Cardiac overexpression of hormone-sensitive lipase inhibits myocardial steatosis and fibrosis in streptozotocin diabetic mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 294, Issue 6, 2008, Pages

  Ueno, Masami ^a   Suzuki, Jinya ^a   Zenimaru, Yasuo ^a   Takahashi, Sadao ^a   Koizumi, Tsutomu ^a   Noriki, Sakon ^a   Yamaguchi, Osamu ^b   Otsu, Kinya ^b   Shen, Wen Jun ^c,d   Kraemer, Fredric B ^c,d   Miyamori, Isamu ^a  

^a UNIVERSITY OF FUKUI   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Animal model; Lipolysis; Lipotoxicity; Transgenic mice

Indexed keywords

COLLAGEN; HORMONE SENSITIVE LIPASE; MESSENGER RNA; METALLOTHIONEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; CHOLESTEROL; CHOLESTEROL ESTERASE; FATTY ACID; INSULIN; LIPOPROTEIN LIPASE; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLLAGEN SYNTHESIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE OVEREXPRESSION; HEART MUSCLE FIBROSIS; HISTOPATHOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEATOSIS; STREPTOZOCIN DIABETES; TISSUE SPECIFICITY; TRANSGENIC MOUSE; ANIMAL; BIOSYNTHESIS; BLOOD; C57BL MOUSE; CARDIOMYOPATHY; CROSS BREEDING; DBA MOUSE; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; FEMALE; FIBROSIS; GENETICS; GLUCOSE BLOOD LEVEL; MALE; METABOLISM; PATHOLOGY;

ANIMALS; BLOOD GLUCOSE; CARDIOMYOPATHIES; CHOLESTEROL; CROSSES, GENETIC; DIABETES MELLITUS, EXPERIMENTAL; FATTY ACIDS, NONESTERIFIED; FEMALE; FIBROSIS; INSULIN; LIPOPROTEIN LIPASE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MICROSCOPY, ELECTRON; PPAR ALPHA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; STEROL ESTERASE; TRIGLYCERIDES;

EID: 47549089671     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00016.2008     Document Type: Article

References (52)

