Lipoprotein lipase and angiopoietin-like 4 – Cardiomyocyte secretory proteins that regulate metabolism during diabetic heart diseaseFootnote

Referees: Dr. Garry Shen, University of Manitoba, Winnipeg, Manitoba, Canada; Dr. Thomas Pulinilkunnil and Dr. Petra Kienesberger, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada

References

• Hamosh M, Hamosh P. Lipoprotein lipase: its physiological and clinical significance. Mol Aspects Med 1983;6:199–289
   PubMed Web of Science ®Google Scholar
• An D, Pulinilkunnil T, Qi D, et al. The metabolic “switch” AMPK regulates cardiac heparin-releasable lipoprotein lipase. Am J Physiol Endocrinol Metab 2005;288:E246–53
   PubMed Web of Science ®Google Scholar
• Dutton S, Trayhurn P. Regulation of angiopoietin-like protein 4/fasting-induced adipose factor (Angptl4/FIAF) expression in mouse white adipose tissue and 3T3-L1 adipocytes. Br J Nutr 2008;100:18–26
   PubMed Web of Science ®Google Scholar
• An D, Kewalramani G, Qi D, et al. beta-Agonist stimulation produces changes in cardiac AMPK and coronary lumen LPL only during increased workload. Am J Physiol Endocrinol Metab 2005;288:E1120–7
   PubMed Web of Science ®Google Scholar
• Kim MS, Kewalramani G, Puthanveetil P, et al. Acute diabetes moderates trafficking of cardiac lipoprotein lipase through p38 mitogen-activated protein kinase-dependent actin cytoskeleton organization. Diabetes 2008;57:64–76
   PubMed Web of Science ®Google Scholar
• Kim MS, Wang F, Puthanveetil P, et al. Protein kinase D is a key regulator of cardiomyocyte lipoprotein lipase secretion after diabetes. Circ Res 2008;103:252–60
   PubMed Web of Science ®Google Scholar
• Wang GE, Li YF, Wu YP, et al. Phloridzin improves lipoprotein lipase activity in stress-loaded mice via AMPK phosphorylation. Int J Food Sci Nutr 2014;65:1–7
   PubMedGoogle Scholar
• Sun C, Qi R, Wang L, et al. p38 MAPK regulates calcium signal-mediated lipid accumulation through changing VDR expression in primary preadipocytes of mice. Mol Biol Rep 2012;39:3179–84
   PubMed Web of Science ®Google Scholar
• Dong B, Qi D, Yang L, et al. TLR4 regulates cardiac lipid accumulation and diabetic heart disease in the nonobese diabetic mouse model of type 1 diabetes. Am J PhysiolHeart Circ Physiol 2012;303:H732–42
   Web of Science ®Google Scholar
• Stapleton CM, Joo JH, Kim YS, et al. Induction of ANGPTL4 expression in human airway smooth muscle cells by PMA through activation of PKC and MAPK pathways. Exp Cell Res 2010;316:507–16
   PubMed Web of Science ®Google Scholar
• Yin DM, Huang YH, Zhu YB, Wang Y. Both the establishment and maintenance of neuronal polarity require the activity of protein kinase D in the Golgi apparatus. J Neurosci 2008;28:8832–43
   PubMed Web of Science ®Google Scholar
• Kim MS, Wang F, Puthanveetil P, et al. Cleavage of protein kinase D after acute hypoinsulinemia prevents excessive lipoprotein lipase-mediated cardiac triglyceride accumulation. Diabetes 2009;58:2464–75
   PubMed Web of Science ®Google Scholar
• Puthanveetil P, Wang Y, Zhang D, et al. Cardiac triglyceride accumulation following acute lipid excess occurs through activation of a FoxO1-iNOS-CD36 pathway. Free Radic Biol Med 2011;51:352–63
   PubMed Web of Science ®Google Scholar
• Puthanveetil P, Wan A, Rodrigues B. FoxO1 is crucial for sustaining cardiomyocyte metabolism and cell survival. Cardiovasc Res 2013;97:393–403
   PubMed Web of Science ®Google Scholar
