Affinity and kinetics of proprotein convertase subtilisin/kexin type 9 binding to low-density lipoprotein receptors on HepG2 cells

FEBS Journal

Volumn 278, Issue 16, 2011, Pages 2938-2950

  Mousavi, Seyed A ^a   Berge, Knut E ^a   Berg, Trond ^b   Leren, Trond P ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

association; dissociation; dissociation constants; low density lipoprotein receptor; proprotein convertase subtilisin kexin 9

Indexed keywords

CELLOBIOSE; KEXIN; KEXIN TYPE 9 ENZYME; LOW DENSITY LIPOPROTEIN RECEPTOR; SERINE PROTEINASE; SUBTILISIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL STRAIN HEPG2; CONTROLLED STUDY; DISSOCIATION; ENZYME INHIBITION; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; GAIN OF FUNCTION MUTATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN DEGRADATION; RECEPTOR BINDING;

HEP G2 CELLS; HUMANS; KINETICS; PROTEIN BINDING; RECEPTORS, LDL; SERINE ENDOPEPTIDASES;

EID: 79961027581     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08219.x     Document Type: Article

References (47)

1. Abifadel M, Varret M, Rabes JP, Allard D, Ouguerram K, Devillers M, Cruaud C, Benjannet S, Wickham L, Erlich D, et al. (2003) Mutations in PCSK9 cause autosomal dominant hypercholesterolemia. Nat Genet 34, 154-156. (Pubitemid 36666925)
2. Seidah NG, Benjannet S, Wickham L, Marcinkiewicz J, Jasmin SB, Stifani S, Basak A, Prat A, &, Chretien M, (2003) The secretory proprotein convertase neural apoptosis-regulated convertase 1 (NARC-1): liver regeneration and neuronal differentiation. Proc Natl Acad Sci USA 100, 928-933. (Pubitemid 36183932)
3. Zaid A, Roubtsova A, Essalmani R, Marcinkiewicz J, Chamberland A, Hamelin J, Tremblay M, Jacques H, Jin W, Davignon J, et al. (2008) Proprotein convertase subtilisin/kexin type 9 (PCSK9): hepatocyte-specific low-density lipoprotein receptor degradation and critical role in mouse liver regeneration. Hepatology 48, 646-654.
4. Lagace TA, Curtis DE, Garuti R, McNutt MC, Park SW, Prather HB, Anderson NN, Ho YK, Hammer RE, &, Horton JD, (2006) Secreted PCSK9 decreases the number of LDL receptors in hepatocytes and in livers of parabiotic mice. J Clin Invest 116, 2995-3005. (Pubitemid 44684484)
5. Maxwell KN, &, Breslow JL, (2004) Adenoviral-mediated expression of Pcsk9 in mice results in a low-density lipoprotein receptor knockout phenotype. Proc Natl Acad Sci USA 101, 7100-7105. (Pubitemid 38596449)
6. Park SW, Moon YA, &, Horton JD, (2004) Post-transcriptional regulation of low density lipoprotein receptor protein by proprotein convertase subtilisin/kexin type 9a in mouse liver. J Biol Chem 279, 50630-50638. (Pubitemid 39577880)
7. Grefhorst A, McNutt MC, Lagace TA, &, Horton JD, (2008) Plasma PCSK9 preferentially reduces liver LDL receptors in mice. J Lipid Res 49, 1303-1311.
8. Berge KE, Ose L, &, Leren TP, (2006) Missense mutations in the PCSK9 gene are associated with hypocholesterolemia and possibly increased response to statin therapy. Arterioscler Thromb Vasc Biol 26, 1094-1100. (Pubitemid 43732117)
9. Cohen J, Pertsemlidis A, Kotowski IK, Graham R, Garcia CK, &, Hobbs HH, (2005) Low LDL cholesterol in individuals of African descent resulting from frequent nonsense mutations in PCSK9. Nat Genet 37, 161-165.
10. Kotowski IK, Pertsemlidis A, Luke A, Cooper RS, Vega GL, Cohen JC, &, Hobbs HH, (2006) A spectrum of PCSK9 alleles contributes to plasma levels of low-density lipoprotein cholesterol. Am J Hum Genet 78, 410-422. (Pubitemid 43291224)
11. Leren TP, (2004) Mutations in the PCSK9 gene in Norwegian subjects with autosomal dominant hypercholesterolemia. Clin Genet 65, 419-422. (Pubitemid 38659713)
12. Timms KM, Wagner S, Samuels ME, Forbey K, Goldfine H, Jammulapati S, Skolnick MH, Hopkins PN, Hunt SC, &, Shattuck DM, (2004) A mutation in PCSK9 causing autosomal-dominant hypercholesterolemia in a Utah pedigree. Hum Genet 114, 349-353. (Pubitemid 38324948)