1. Asayama K, Sandhir R, Sheikh FG, Hayashibe H, Nakane T, Singh I. Increased peroxisomal fatty acid beta-oxidation and enhanced expression of peroxisome proliferator-activated receptor-alpha in diabetic rat liver. Mol Cell Biochem 194: 227-234, 1999.
2. Asbun J, Villarreal FJ. The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J Am Coll Cardiol 47: 693-700, 2006.
3. Belke DD, Betuing S, Tuttle MJ, Graveleau C, Young ME, Pham M, Zhang D, Cooksey RC, McClain DA, Litwin SE, Taegtmeyer H, Severson D, Kahn CR, Abel ED. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J Clin Invest 109: 629-639, 2002.
4. Bell DS. Diabetic cardiomyopathy. A unique entity or a complication of coronary artery disease? Diabetes Care 18: 708-714, 1995.
5. Cai L. Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic Biol Med 41: 851-861, 2006.
6. Chiu HC, Kovacs A, Blanton RM, Han X, Courtois M, Weinheimer CJ, Yamada KA, Brunet S, Xu H, Nerbonne JM, Welch MJ, Fettig NM, Sharp TL, Sambandam N, Olson KM, Ory DS, Schaffer JE. Transgenic expression of fatty acid transport protein 1 in the heart causes lipotoxic cardiomyopathy. Circ Res 96: 225-233, 2005.
7. Das Evcimen N, King GL. The role of protein kinase C activation and the vascular complications of diabetes. Pharmacol Res 55: 498-510, 2007.
8. Dewald O, Sharma S, Adrogue J, Salazar R, Duerr GD, Crapo JD, Entman ML, Taegtmeyer H. Downregulation of peroxisome proliferator-activated receptor-alpha gene expression in a mouse model of ischemic cardiomyopathy is dependent on reactive oxygen species and prevents lipotoxicity. Circulation 112: 407-415, 2005.
9. Dong F, Li Q, Sreejayan N, Nunn JM, Ren J. Metallothionein prevents high-fat diet induced cardiac contractile dysfunction: role of peroxisome proliferator activated receptor gamma coactivator 1alpha and mitochondrial biogenesis. Diabetes 56: 2201-2212, 2007.
10. Escary JL, Choy HA, Reue K, Wang XP, Castellani LW, Glass CK, Lusis AJ, Schotz MC. Paradoxical effect on atherosclerosis of hormone-sensitive lipase overexpression in macrophages. J Lipid Res 40: 397-404, 1999.
11. Finck BN, Lehman JJ, Leone TC, Welch MJ, Bennett MJ, Kovacs A, Han X, Gross RW, Kozak R, Lopaschuk GD, Kelly DP. The cardiac phenotype induced by PPARalpha overexpression mimics that caused by diabetes mellitus. J Clin Invest 109: 121-130, 2002.
12. Finck BN, Han X, Courtois M, Aimond F, Nerbonne JM, Kovacs A, Gross RW, Kelly DP. A critical role for PPARalpha-mediated lipotoxicity in the pathogenesis of diabetic cardiomyopathy: modulation by dietary fat content. Proc Natl Acad Sci USA 100: 1226-1231, 2003.
13. Haemmerle G, Zimmermann R, Hayn M, Theussl C, Waeg G, Wagner E, Sattler W, Magin TM, Wagner EF, Zechner R. Hormone-sensitive lipase deficiency in mice causes diglyceride accumulation in adipose tissue, muscle, and testis. J Biol Chem 277: 4806-4815, 2002.
14. Haemmerle G, Lass A, Zimmermann R, Gorkiewicz G, Meyer C, Rozman J, Heldmaier G, Maier R, Theussl C, Eder S, Kratky D, Wagner EF, Klingenspor M, Hoefler G, Zechner R. Defective lipolysis and altered energy metabolism in mice lacking adipose triglyceride lipase. Science 312: 734-737, 2006.
15. Hamilton JA, Guo W, Kamp F. Mechanism of cellular uptake of long-chain fatty acids: Do we need cellular proteins? Mol Cell Biochem 239: 17-23, 2002.
16. Holm C, Kirchgessner TG, Svenson KL, Fredrikson G, Nilsson S, Miller CG, Shively JE, Heinzmann C, Sparkes RS, Mohandas T, Lusis AJ, Belfrage P, Schotz MC. Hormone-sensitive lipase: sequence, expression, and chromosomal localization to 19 cent-q13.3. Science 241: 1503-1506, 1988.
17. Holm C, Osterlund T, Laurell H, Contreras JA. Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Annu Rev Nutr 20: 365-393, 2000.
18. Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL. Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci USA 89: 11059-11063, 1992.
19. Junqueira LC, Bignolas G, Brentani RR. Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11: 447-455, 1979.
20. Kanehara H, Suzuki J, Zenimaru Y, Takahashi S, Oida K, Shen WJ, Kraemer FB, Miyamori I. Function of hormone-sensitive lipase in diacylglycerol-protein kinase C pathway. Diabetes Res Clin Pract 65: 209-215, 2004.