• Kamei Y, Mizukami J, Miura S, et al. A forkhead transcription factor FKHR up-regulates lipoprotein lipase expression in skeletal muscle. FEBS Lett 2003;536:232–6
   PubMed Web of Science ®Google Scholar
• Battiprolu PK, Hojayev B, Jiang N, et al. Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J Clin Invest 2012;122:1109–18
   PubMed Web of Science ®Google Scholar
• Pulinilkunnil T, Puthanveetil P, Kim MS, et al. Ischemia-reperfusion alters cardiac lipoprotein lipase. Biochim Biophys Acta 2010;1801:171–5
   PubMed Web of Science ®Google Scholar
• Casanovas A, Carrascal M, Abian J, et al. Lipoprotein lipase is nitrated in vivo after lipopolysaccharide challenge. Free Radic Biol Med 2009;47:1553–60
   PubMed Web of Science ®Google Scholar
• Yamada T, Ozaki N, Kato Y, et al. Insulin downregulates angiopoietin-like protein 4 mRNA in 3T3-L1 adipocytes. Biochem Biophys Res Commun 2006;347:1138–44
   PubMed Web of Science ®Google Scholar
• Ranganathan G, Phan D, Pokrovskaya ID, et al. The translational regulation of lipoprotein lipase by epinephrine involves an RNA binding complex including the catalytic subunit of protein kinase A. J Biol Chem 2002;277:43281–7
   PubMed Web of Science ®Google Scholar
• Ranganathan G, Pokrovskaya I, Ranganathan S, Kern PA. Role of A kinase anchor proteins in the tissue-specific regulation of lipoprotein lipase. Mol Endocrinol 2005;19:2527–34
   PubMed Web of Science ®Google Scholar
• Motoyashiki T, Miyake M, Yoshida A, et al. A vanadyl sulfate-bovine serum albumin complex stimulates the release of lipoprotein lipase activity from isolated rat fat pads through an increase in the cellular content of cAMP and myo-inositol 1,4,5-trisphosphate. Biol Pharm Bull 1999;22:780–6
   PubMed Web of Science ®Google Scholar
• Sera M, Tanaka K, Morita T, Ueki H. Increasing effect of vanadate on lipoprotein lipase activity in isolated rat fat pads. Arch Biochem Biophys 1990;279:291–7
   PubMed Web of Science ®Google Scholar
• Kim SJ, Nian C, McIntosh CH. GIP increases human adipocyte LPL expression through CREB and TORC2-mediated trans-activation of the LPL gene. J Lipid Res 2010;51:3145–57
   PubMed Web of Science ®Google Scholar
• Husain S, Abdel-Latif AA. Role of protein kinase C alpha in endothelin-1 stimulation of cytosolic phospholipase A2 and arachidonic acid release in cultured cat iris sphincter smooth muscle cells. Biochim Biophys Acta 1998;1392:127–44
   PubMed Web of Science ®Google Scholar
• Beauchamp MC, Renier G. Homocysteine induces protein kinase C activation and stimulates c-Fos and lipoprotein lipase expression in macrophages. Diabetes 2002;51:1180–7
   PubMed Web of Science ®Google Scholar
• Ranganathan G, Kaakaji R, Kern PA. Role of protein kinase C in the translational regulation of lipoprotein lipase in adipocytes. J Biol Chem 1999;274:9122–7
   PubMed Web of Science ®Google Scholar
• Pulinilkunnil T, An D, Yip P, et al. Palmitoyl lysophosphatidylcholine mediated mobilization of LPL to the coronary luminal surface requires PKC activation. J Mol Cell Cardiol 2004;37:931–8
   PubMed Web of Science ®Google Scholar
• Pulinilkunnil T, An D, Ghosh S, et al. Lysophosphatidic acid-mediated augmentation of cardiomyocyte lipoprotein lipase involves actin cytoskeleton reorganization. Am J Physiol Heart Circ Physiol 2005;288:H2802–10
   PubMed Web of Science ®Google Scholar
• Ganguly R, Schram K, Fang X, et al. Adiponectin increases LPL activity via RhoA/ROCK-mediated actin remodelling in adult rat cardiomyocytes. Endocrinology 2011;152:247–54