13. Rashid S, Curtis DE, Garuti R, Anderson NN, Bashmakov Y, Ho YK, Hammer RE, Moon YA, &, Horton JD, (2005) Decreased plasma cholesterol and hypersensitivity to statins in mice lacking Pcsk9. Proc Natl Acad Sci USA 102, 5374-5379. (Pubitemid 40530265)
14. Mousavi SA, Berge KE, &, Leren TP, (2009) The unique role of proprotein convertase subtilisin/kexin 9 in cholesterol homeostasis. J Intern Med 266, 507-519.
15. Zhang DW, Lagace TA, Garuti R, Zhao Z, McDonald M, Horton JD, Cohen JC, &, Hobbs HH, (2007) Binding of proprotein convertase subtilisin/kexin type 9 to epidermal growth factor-like repeat A of low density lipoprotein receptor decreases receptor recycling and increases degradation. J Biol Chem 282, 18602-18612. (Pubitemid 47100234)
16. Bottomley MJ, Cirillo A, Orsatti L, Ruggeri L, Fisher TS, Santoro JC, Cummings RT, Cubbon RM, Lo Surdo P, Calzetta A, et al. (2009) Structural and biochemical characterization of the wild type PCSK9-EGF(AB) complex and natural familial hypercholesterolemia mutants. J Biol Chem 284, 1313-1323.
17. Kwon HJ, Lagace TA, McNutt MC, Horton JD, &, Deisenhofer J, (2008) Molecular basis for LDL receptor recognition by PCSK9. Proc Natl Acad Sci USA 105, 1820-1825. (Pubitemid 351439423)
18. Yamamoto T, Lu C, &, Ryan RO, (2011) A two step binding model of PCSK9 interaction with the low density lipoprotein receptor. J Biol Chem 286, 5464-5470.
19. Fisher TS, Lo Surdo P, Pandit S, Mattu M, Santoro JC, Wisniewski D, Cummings RT, Calzetta A, Cubbon RM, Fischer PA, et al. (2007) Effects of pH and low density lipoprotein (LDL) on PCSK9-dependent LDL receptor regulation. J Biol Chem 282, 20502-20512. (Pubitemid 47100016)
20. Strom TB, Holla OL, Cameron J, Berge KE, &, Leren TP, (2010) Loss-of-function mutation R46L in the PCSK9 gene has little impact on the levels of total serum cholesterol in familial hypercholesterolemia heterozygotes. Clin Chim Acta 411, 229-233.
21. Horiuchi S, Murakami M, Takata K, &, Morino Y, (1986) Scavenger receptor for aldehyde-modified proteins. J Biol Chem 261, 4962-4966. (Pubitemid 17204287)
22. DeBlasi A, O'Reilly K, &, Motulsky HJ, (1989) Calculating receptor number from binding experiments using same compound as radioligand and competitor. Trends Pharmacol Sci 10, 227-229. (Pubitemid 19146394)
23. Klotz IM, (1982) Numbers of receptor sites from Scatchard graphs: facts and fantasies. Science 217, 1247-1249.
24. Bennett J, (1978) Methods in binding studies. In Neurotransmitter Receptor Binding (, Yamamura HI, Enna SJ, Kuhar MJ, eds), pp. 57-90. Raven Press, New York.
25. Cunningham D, Danley DE, Geoghegan KF, Griffor MC, Hawkins JL, Subashi TA, Varghese AH, Ammirati MJ, Culp JS, Hoth LR, et al. (2007) Structural and biophysical studies of PCSK9 and its mutants linked to familial hypercholesterolemia. Nat Struct Mol Biol 14, 413-419. (Pubitemid 46685885)
26. Marshall S, Podlecki DA, &, Olefsky JM, (1983) Low pH accelerates dissociation of receptor-bound insulin. Endocrinology 113, 37-42. (Pubitemid 13045113)
27. Harwood HJ Jr, &, Pellarin LD, (1997) Kinetics of low-density lipoprotein receptor activity in Hep-G2 cells: derivation and validation of a Briggs-Haldane-based kinetic model for evaluating receptor-mediated endocytotic processes in which receptors recycle. Biochem J 323 (Pt 3), 649-659.
28. Ostlund RE Jr, Levy RA, Witztum JL, &, Schonfeld G, (1982) Familial hypercholesterolemia. Evidence for a newly recognized mutation determining increased fibroblast receptor affinity but decreased capacity for low density lipoprotein in two siblings. J Clin Invest 70, 823-831. (Pubitemid 12038098)
