Transgenic expression and genetic variation of Lmf1 affect LPL activity in mice and humans

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 5, 2012, Pages 1204-1210

  Hosseini, Maryam ^a,b,c   Ehrhardt, Nicole ^a   Weissglas Volkov, Daphna ^c   Lai, Ching Mei ^b,c   Mao, Hui Z ^a   Liao, Jo Ling ^a,b   Nikkola, Elina ^c   Bensadoun, André ^d   Taskinen, Marja Riitta ^e   Doolittle, Mark H ^b,c   Pajukanta, Päivi ^c   Péterfy, Miklós ^a,b,c  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Cornell University ^*  (United States)

^e HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

Author keywords

Hyperlipoproteinemia; Lipases; Lipoprotein lipase; Transgenic models

Indexed keywords

CHAPERONE; LIPASE MATURATION FACTOR 1; LIPOPROTEIN LIPASE; UNCLASSIFIED DRUG;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DYSLIPIDEMIA; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; MOUSE; MUSCLE TISSUE; NONHUMAN; OMENTUM; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PROCESSING; SINGLE NUCLEOTIDE POLYMORPHISM; SUBCUTANEOUS TISSUE;

ADIPOSE TISSUE; ANIMALS; DNA; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETIC VARIATION; HUMANS; HYPERTRIGLYCERIDEMIA; LIPOPROTEIN LIPASE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; MYOCARDIUM;

EID: 84860214013     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.245696     Document Type: Article

References (43)