   PubMed Web of Science ®Google Scholar
• Zhou H, Yang YH, Basile JR. The Semaphorin 4D-Plexin-B1-RhoA signaling axis recruits pericytes and regulates vascular permeability through endothelial production of PDGF-B and ANGPTL4. Angiogenesis 2014;17:261–74
   PubMed Web of Science ®Google Scholar
• Yao L, Kan EM, Lu J, et al. Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: role of TLR4 in hypoxic microglia. J Neuroinflammation 2013;10:23
   PubMed Web of Science ®Google Scholar
• Seehase M, Gantert M, Ladenburger A, et al. Myocardial response in preterm fetal sheep exposed to systemic endotoxinaemia. Pediatr Res 2011;70:242–6
   PubMed Web of Science ®Google Scholar
• Baumgarten G, Knuefermann P, Schuhmacher G, et al. Toll-like receptor 4, nitric oxide, and myocardial depression in endotoxemia. Shock 2006;25:43–9
   PubMed Web of Science ®Google Scholar
• Yan H, Aziz E, Shillabeer G, et al. Nitric oxide promotes differentiation of rat white preadipocytes in culture. J Lipid Res 2002;43:2123–9
   PubMed Web of Science ®Google Scholar
• Lee J, Jung E, Lee J, et al. Anti-adipogenesis by 6-thioinosine is mediated by downregulation of PPAR gamma through JNK-dependent upregulation of iNOS. Cell Mol Life Sci 2010;67:467–81
   PubMed Web of Science ®Google Scholar
• Lee JK, Won JS, Singh AK, Singh I. Adenosine kinase inhibitor attenuates the expression of inducible nitric oxide synthase in glial cells. Neuropharmacology 2005;48:151–60
   PubMed Web of Science ®Google Scholar
• Chong HC, Chan JS, Goh CQ, et al. Angiopoietin-like 4 stimulates STAT3-mediated iNOS expression and enhances angiogenesis to accelerate wound healing in diabetic mice. Mol Ther 2014;22:1593–604
   PubMed Web of Science ®Google Scholar
• Sadur CN, Eckel RH. Insulin stimulation of adipose tissue lipoprotein lipase. Use of the euglycemic clamp technique. J Clin Invest 1982;69:1119–25
   PubMed Web of Science ®Google Scholar
• Braun JE, Severson DL. Regulation of the synthesis, processing and translocation of lipoprotein lipase. Biochem J 1992;287:337–47
   PubMed Web of Science ®Google Scholar
• Braun JE, Severson DL. Tissue-specific regulation of lipoprotein lipase. Can Med Assoc J 1992;147:1192
   Web of Science ®Google Scholar
• Braun JE, Severson DL. Lipoprotein lipase release from cardiac myocytes is increased by decavanadate but not insulin. Am J Physiol 1992;262:E663–70
   PubMed Web of Science ®Google Scholar
• Sambandam N, Abrahani MA, St Pierre E, et al. Localization of lipoprotein lipase in the diabetic heart: regulation by acute changes in insulin. Arterioscler Thromb Vasc Biol 1999;19:1526–34
   PubMed Web of Science ®Google Scholar
• Caren R, Corbo L. Glucagon and plasma lipoprotein lipase. Proc Soc Exp Biol Med 1974;146:1106–10
   PubMed Web of Science ®Google Scholar
• Oscarsson J, Ottosson M, Vikman-Adolfsson K, et al. GH but not IGF-I or insulin increases lipoprotein lipase activity in muscle tissues of hypophysectomised rats. J Endocrinol 1999;160:247–55
   PubMed Web of Science ®Google Scholar
• Yang J, Ren J, Song J, et al. Glucagon-like peptide 1 regulates adipogenesis in 3T3-L1 preadipocytes. IntJ Mol Med 2013;31:1429–35
   PubMed Web of Science ®Google Scholar
• Balasubramaniyan V, Nalini N. Intraperitoneal leptin regulates lipid metabolism in ethanol supplemented Mus musculas heart. Life Sci 2006;78:831–7
   PubMed Web of Science ®Google Scholar
