GPIHBP1 missense mutations often cause multimerization of GPIHBP1 and thereby prevent lipoprotein lipase binding

Circulation Research

Volumn 116, Issue 4, 2015, Pages 624-632

  Beigneux, Anne P ^a   Fong, Loren G ^a   Bensadoun, André ^b   Davies, Brandon S J ^c   Oberer, Monika ^d   Gårdsvoll, Henrik ^e   Ploug, Michael ^e   Young, Stephen G ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Department of Molecular Biology and Genetics   (United States)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF GRAZ   (Austria)

^e FINSEN LABORATORY   (Denmark)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chylomicrons; Endothelial cells; GPIHBP1 protein; Hypertriglyceridemia; Lipoprotein lipase; Protein multimerization; Triglycerides

Indexed keywords

AMINO ACID; CYSTEINE; DIMER; DISULFIDE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; GPIHBP1 PROTEIN; LIPOPROTEIN LIPASE; MONOMER; POLYMER; UNCLASSIFIED DRUG; GPI-HBP1 PROTEIN, MOUSE; GPIHBP1 PROTEIN, HUMAN; LIPOPROTEIN RECEPTOR; LPL PROTEIN, HUMAN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CHO CELL LINE; CONTROLLED STUDY; DIMERIZATION; DROSOPHILA; ENZYME BINDING; FEMALE; GENE EXPRESSION SYSTEM; HUMAN; HUMAN CELL; MISSENSE MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MULTIMERIZATION; RAT; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; CRICETULUS; CYTOLOGY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; HYPERLIPOPROTEINEMIA TYPE 1; METABOLISM; PROTEIN CONFORMATION;

ANIMALS; BINDING SITES; CHO CELLS; CRICETULUS; CYSTEINE; DROSOPHILA; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYPERLIPOPROTEINEMIA TYPE I; LIPOPROTEIN LIPASE; MODELS, MOLECULAR; MUTATION, MISSENSE; PHOSPHOINOSITIDE PHOSPHOLIPASE C; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; RATS; RECEPTORS, LIPOPROTEIN; TRANSFECTION;

EID: 84924203151     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.305085     Document Type: Article

References (33)