1. Wang H, Eckel RH. Lipoprotein lipase: from gene to obesity. Am J Physiol Endocrinol Metab. 2009;297:E271-E288.
2. Weinstock PH, Bisgaier CL, Aalto-Setala K, Radner H, Ramakrishnan R, Levak-Frank S, Essenburg AD, Zechner R, Breslow JL. Severe hypertriglyceridemia, reduced high density lipoprotein, and neonatal death in lipoprotein lipase knockout mice. Mild hypertriglyceridemia with impaired very low density lipoprotein clearance in heterozygotes. J Clin Invest. 1995;96:2555-2568.
3. Kim JK, Fillmore JJ, Chen Y, Yu C, Moore IK, Pypaert M, Lutz EP, Kako Y, Velez-Carrasco W, Goldberg IJ, Breslow JL, Shulman GI. Tissue-specific overexpression of lipoprotein lipase causes tissue-specific insulin resistance. Proc Natl Acad Sci USA. 2001;98:7522-7527. (Pubitemid 32567981)
4. Goodarzi MO, Guo X, Taylor KD, Quinones MJ, Saad MF, Yang H, Hsueh WA, Rotter JI. Lipoprotein lipase is a gene for insulin resistance in Mexican Americans. Diabetes. 2004;53:214-220. (Pubitemid 38044718)
5. Teslovich TM, Musunuru K, Smith AV, Edmondson AC, Stylianou IM, Koseki M, Pirruccello JP, Ripatti S, Chasman DI, Willer CJ, Johansen CT, Fouchier SW, Isaacs A, Peloso GM, Barbalic M, Ricketts SL, Bis JC, Aulchenko YS, Thorleifsson G, Feitosa MF, Chambers J, Orho-Melander M, Melander O, Johnson T, Li X, Guo X, Li M, Shin Cho Y, Jin Go M, Jin Kim Y, Lee JY, Park T, Kim K, Sim X, Twee-Hee Ong R, Croteau-Chonka DC, Lange LA, Smith JD, Song K, Hua Zhao J, Yuan X, Luan J, Lamina C, Ziegler A, Zhang W, Zee RY, Wright AF, Witteman JC, Wilson JF, Willemsen G, Wichmann HE, Whitfield JB, Waterworth DM, Wareham NJ, Waeber G, Vollenweider P, Voight BF, Vitart V, Uitterlinden AG, Uda M, Tuomilehto J, Thompson JR, Tanaka T, Surakka I, Stringham HM, Spector TD, Soranzo N, Smit JH, Sinisalo J, Silander K, Sijbrands EJ, Scuteri A, Scott J, Schlessinger D, Sanna S, Salomaa V, Saharinen J, Sabatti C, Ruokonen A, Rudan I, Rose LM, Roberts R, Rieder M, Psaty BM, Pramstaller PP, Pichler I, Perola M, Penninx BW, Pedersen NL, Pattaro C, Parker AN, Pare G, Oostra BA, O'Donnell CJ, Nieminen MS, Nickerson DA, Montgomery GW, Meitinger T, McPherson R, McCarthy MI, McArdle W, Masson D, Martin NG, Marroni F, Mangino M, Magnusson PK, Lucas G, Luben R, Loos RJ, Lokki ML, Lettre G, Langenberg C, Launer LJ, Lakatta EG, Laaksonen R, Kyvik KO, Kronenberg F, Konig IR, Khaw KT, Kaprio J, Kaplan LM, Johansson A, Jarvelin MR, Janssens AC, Ingelsson E, Igl W, Kees Hovingh G, Hottenga JJ, Hofman A, Hicks AA, Hengstenberg C, Heid IM, Hayward C, Havulinna AS, Hastie ND, Harris TB, Haritunians T, Hall AS, Gyllensten U, Guiducci C, Groop LC, Gonzalez E, Gieger C, Freimer NB, Ferrucci L, Erdmann J, Elliott P, Ejebe KG, Doring A, Dominiczak AF, Demissie S, Deloukas P, de Geus EJ, de Faire U, Crawford G, Collins FS, Chen YD, Caulfield MJ, Campbell H, Burtt NP, Bonnycastle LL, Boomsma DI, Boekholdt SM, Bergman RN, Barroso I, Bandinelli S, Ballantyne CM, Assimes TL, Quertermous T, Altshuler D, Seielstad M, Wong TY, Tai ES, Feranil AB, Kuzawa CW, Adair LS, Taylor HA, Taylor HA., Borecki IB, Gabriel SB, Wilson JG, Holm H, Thorsteinsdottir U, Gudnason V, Krauss RM, Mohlke KL, Ordovas JM, Munroe PB, Kooner JS, Tall AR, Hegele RA, Kastelein JJ, Schadt EE, Rotter JI, Boerwinkle E, Strachan DP, Mooser V, Stefansson K, Reilly MP, Samani NJ, Schunkert H, Cupples LA, Sandhu MS, Ridker PM, Rader DJ, van Duijn CM, Peltonen L, Abecasis GR, Boehnke M, Kathiresan S. Biological, clinical and population relevance of 95 loci for blood lipids. Nature. 2010;466:707-713.
6. Doolittle MH, Peterfy M. Mechanisms of lipase maturation. Clin Lipidol. 2010;5:71-85.
7. Speake BK, Parkin SM, Robinson DS. Degradation of lipoprotein lipase in rat adipose tissue. Biochim Biophys Acta. 1985;840:419-422. (Pubitemid 15069416)