• von Eynatten M, Schneider JG, Humpert PM, et al. Decreased plasma lipoprotein lipase in hypoadiponectinemia: an association independent of systemic inflammation and insulin resistance. Diabetes Care 2004;27:2925–9
   PubMed Web of Science ®Google Scholar
• Ewart HS, Carroll R, Severson DL. Lipoprotein lipase activity is stimulated by insulin and dexamethasone in cardiomyocytes from diabetic rats. Can J Physiol Pharmacol 1999;77:571–8
   PubMed Web of Science ®Google Scholar
• Ewart HS, Severson DL. Insulin and dexamethasone stimulation of cardiac lipoprotein lipase activity involves the actin-based cytoskeleton. Biochem J 1999;340:485–90
   PubMed Web of Science ®Google Scholar
• Qi D, Pulinilkunnil T, An D, et al. Single-dose dexamethasone induces whole-body insulin resistance and alters both cardiac fatty acid and carbohydrate metabolism. Diabetes 2004;53:1790–7
   PubMed Web of Science ®Google Scholar
• Kewalramani G, Puthanveetil P, Kim MS, et al. Acute dexamethasone-induced increase in cardiac lipoprotein lipase requires activation of both Akt and stress kinases. Am J Physiol Endocrinol Metab 2008;295:E137–47
   PubMed Web of Science ®Google Scholar
• Grunfeld C, Gulli R, Moser AH, et al. Effect of tumor necrosis factor administration in vivo on lipoprotein lipase activity in various tissues of the rat. J Lipid Res 1989;30:579–85
   PubMed Web of Science ®Google Scholar
• Hulsmann WC, Dubelaar ML, De Wit LE, Persoon NL. Cardiac lipoprotein lipase: effects of lipopolysaccharide and tumor necrosis factor. Mol Cell Biochem 1988;79:137–45
   PubMed Web of Science ®Google Scholar
• Koliwad SK, Gray NE, Wang JC. Angiopoietin-like 4 (Angptl4): a glucocorticoid-dependent gatekeeper of fatty acid flux during fasting. Adipocyte 2012;1:182–7
   PubMedGoogle Scholar
• Kaddatz K, Adhikary T, Finkernagel F, et al. Transcriptional profiling identifies functional interactions of TGF beta and PPAR beta/delta signaling: synergistic induction of ANGPTL4 transcription. J Biol Chem 2010;285:29469–79
   PubMed Web of Science ®Google Scholar
• Knowles HJ, Cleton-Jansen AM, Korsching E, Athanasou NA. Hypoxia-inducible factor regulates osteoclast-mediated bone resorption: role of angiopoietin-like 4. FASEB J 2010;24:4648–59
   PubMed Web of Science ®Google Scholar
• Kewalramani G, An D, Kim MS, et al. AMPK control of myocardial fatty acid metabolism fluctuates with the intensity of insulin-deficient diabetes. J Mol Cell Cardiol 2007;42:333–42
   PubMed Web of Science ®Google Scholar
• An D, Rodrigues B. Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 2006;291:H1489–506
   PubMed Web of Science ®Google Scholar
• Wu Y, Song P, Xu J, et al. Activation of protein phosphatase 2A by palmitate inhibits AMP-activated protein kinase. J Biol Chem 2007;282:9777–88
   Google Scholar
• Wang F, Wang Y, Kim MS, et al. Glucose-induced endothelial heparanase secretion requires cortical and stress actin reorganization. Cardiovasc Res 2010;87:127–36
   PubMed Web of Science ®Google Scholar
• Cruz WS, Kwon G, Marshall CA, et al. Glucose and insulin stimulate heparin-releasable lipoprotein lipase activity in mouse islets and INS-1 cells. A potential link between insulin resistance and beta-cell dysfunction. J Biol Chem 2001;276:12162–8
   PubMed Web of Science ®Google Scholar
• Kovar J, Fejfarova V, Pelikanova T, Poledne R. Hyperglycemia downregulates total lipoprotein lipase activity in humans. Physiol Res 2004;53:61–8
   PubMed Web of Science ®Google Scholar
