysis in sedimentation transport experiments: a procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile. Anal. Biochem. 203, 295-301
30. Wales, T. E., Fadgen, K. E., Gerhardt, G. C., and Engen, J. R. (2008) Highspeed and high-resolution UPLC separation at zero degrees Celsius. Anal Chem. 80, 6815-6820
31. Houde, D., Berkowitz, S. A., and Engen, J. R. (2011) The utility of hydrogen/deuterium exchange mass spectrometry in biopharmaceutical comparability studies. J. Pharm. Sci. 100, 2071-2086
32. Iacob, R. E., and Engen, J. R. (2012) Hydrogen exchange mass spectrometry: are we out of the quicksand? J. Am. Soc. Mass Spectrom. 23, 1003-1010
33. Iacob, R. E., Pene-Dumitrescu, T., Zhang, J., Gray, N. S., Smithgall, T. E., and Engen, J. R. (2009) Conformational disturbance in Abl kinase upon mutation and deregulation. Proc. Natl. Acad. Sci. U.S.A. 106, 1386-1391
34. Wales, T. E., and Engen, J. R. (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom. Rev. 25, 158-170
35. Zhang, Z., and Smith, D. (1993) Determination of amide hydrogen exchange by mass spectrometry: a new tool for protein structure elucidation. Protein Sci. 2, 522-531
36. Chen, Y., Sheng, R., Källberg, M., Silkov, A., Tun, M. P., Bhardwaj, N., Kurilova, S., Hall, R. A., Honig, B., Lu, H., and Cho, W. (2012) Genomewide functional annotation of dual-specificity protein-and lipid-binding modules that regulate protein interactions. Mol. Cell 46, 226-237
37. Stahelin, R. V., and Cho, W. (2001) Differential roles of ionic, aliphatic, and aromatic residues in membrane-protein interactions: a surface plasmon resonance study on phospholipases A2. Biochemistry 40, 4672-4678
38. Kocher, O., Pal, R., Roberts, M., Cirovic, C., and Gilchrist, A. (2003) Targeted disruption of the PDZK1 gene by homologous recombination. Mol. Cell. Biol. 23, 1175-1180
39. Palmiter, R. D., and Brinster, R. L. (1986) Germ-line transformation of mice. Annu. Rev. Genet. 20, 465-499
40. Guo, Q., Penman, M., Trigatti, B. L., and Krieger, M. (1996) A single point mutation in epsilon-COP results in temperature-sensitive, lethal defects in membrane transport in a Chinese hamster ovary cell mutant. J. Biol. Chem. 271, 11191-11196
41. Yesilaltay, A., Kocher, O., Pal, R., Leiva, A., Quiñones, V., Rigotti, A., and Krieger, M. (2006) PDZK1 is required for maintaining hepatic scavenger receptor, class B, type I (SR-BI) steady state levels but not its surface localization or function. J. Biol. Chem. 281, 28975-28980
42. Stiffler, M. A., Chen, J. R., Grantcharova, V. P., Lei, Y., Fuchs, D., Allen, J. E., Zaslavskaia, L. A., and MacBeath, G. (2007) PDZ domain binding selectivity is optimized across the mouse proteome. Science 317, 364-369
43. Fanning, A. S., Lye, M. F., Anderson, J. M., and Lavie, A. (2007) Domain swapping within PDZ2 is responsible for dimerization of ZO proteins. J. Biol. Chem. 282, 37710-37716
44. Im, Y. J., Lee, J. H., Park, S. H., Park, S. J., Rho, S. H., Kang, G. B., Kim, E., and Eom, S. H. (2003) Crystal structure of the Shank PDZ-ligand complex reveals a class I PDZ interaction and a novel PDZ-PDZ dimerization. J. Biol. Chem. 278, 48099-48104
45. Im, Y. J., Park, S. H., Rho, S. H., Lee, J. H., Kang, G. B., Sheng, M., Kim, E., and Eom, S. H. (2003) Crystal structure of GRIP1 PDZ6-peptide complex reveals the structural basis for class II PDZ target recognition and PDZ domain-mediated multimerization. J. Biol. Chem. 278, 8501-8507
46. Kocher, O., Comella, N., Gilchrist, A., Pal, R., Tognazzi, K., Brown, L. F., and Knoll, J. H. (1999) PDZK1, a novel PDZ domain-containing protein up-regulated in carcinomas and mapped to chromosome 1q21, interacts with cMOAT (MRP2), the multidrug resistance-associated protein. Lab. Invest. 79, 1161-1170
47. LaLonde, D. P., and Bretscher, A. (2009) The scaffold protein PDZK1 undergoes a head-to-tail intramolecular association that negatively regulates its interaction with EBP50. Biochemistry 48, 2261-2271
48. Zimmermann, P. (2006) The prevalence and significance of PDZ domainphosphoinositide interactions. Biochim. Biophys. Acta 1761, 947-956
49. Feng, W., and Zhang, M. (2009) Organization and dynamics of PDZdomain-related supramodules in the postsynaptic density. Nat. Rev. Neurosci. 10, 87-99
50. Stahelin, R. V., Long, F., Peter, B. J., Murray, D., De Camilli, P., McMahon, H. T., and Cho, W. (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J. Biol. Chem. 278, 28993-28999
51. Mineo, C., and Shaul, P. (2012) Functions of scavenger receptor class B, type I in atherosclerosis. Curr. Opin. Lipidol. 23, 487-493
52. Thomson, R. B., Wang, T., Thomson, B. R., Tarrats, L., Girardi, A., Mentone, S., Soleimani, M., Kocher, O., and Aronson, P. S. (2005) Role of PDZK1 in membrane expression of renal brush border ion exchangers. Proc. Natl. Acad. Sci. U.S.A. 102, 13331-13336
53. Wang, P., Wang, J. J., Xiao, Y., Murray, J. W., Novikoff, P. M., Angeletti, R. H., Orr, G. A., Lan, D., Silver, D. L., and Wolkoff, A. W. (2005) Interaction with PDZK1 is required for expression of organic anion transporting protein 1A1 on the hepatocyte surface. J. Biol. Chem. 280, 30143-30149
54. Wang, S., Yue, H., Derin, R. B., Guggino, W. B., and Li, M. (2000) Accessory protein facilitated CFTR-CFTR interaction, a molecular mechanism to potentiate the chloride channel activity. Cell 103, 169-179
55. Kavan, D., and Man, P. (2011) MSTools-Web-based application for visualization and presentation of HXMS data. Int. J. Mass Spectrom. 302, 53-58