29. Pitas RE, Innerarity TL, Arnold KS, &, Mahley RW, (1979) Rate and equilibrium constants for binding of apo-E HDLc (a cholesterol-induced lipoprotein) and low density lipoproteins to human fibroblasts: evidence for multiple receptor binding of apo-E HDLc. Proc Natl Acad Sci USA 76, 2311-2315. (Pubitemid 9184920)
30. Chappell DA, Fry GL, Waknitz MA, &, Berns JJ, (1991) Ligand size as a determinant for catabolism by the low density lipoprotein (LDL) receptor pathway. A lattice model for LDL binding. J Biol Chem 266, 19296-19302. (Pubitemid 21908232)
31. Hwang J, &, Menon KM, (1983) Characterization of low density and high density lipoprotein receptors in the rat corpus luteum and regulation by gonadotropin. J Biol Chem 258, 8020-8027. (Pubitemid 13075269)
32. Taylor SI, (1975) Binding of hormones to receptors. An alternative explanation of nonlinear Scatchard plots. Biochemistry 14, 2357-2361.
33. Kowal RC, Herz J, Goldstein JL, Esser V, &, Brown MS, (1989) Low density lipoprotein receptor-related protein mediates uptake of cholesteryl esters derived from apoprotein E-enriched lipoproteins. Proc Natl Acad Sci USA 86, 5810-5814. (Pubitemid 19217543)
34. Pearlstein RA, Hu QY, Zhou J, Yowe D, Levell J, Dale B, Kaushik VK, Daniels D, Hanrahan S, Sherman W, et al. (2010) New hypotheses about the structure-function of proprotein convertase subtilisin/kexin type 9: analysis of the epidermal growth factor-like repeat A docking site using WaterMap. Proteins 78, 2571-2586.
35. Piper DE, Jackson S, Liu Q, Romanow WG, Shetterly S, Thibault ST, Shan B, &, Walker NP, (2007) The crystal structure of PCSK9: a regulator of plasma LDL-cholesterol. Structure 15, 545-552. (Pubitemid 46702689)
36. Anderson RG, Brown MS, &, Goldstein JL, (1977) Role of the coated endocytic vesicle in the uptake of receptor-bound low density lipoprotein in human fibroblasts. Cell 10, 351-364. (Pubitemid 8081701)
37. Goldstein JL, Anderson RG, &, Brown MS, (1979) Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279, 679-685. (Pubitemid 9205224)
38. van Driel IR, Davis CG, Goldstein JL, &, Brown MS, (1987) Self-association of the low density lipoprotein receptor mediated by the cytoplasmic domain. J Biol Chem 262, 16127-16134.
39. Anderson RG, Goldstein JL, &, Brown MS, (1980) Fluorescence visualization of receptor-bound low density lipoprotein in human fibroblasts. J Recept Res 1, 17-39. (Pubitemid 11237711)
40. de Meyts P, Roth J, Neville DM Jr, Gavin JR 3rd, &, Lesniak MA, (1973) Insulin interactions with its receptors: experimental evidence for negative cooperativity. Biochem Biophys Res Commun 55, 154-161.
41. De Lean A, Munson PJ, &, Rodbard D, (1979) Multi-subsite receptors for multivalent ligands. Application to drugs, hormones, and neurotransmitters. Mol Pharmacol 15, 60-70. (Pubitemid 9150360)
42. Stoker MG, (1973) Role of diffusion boundary layer in contact inhibition of growth. Nature 246, 200-203.
43. Wiley HS, &, Cunningham DD, (1982) The endocytotic rate constant. A cellular parameter for quantitating receptor-mediated endocytosis. J Biol Chem 257, 4222-4229. (Pubitemid 12080144)
44. Holla OL, Strom TB, Cameron J, Berge KE, &, Leren TP, (2010) A chimeric LDL receptor containing the cytoplasmic domain of the transferrin receptor is degraded by PCSK9. Mol Genet Metab 99, 149-156.
45. Pittman RC, Carew TE, Glass CK, Green SR, Taylor CA Jr, &, Attie AD, (1983) A radioiodinated, intracellularly trapped ligand for determining the sites of plasma protein degradation in vivo. Biochem J 212, 791-800. (Pubitemid 13056899)
46. Martinsson K, Skogh T, Mousavi SA, Berg T, Jonsson JI, &, Hultman P, (2010) Deficiency of activating Fcgamma-receptors reduces hepatic clearance and deposition of IC and increases CIC levels in mercury-induced autoimmunity. PLoS ONE 5, e13413.
47. Scatchard G, (1949) Equilibrium in non-electrolyte mixtures. Chem Rev 44, 7-35.