• Rodrigues B, Braun JE, Spooner M, Severson DL. Regulation of lipoprotein lipase activity in cardiac myocytes from control and diabetic rat hearts by plasma lipids. Can J Physiol Pharmacol 1992;70:1271–9
   PubMed Web of Science ®Google Scholar
• Rodrigues B, Spooner M, Severson DL. Free fatty acids do not release lipoprotein lipase from isolated cardiac myocytes or perfused hearts. Am J Physiol 1992;262:E216–23
   PubMed Web of Science ®Google Scholar
• Rodrigues B, Spooner MR, Severson DL. Long term incubation of cardiac myocytes with oleic acid and very-low density lipoprotein reduces heparin-releasable lipoprotein lipase activity. Mol Cell Biochem 1992;116:33–7
   PubMed Web of Science ®Google Scholar
• Vucicevic L, Misirkic M, Janjetovic K, et al. AMP-activated protein kinase-dependent and -independent mechanisms underlying in vitro antiglioma action of compound C. Biochem Pharmacol 2009;77:1684–93
   PubMed Web of Science ®Google Scholar
• Nagata D, Kiyosue A, Takahashi M, et al. A new constitutively active mutant of AMP-activated protein kinase inhibits anoxia-induced apoptosis of vascular endothelial cell. Hypertens Res 2009;32:133–9
   PubMed Web of Science ®Google Scholar
• Catoire M, Alex S, Paraskevopulos N, et al. Fatty acid-inducible ANGPTL4 governs lipid metabolic response to exercise. Proc Natl Acad Sci USA 2014;111:E1043–52
   PubMed Web of Science ®Google Scholar
• O'Brien KD, Ferguson M, Gordon D, et al. Lipoprotein lipase is produced by cardiac myocytes rather than interstitial cells in human myocardium. Arterioscler Thromb 1994;14:1445–51
   PubMedGoogle Scholar
• Yagyu H, Chen G, Yokoyama M, et al. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest 2003;111:419–26
   PubMed Web of Science ®Google Scholar
• Pei-Ling Chiu A, Wang F, Lal N, et al. Endothelial cells respond to hyperglycemia by increasing the LPL transporter GPIHBP1. Am J Physiol Endocrinol Metab 2014;306:E1274–83
   PubMed Web of Science ®Google Scholar
• Wang F, Wan A, Rodrigues B. The function of heparanase in diabetes and its complications. Can J Diabetes 2013;37:332–8
   Web of Science ®Google Scholar
• Wang F, Kim MS, Puthanveetil P, et al. Endothelial heparanase secretion after acute hypoinsulinemia is regulated by glucose and fatty acid. Am J Physiol Heart Circ Physiol 2009;296:H1108–16
   PubMed Web of Science ®Google Scholar
• Wang Y, Chiu AP, Neumaier K, et al. Endothelial cell heparanase taken up by cardiomyocytes regulates lipoprotein lipase transfer to the coronary lumen after diabetes. Diabetes 2014;63:2643–55
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang D, Chiu AP, et al. Endothelial heparanase regulates heart metabolism by stimulating lipoprotein lipase secretion from cardiomyocytes. Arterioscler Thromb Vasc Biol 2013;33:894–902
   PubMed Web of Science ®Google Scholar
• Zhang D, Wan A, Chiu AP, et al. Hyperglycemia-induced secretion of endothelial heparanase stimulates a vascular endothelial growth factor autocrine network in cardiomyocytes that promotes recruitment of lipoprotein lipase. Arterioscler Thromb Vasc Biol 2013;33:2830–8
   PubMed Web of Science ®Google Scholar
• Wang Y, Puthanveetil P, Wang F, et al. Severity of diabetes governs vascular lipoprotein lipase by affecting enzyme dimerization and disassembly. Diabetes 2011;60:2041–50
   PubMed Web of Science ®Google Scholar
• Cazes A, Galaup A, Chomel C, et al. Extracellular matrix-bound angiopoietin-like 4 inhibits endothelial cell adhesion, migration, and sprouting and alters actin cytoskeleton. Circ Res 2006;99:1207–15