1. Beigneux AP, Davies B, Gin P, et al. Glycosylphosphatidylinositol-anchored high density lipoprotein-binding protein 1 plays a critical role in the lipolytic processing of chylomicrons. Cell Metab. 2007;5:279-291.
2. Davies BS, Beigneux AP, Barnes RH II, Tu Y, Gin P, Weinstein MM, Nobumori C, Nyrén R, Goldberg I, Olivecrona G, Bensadoun A, Young SG, Fong LG. GPIHBP1 is responsible for the entry of lipoprotein lipase into capillaries. Cell Metab. 2010;12:42-52. doi: 10.1016/j.cmet.2010.04.016.
3. Beigneux AP, Franssen R, Bensadoun A, Gin P, Melford K, Peter J, Walzem RL, Weinstein MM, Davies BS, Kuivenhoven JA, Kastelein JJ, Fong LG, Dallinga-Thie GM, Young SG. Chylomicronemia with a mutant GPIHBP1 (Q115P) that cannot bind lipoprotein lipase. Arterioscler Thromb Vasc Biol. 2009;29:956-962. doi: 10.1161/ATVBAHA.109.186577.
4. Franssen R, Young SG, Peelman F, Hertecant J, Sierts JA, Schimmel AW, Bensadoun A, Kastelein JJ, Fong LG, Dallinga-Thie GM, Beigneux AP. Chylomicronemia with low postheparin lipoprotein lipase levels in the setting of GPIHBP1 defects. Circ Cardiovasc Genet. 2010;3:169-178. doi: 10.1161/CIRCGENETICS.109.908905.
5. Olivecrona G, Ehrenborg E, Semb H, Makoveichuk E, Lindberg A, Hayden MR, Gin P, Davies BS, Weinstein MM, Fong LG, Beigneux AP, Young SG, Olivecrona T, Hernell O. Mutation of conserved cysteines in the Ly6 domain of GPIHBP1 in familial chylomicronemia. J Lipid Res. 2010;51:1535-1545. doi: 10.1194/jlr.M002717.
6. Charrière S, Peretti N, Bernard S, Di Filippo M, Sassolas A, Merlin M, Delay M, Debard C, Lefai E, Lachaux A, Moulin P, Marc¸ais C. GPIHBP1 C89F neomutation and hydrophobic C-terminal domain G175R mutation in two pedigrees with severe hyperchylomicronemia. J Clin Endocrinol Metab. 2011;96:E1675-E1679. doi: 10.1210/jc.2011-1444.
7. Coca-Prieto I, Kroupa O, Gonzalez-Santos P, Magne J, Olivecrona G, Ehrenborg E, Valdivielso P. Childhood-onset chylomicronaemia with reduced plasma lipoprotein lipase activity and mass: identification of a novel GPIHBP1 mutation. J Intern Med. 2011;270:224-228. doi: 10.1111/j.1365-2796.2011.02361.x.
8. Rios JJ, Shastry S, Jasso J, Hauser N, Garg A, Bensadoun A, Cohen JC, Hobbs HH. Deletion of GPIHBP1 causing severe chylomicronemia. J Inherit Metab Dis. 2012;35:531-540. doi: 10.1007/s10545-011-9406-5.
9. Plengpanich W, Young SG, Khovidhunkit W, Bensadoun A, Karnman H, Ploug M, Gardsvoll H, Leung CS, Adeyo O, Larsson M, Muanpetch S, Charoen S, Fong LG, Niramitmahapanya S, Beigneux AP. Multimerization of GPIHBP1 and familial chylomicronemia from a serine-to-cysteine substitution in GPIHBP1's ly6 domain. J Biol Chem. 2014;289:19491-19499.
10. Weinstein MM, Goulbourne CN, Davies BS, Tu Y, Barnes RH II, Watkins SM, Davis R, Reue K, Tontonoz P, Beigneux AP, Fong LG, Young SG. Reciprocal metabolic perturbations in the adipose tissue and liver of GPIHBP1-deficient mice. Arterioscler Thromb Vasc Biol. 2012;32:230-235. doi: 10.1161/ATVBAHA.111.241406.
11. Ploug M, Gårdsvoll H, Jørgensen TJ, Lønborg Hansen L, Danø K. Structural analysis of the interaction between urokinase-type plasminogen activator and its receptor: a potential target for anti-invasive cancer therapy. Biochem Soc Trans. 2002;30:177-183. doi: 10.1042/.
12. Mallya M, Campbell RD, Aguado B. Characterization of the five novel Ly-6 superfamily members encoded in the MHC, and detection of cells expressing their potential ligands. Protein Sci. 2006;15:2244-2256. doi: 10.1110/ps.062242606.
13. Adeyo O, Allan BB, Barnes RH II, Goulbourne CN, Tatar A, Tu Y, Young LC, Weinstein MM, Tontonoz P, Fong LG, Beigneux AP, Young SG. Palmoplantar keratoderma along with neuromuscular and metabolic phenotypes in Slurp1-deficient mice. J Invest Dermatol. 2014;134:1589-1598. doi: 10.1038/jid.2014.19.
14. Fry BG, Wüster W, Kini RM, Brusic V, Khan A, Venkataraman D, Rooney AP. Molecular evolution and phylogeny of elapid snake venom three-finger toxins. J Mol Evol. 2003;57:110-129. doi: 10.1007/s00239-003-2461-2.
15. Gin P, Yin L, Davies BSJ, Weinstein MM, Ryan RO, Bensadoun A, Fong LG, Young SG, Beigneux AP. The acidic domain of GPIHBP1 is important for the binding of lipoprotein lipase and chylomicrons. J Biol Chem. 2008;283:29554-29562.