8. Semb H, Olivecrona T. Mechanisms for turnover of lipoprotein lipase in guinea pig adipocytes. Biochim Biophys Acta. 1987;921:104-115.
9. Ben-Zeev O, Doolittle MH, Davis RC, Elovson J, Schotz MC. Maturation of lipoprotein lipase. Expression of full catalytic activity requires glucose trimming but not translocation to the cis-Golgi compartment. J Biol Chem. 1992;267:6219-6227.
10. 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. (Pubitemid 34968201)
11. Doolittle MH, Ben-Zeev O, Bassilian S, Whitelegge JP, Peterfy M, Wong H. Hepatic lipase maturation: a partial proteome of interacting factors. J Lipid Res. 2009;50:1173-1184.
12. Peterfy M, Ben-Zeev O, Mao HZ, Weissglas-Volkov D, Aouizerat BE, Pullinger CR, Frost PH, Kane JP, Malloy MJ, Reue K, Pajukanta P, Doolittle MH. Mutations in LMF1 cause combined lipase deficiency and severe hypertriglyceridemia. Nat Genet. 2007;39:1483-1487. (Pubitemid 350191343)
13. Briquet-Laugier V, Ben-Zeev O, White A, Doolittle MH. Cld and lec23 are disparate mutations that affect maturation of lipoprotein lipase in the endoplasmic reticulum. J Lipid Res. 1999;40:2044-2058. (Pubitemid 29523431)
14. Doolittle MH, Neher SB, Ben-Zeev O, Ling-Liao J, Gallagher CM, Hosseini M, Yin F, Wong H, Walter P, Peterfy M. Lipase maturation factor LMF1, membrane topology and interaction with lipase proteins in the endoplasmic reticulum. J Biol Chem. 2009;284:33623-33633.
15. Cefalu AB, Noto D, Arpi ML, Yin F, Spina R, Hilden H, Barbagallo CM, Carroccio A, Tarugi P, Squatrito S, Vigneri R, Taskinen MR, Peterfy M, Averna MR. Novel LMF1 nonsense mutation in a patient with severe hypertriglyceridemia. J Clin Endocrinol Metab. 2009;94:4584-4590.
16. Ben-Zeev O, Hosseini M, Lai CM, Ehrhardt N, Wong H, Cefalu AB, Noto D, Averna MR, Doolittle MH, Peterfy M. Lipase maturation factor 1 is required for endothelial lipase activity. J Lipid Res. 2011;52:1162-1169.
17. Hill JS, Davis RC, Yang D, Schotz MC, Wong H. Hepatic lipase: high-level expression and subunit structure determination. Methods Enzymol. 1997;284:232-246. (Pubitemid 27381578)
18. Griffon N, Jin W, Petty TJ, Millar J, Badellino KO, Saven JG, Marchadier DH, Kempner ES, Billheimer J, Glick JM, Rader DJ. Identification of the active form of endothelial lipase, a homodimer in a head-to-tail conformation. J Biol Chem. 2009;284:23322-23330.
19. Lowe ME. The triglyceride lipases of the pancreas. J Lipid Res. 2002;43:2007-2016.
20. Scow RO, Schultz CJ, Park JW, Blanchette-Mackie EJ. Combined lipase deficiency (cld/cld) in mice affects differently post-translational processing of lipoprotein lipase, hepatic lipase and pancreatic lipase. Chem Phys Lipids. 1998;93:149-155. (Pubitemid 28383214)
21. Doolittle MH, Ehrhardt N, Peterfy M. Lipase maturation factor 1: structure and role in lipase folding and assembly. Curr Opin Lipidol. 2010;21:198-203.
22. Zhang L, Lookene A, Wu G, Olivecrona G. Calcium triggers folding of lipoprotein lipase into active dimers. J Biol Chem. 2005;280:42580-42591. (Pubitemid 43049216)
23. Peterfy M. Lipase maturation factor 1: a lipase chaperone involved in lipid metabolism. Biochim Biophys Acta. In press.
24. Ross SR, Graves RA, Greenstein A, Platt KA, Shyu HL, Mellovitz B, Spiegelman BM. A fat-specific enhancer is the primary determinant of gene expression for adipocyte P2 in vivo. Proc Natl Acad Sci USA. 1990;87:9590-9594. (Pubitemid 120016489)
25. Graves RA, Tontonoz P, Platt KA, Ross SR, Spiegelman BM. Identification of a fat cell enhancer: analysis of requirements for adipose tissue-specific gene expression. J Cell Biochem. 1992;49:219-224.
26. Yin F, Doolittle MH, Peterfy M. A quantitative assay measuring the function of lipase maturation factor 1. J Lipid Res. 2009;50:2265-2269.