   PubMed Web of Science ®Google Scholar
• Galaup A, Cazes A, Le Jan S, et al. Angiopoietin-like 4 prevents metastasis through inhibition of vascular permeability and tumor cell motility and invasiveness. Proc Natl Acad Sci USA 2006;103:18721–6
   PubMed Web of Science ®Google Scholar
• Maalouf RM, Eid AA, Gorin YC, et al. Nox4-derived reactive oxygen species mediate cardiomyocyte injury in early type 1 diabetes. Am J Physiol Cell Physiol 2012;302:C597–604
   PubMed Web of Science ®Google Scholar
• Florini JR, Ewton DZ. Actions of anabolic hormones and growth factors on cultured neonatal heart cells. Growth Regul 1995;5:28–35
   PubMedGoogle Scholar
• Grazul-Bilska AT, Johnson ML, Bilski JJ, et al. Wound healing: the role of growth factors. Drugs Today (Barc) 2003;39:787–800
   PubMed Web of Science ®Google Scholar
• Hetzel M, Bachem M, Anders D, et al. Different effects of growth factors on proliferation and matrix production of normal and fibrotic human lung fibroblasts. Lung 2005;183:225–37
   PubMed Web of Science ®Google Scholar
• Dautzenberg M, Keilhoff G, Just A. Modulation of the myogenic response in renal blood flow autoregulation by NO depends on endothelial nitric oxide synthase (eNOS), but not neuronal or inducible NOS. J Physiol 2011;589:4731–44
   PubMed Web of Science ®Google Scholar
• Prado CM, Rossi MA. Circumferential wall tension due to hypertension plays a pivotal role in aorta remodelling. Int J Exp Pathol 2006;87:425–36
   PubMed Web of Science ®Google Scholar
• Casteilla L, Planat-Benard V, Cousin B, et al. Plasticity of adipose tissue: a promising therapeutic avenue in the treatment of cardiovascular and blood diseases? Arch Mal Coeur Vaiss 2005;98:922–6
   PubMedGoogle Scholar
• Jadhav A, Tiwari S, Lee P, Ndisang JF. The heme oxygenase system selectively enhances the anti-inflammatory macrophage-M2 phenotype, reduces pericardial adiposity, and ameliorated cardiac injury in diabetic cardiomyopathy in Zucker diabetic fatty rats. J Pharmacol Exp Ther 2013;345:239–49
   PubMed Web of Science ®Google Scholar
• Lemstrom KB, Krebs R, Nykanen AI, et al. Vascular endothelial growth factor enhances cardiac allograft arteriosclerosis. Circulation 2002;105:2524–30
   PubMed Web of Science ®Google Scholar
• Li ZL, Ebrahimi B, Zhang X, et al. Obesity-metabolic derangement exacerbates cardiomyocyte loss distal to moderate coronary artery stenosis in pigs without affecting global cardiac function. Am J Physiol Heart Circ Physiol 2014;306:H1087–101
   PubMed Web of Science ®Google Scholar
• Mathieu P, Lemieux I, Despres JP. Obesity, inflammation, and cardiovascular risk. Clin Pharmacol Ther 2010;87:407–16
   PubMed Web of Science ®Google Scholar
• Summers SA. Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 2006;45:42–72
   PubMed Web of Science ®Google Scholar
• Obunike JC, Sivaram P, Paka L, et al. Lipoprotein lipase degradation by adipocytes: receptor-associated protein (RAP)-sensitive and proteoglycan-mediated pathways. J Lipid Res 1996;37:2439–49
   PubMed Web of Science ®Google Scholar
• Sha H, Sun S, Francisco AB, et al. The ER-associated degradation adaptor protein Sel1L regulates LPL secretion and lipid metabolism. Cell Metab 2014;20:458–70
   PubMed Web of Science ®Google Scholar
• Shimada M, Shimano H, Gotoda T, et al. Overexpression of human lipoprotein lipase in transgenic mice. Resistance to diet-induced hypertriglyceridemia and hypercholesterolemia. J Biol Chem 1993;268:17924–9
   PubMed Web of Science ®Google Scholar