16. Beigneux AP, Gin P, Davies BS, Weinstein MM, Bensadoun A, Fong LG, Young SG. Highly conserved cysteines within the Ly6 domain of GPIHBP1 are crucial for the binding of lipoprotein lipase. J Biol Chem. 2009;284:30240-30247. doi: 10.1074/jbc.M109.046391.
17. Beigneux AP, Davies BS, Tat S, Chen J, Gin P, Voss CV, Weinstein MM, Bensadoun A, Pullinger CR, Fong LG, Young SG. Assessing the role of the glycosylphosphatidylinositol-anchored high density lipoprotein-binding protein 1 (GPIHBP1) three-finger domain in binding lipoprotein lipase. J Biol Chem. 2011;286:19735-19743. doi: 10.1074/jbc.M111.242024.
18. Surendran RP, Visser ME, Heemelaar S, Wang J, Peter J, Defesche JC, Kuivenhoven JA, Hosseini M, Péterfy M, Kastelein JJ, Johansen CT, Hegele RA, Stroes ES, Dallinga-Thie GM. Mutations in LPL, APOC2, APOA5, GPIHBP1 and LMF1 in patients with severe hypertriglyceridaemia. J Intern Med. 2012;272:185-196. doi: 10.1111/j.1365-2796.2012.02516.x.
19. Gårdsvoll H, Hansen LV, Jørgensen TJ, Ploug M. A new tagging system for production of recombinant proteins in Drosophila S2 cells using the third domain of the urokinase receptor. Protein Expr Purif. 2007;52:384-394. doi: 10.1016/j.pep.2006.11.013.
20. Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009;4:363-371. doi: 10.1038/nprot.2009.2.
21. Lyukmanova EN, Shenkarev ZO, Shulepko MA, Mineev KS, D'Hoedt D, Kasheverov IE, Filkin SY, Krivolapova AP, Janickova H, Dolezal V, Dolgikh DA, Arseniev AS, Bertrand D, Tsetlin VI, Kirpichnikov MP. NMR structure and action on nicotinic acetylcholine receptors of watersoluble domain of human LYNX1. J Biol Chem. 2011;286:10618-10627. doi: 10.1074/jbc.M110.189100.
22. Lin L, Gårdsvoll H, Huai Q, Huang M, Ploug M. Structure-based engineering of species selectivity in the interaction between urokinase and its receptor: implication for preclinical cancer therapy. J Biol Chem. 2010;285:10982-10992. doi: 10.1074/jbc.M109.093492.
23. Gårdsvoll H, Kriegbaum MC, Hertz EP, Alpízar-Alpízar W, Ploug M. The urokinase receptor homolog Haldisin is a novel differentiation marker of stratum granulosum in squamous epithelia. J Histochem Cytochem. 2013;61:802-813. doi: 10.1369/0022155413501879.
24. Xu X, Gårdsvoll H, Yuan C, Lin L, Ploug M, Huang M. Crystal structure of the urokinase receptor in a ligand-free form. J Mol Biol. 2012;416:629-641. doi: 10.1016/j.jmb.2011.12.058.
25. Peterson J, Fujimoto WY, Brunzell JD. Human lipoprotein lipase: relationship of activity, heparin affinity, and conformation as studied with monoclonal antibodies. J Lipid Res. 1992;33:1165-1170.
26. Ben-Zeev O, Mao HZ, Doolittle MH. Maturation of lipoprotein lipase in the endoplasmic reticulum. Concurrent formation of functional dimers and inactive aggregates. J Biol Chem. 2002;277:10727-10738. doi: 10.1074/jbc.M108128200.
27. Bogan AA, Thorn KS. Anatomy of hot spots in protein interfaces. J Mol Biol. 1998;280:1-9. doi: 10.1006/jmbi.1998.1843.
28. Chakrabarti P, Janin J. Dissecting protein-protein recognition sites. Proteins. 2002;47:334-343.
29. Glaser F, Steinberg DM, Vakser IA, Ben-Tal N. Residue frequencies and pairing preferences at protein-protein interfaces. Proteins. 2001;43:89-102.
30. Young SG, Davies BS, Fong LG, Gin P, Weinstein MM, Bensadoun A, Beigneux AP. GPIHBP1: an endothelial cell molecule important for the lipolytic processing of chylomicrons. Curr Opin Lipidol. 2007;18:389-396. doi: 10.1097/MOL.0b013e3281527914.
31. Muskal SM, Holbrook SR, Kim SH. Prediction of the disulfide-bonding state of cysteine in proteins. Protein Eng. 1990;3:667-672.
32. Fletcher A, Bryant JA, Gardner B, Judson PA, Spring FA, Parsons SF, Mallinson G, Anstee DJ. New monoclonal antibodies in CD59: use for the analysis of peripheral blood cells from paroxysmal nocturnal haemoglobinuria (PNH) patients and for the quantitation of CD59 on normal and decay accelerating factor (DAF)-deficient erythrocytes. Immunology. 1992;75:507-512.
33. Osipov AV, Kasheverov IE, Makarova YV, Starkov VG, Vorontsova OV, Ziganshin RKh, Andreeva TV, Serebryakova MV, Benoit A, Hogg RC, Bertrand D, Tsetlin VI, Utkin YN. Naturally occurring disulfide-bound dimers of three-fingered toxins: a paradigm for biological activity diversification. J Biol Chem. 2008;283:14571-14580. doi: 10.1074/jbc.M802085200.