27. Bruning JC, Michael MD, Winnay JN, Hayashi T, Horsch D, Accili D, Goodyear LJ, Kahn CR. A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell. 1998;2:559-569. (Pubitemid 128379082)
28. Abecasis GR, Cardon LR, Cookson WO. A general test of association for quantitative traits in nuclear families. Am J Hum Genet. 2000;66:279-292. (Pubitemid 30481489)
29. Havill LM, Dyer TD, Richardson DK, Mahaney MC, Blangero J. The quantitative trait linkage disequilibrium test: a more powerful alternative to the quantitative transmission disequilibrium test for use in the absence of population stratification. BMC Genet. 2005;6(Suppl 1):S91.
30. Weissglas-Volkov D, Pajukanta P. Genetic causes of high and low serum HDL-cholesterol. J Lipid Res. 2010;51:2032-2057.
31. Li Y, Willer C, Sanna S, Abecasis G. Genotype imputation. Annu Rev Genomics Hum Genet. 2009;10:387-406.
32. Lichtenstein L, Kersten S. Modulation of plasma TG lipolysis by Angiopoietin-like proteins and GPIHBP1. Biochim Biophys Acta. 2010;1801:415-420.
33. Neuger L, Vilaro S, Lopez-Iglesias C, Gupta J, Olivecrona T, Olivecrona G. Effects of heparin on the uptake of lipoprotein lipase in rat liver. BMC Physiol. 2004;4:13.
34. Ruge T, Sukonina V, Myrnas T, Lundgren M, Eriksson JW, Olivecrona G. Lipoprotein lipase activity/mass ratio is higher in omental than in subcutaneous adipose tissue. Eur J Clin Invest. 2006;36:16-21.
35. Doolittle MH, Ben-Zeev O, Elovson J, Martin D, Kirchgessner TG. The response of lipoprotein lipase to feeding and fasting. Evidence for posttranslational regulation. J Biol Chem. 1990;265:4570-4577. (Pubitemid 20096128)
36. Halberg N, Khan T, Trujillo ME, Wernstedt-Asterholm I, Attie AD, Sherwani S, Wang ZV, Landskroner-Eiger S, Dineen S, Magalang UJ, Brekken RA, Scherer PE. Hypoxia-inducible factor 1alpha induces fibrosis and insulin resistance in white adipose tissue. Mol Cell Biol. 2009;29:4467-4483.
37. Ben-Zeev O, Lusis AJ, LeBoeuf RC, Nikazy J, Schotz MC. Evidence for independent genetic regulation of heart and adipose lipoprotein lipase activity. J Biol Chem. 1983;258:13632-13636. (Pubitemid 14212001)
38. Davies PJ, Berry SA, Shipley GL, Eckel RH, Hennuyer N, Crombie DL, Ogilvie KM, Peinado-Onsurbe J, Fievet C, Leibowitz MD, Heyman RA, Auwerx J. Metabolic effects of rexinoids: tissue-specific regulation of lipoprotein lipase activity. Mol Pharmacol. 2001;59:170-176. (Pubitemid 32108547)
39. Hensley LL, Ranganathan G, Wagner EM, Wells BD, Daniel JC, Vu D, Semenkovich CF, Zechner R, Kern PA. Transgenic mice expressing lipoprotein lipase in adipose tissue. Absence of the proximal 3-untranslated region causes translational upregulation. J Biol Chem. 2003;278:32702-32709. (Pubitemid 37055709)
40. Shimada M, Shimada M. S., Gotoda T, Yamamoto K, Kawamura M, Inaba T, Yazaki Y, Yamada N. Overexpression of human lipoprotein lipase in transgenic mice. J Biol Chem. 1993;268:17924-17929.
41. Zsigmond E, Scheffler E, Forte TM, Potenz R, Wu W, Chan L. Transgenic mice expressing human lipoprotein lipase driven by the mouse metallothionein promoter. A phenotype associated with increased perinatal mortality and reduced plasma very low density lipoprotein of normal size. J Biol Chem. 1994;269:18757-18766.
42. Liu M-S, Jirik FR, LeBoeuf RC, Henderson H, Castellani LW, Lusis AJ, Ma Y, Forsythe IJ, Zhang H, Kirk E, Brunzell JD, Hayde MR. Alteration of lipid profiles in plasma of transgenic mice expressing human lipoprotein lipase. J Biol Chem. 1994;269:11417-11424. (Pubitemid 24200357)
43. Johansen CT, Wang J, McIntyre AD, Martins RA, Ban MR, Lanktree MB, Huff MW, Peterfy M, Mehrabian M, Lusis AJ, Kathiresan S, Anand SS, Yusuf S, Lee AH, Glimcher LH, Cao H, Hegele RA. Excess of rare variants in non-GWAS candidate genes in patients with hypertriglyceridemia. Circ Cardiovasc Genet. In press.