• Shimada M, Ishibashi S, Inaba T, et al. Suppression of diet-induced atherosclerosis in low density lipoprotein receptor knockout mice overexpressing lipoprotein lipase. Proc Natl Acad Sci USA 1996;93:7242–6
   PubMed Web of Science ®Google Scholar
• Yagyu H, Ishibashi S, Chen Z, et al. Overexpressed lipoprotein lipase protects against atherosclerosis in apolipoprotein E knockout mice. J Lipid Res 1999;40:1677–85
   PubMed Web of Science ®Google Scholar
• Jensen DR, Schlaepfer IR, Morin CL, et al. Prevention of diet-induced obesity in transgenic mice overexpressing skeletal muscle lipoprotein lipase. Am J Physiol 1997;273:R683–9
   PubMed Web of Science ®Google Scholar
• Ferreira LD, Pulawa LK, Jensen DR, Eckel RH. Overexpressing human lipoprotein lipase in mouse skeletal muscle is associated with insulin resistance. Diabetes 2001;50:1064–8
   PubMed Web of Science ®Google Scholar
• Augustus A, Yagyu H, Haemmerle G, et al. Cardiac-specific knock-out of lipoprotein lipase alters plasma lipoprotein triglyceride metabolism and cardiac gene expression. J Biol Chem 2004;279:25050–7
   PubMed Web of Science ®Google Scholar
• Wang H, Knaub LA, Jensen DR, et al. Skeletal muscle-specific deletion of lipoprotein lipase enhances insulin signaling in skeletal muscle but causes insulin resistance in liver and other tissues. Diabetes 2009;58:116–24
   PubMed Web of Science ®Google Scholar
• Garcia-Arcos I, Hiyama Y, Drosatos K, et al. Adipose-specific lipoprotein lipase deficiency more profoundly affects brown than white fat biology. J Biol Chem 2013;288:14046–58
   PubMed Web of Science ®Google Scholar
• Lee EC, Desai U, Gololobov G, et al. Identification of a new functional domain in angiopoietin-like 3 (ANGPTL3) and angiopoietin-like 4 (ANGPTL4) involved in binding and inhibition of lipoprotein lipase (LPL). J Biol Chem 2009;284:13735–45
   PubMed Web of Science ®Google Scholar
• Takagi A, Ikeda Y, Tsutsumi Z, et al. Molecular studies on primary lipoprotein lipase (LPL) deficiency. One base deletion (G916) in exon 5 of LPL gene causes no detectable LPL protein due to the absence of LPL mRNA transcript. J Clin Invest 1992;89:581–91
   PubMed Web of Science ®Google Scholar
• Nakamura T, Suehiro T, Yasuoka N, et al. A novel nonsense mutation in exon 1 and a transition in intron 3 of the lipoprotein lipase gene. J Atheroscler Thromb 1996;3:17–24
   PubMedGoogle Scholar
• Julien P, Vohl MC, Gaudet D, et al. Hyperinsulinemia and abdominal obesity affect the expression of hypertriglyceridemia in heterozygous familial lipoprotein lipase deficiency. Diabetes 1997;46:2063–8
   PubMed Web of Science ®Google Scholar
• Wang J, Ban MR, Zou GY, et al. Polygenic determinants of severe hypertriglyceridemia. Hum Mol Genet 2008;17:2894–9
   PubMed Web of Science ®Google Scholar
• Radhakutty A, Shen J, Hooper AJ, et al. Quantification and genotyping of lipoprotein lipase in patients with diabetic lipaemia. Diabet Med 2014;31:1702–7
   PubMed Web of Science ®Google Scholar
• Augustus AS, Buchanan J, Park TS, et al. Loss of lipoprotein lipase-derived fatty acids leads to increased cardiac glucose metabolism and heart dysfunction. J Biol Chem 2006;281:8716–23
   PubMed Web of Science ®Google Scholar
• Bharadwaj KG, Hiyama Y, Hu Y, et al. Chylomicron- and VLDL-derived lipids enter the heart through different pathways: in vivo evidence for receptor- and non-receptor-mediated fatty acid uptake. J Biol Chem 2010;285:37976–86
   PubMed Web of Science ®Google Scholar