21. Kang YJ, Chen Y, Yu A, Voss-McCowan M, Epstein PN. Overexpression of metallothionein in the heart of transgenic mice suppresses doxorubicin cardiotoxicity. J Clin Invest 100: 1501-1506, 1997.
22. Kraemer FB, Patel S, Saedi MS, Sztalryd C. Detection of hormone-sensitive lipase in various tissues. I. Expression of an HSL/bacterial fusion protein and generation of anti-HSL antibodies. J Lipid Res 34: 663-671, 1993.
23. Kraemer FB, Shen WJ. Hormone-sensitive lipase: control of intracellular tri-(di-)acylglycerol and cholesteryl ester hydrolysis. J Lipid Res 43: 1585-1594, 2002.
24. Kuriyama H, Liang G, Engelking LJ, Horton JD, Goldstein JL, Brown MS. Compensatory increase in fatty acid synthesis in adipose tissue of mice with conditional deficiency of SCAP in liver. Cell Metab 1: 41-51, 2005.
25. Lucas S, Tavernier G, Tiraby C, Mairal A, Langin D. Expression of human hormone-sensitive lipase in white adipose tissue of transgenic mice increases lipase activity but does not enhance in vitro lipolysis. J Lipid Res 44: 154-163, 2003.
26. Maxwell MA, Cleasby ME, Harding A, Stark A, Cooney GJ, Muscat GE. Nur77 regulates lipolysis in skeletal muscle cells. Evidence for cross-talk between the beta-adrenergic and an orphan nuclear hormone receptor pathway. J Biol Chem 280: 12573-12584, 2005.
27. Murphy E, Steenbergen C. Cardioprotection in females: a role for nitric oxide and altered gene expression. Heart Fail Rev 12: 293-300, 2007.
28. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13: 619-624, 2007.
29. Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95: 351-358, 1979.
30. Park SY, Kim HJ, Wang S, Higashimori T, Dong J, Kim YJ, Cline G, Li H, Prentki M, Shulman GI, Mitchell GA, Kim JK. Hormonesensitive lipase knockout mice have increased hepatic insulin sensitivity and are protected from short-term diet-induced insulin resistance in skeletal muscle and heart. Am J Physiol Endocrinol Metab 289: E30-E39, 2005.
31. Park TS, Yamashita H, Blaner WS, Goldberg IJ. Lipids in the heart: a source of fuel and a source of toxins. Curr Opin Lipidol 18: 277-282, 2007.
32. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 98: 596-605, 2006.
33. Preiss J, Loomis CR, Bishop WR, Stein R, Niedel JE, Bell RM. Quantitative measurement of sn-1,2-diacylglycerols present in platelets, hepatocytes, and ras- and sis-transformed normal rat kidney cells. J Biol Chem 261: 8597-8600, 1986.
34. Pruimboom-Brees I, Haghpassand M, Royer L, Brees D, Aldinger C, Reagan W, Singh J, Kerlin R, Kane C, Bagley S, Hayward C, Loy J, O'Brien P, Francone OL. A critical role for peroxisomal proliferator-activated receptor-alpha nuclear receptors in the development of cardiomyocyte degeneration and necrosis. Am J Pathol 169: 750-760, 2006.
35. Regan TJ, Lyons MM, Ahmed SS, Levinson GE, Oldewurtel HA, Ahmad MR, Haider B. Evidence for cardiomyopathy in familial diabetes mellitus. J Clin Invest 60: 884-899, 1977.
36. Rosenkranz S. TGF-beta1 and angiotensin networking in cardiac remodeling. Cardiovasc Res 63: 423-432, 2004.
37. Rubler S, Dlugash J, Yuceoglu YZ, Kumral T, Branwood AW, Grishman A. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30: 595-602, 1972.
38. Son NH, Park TS, Yamashita H, Yokoyama M, Huggins LA, Okajima K, Homma S, Szabolcs MJ, Huang LS, Goldberg IJ. Cardiomyocyte expression of PPARgamma leads to cardiac dysfunction in mice. J Clin Invest 117: 2791-2801, 2007.
39. Subramaniam A, Gulick J, Neumann J, Knotts S, Robbins J. Transgenic analysis of the thyroid-responsive elements in the alpha-cardiac myosin heavy chain gene promoter. J Biol Chem 268: 4331-4336, 1993.
40. Suzuki J, Kanehara H, Takahashi S, Oida K, Osuga J, Ishibashi S, Shen WJ, Kraemer FB, Miyamori I. Paradoxical regulation of cardiac lipases and lipid accumulation in hormone-sensitive lipase knockout mice (Abstract). Diabetes 53, Suppl 2: A338, 2004.
41. Suzuki J, Shen WJ, Nelson BD, Patel S, Veerkamp JH, Selwood SP, Murphy GM Jr, Reaven E, Kraemer FB. Absence of cardiac lipid accumulation in transgenic mice with heart-specific HSL overexpression. Am J Physiol Endocrinol Metab 281: E857-E866, 2001.
42. Suzuki J, Shen WJ, Nelson BD, Selwood SP, Murphy GM Jr, Kanehara H, Takahashi S, Oida K, Miyamori I, Kraemer FB. Cardiac gene expression profile and lipid accumulation in response to starvation. Am J Physiol Endocrinol Metab 283: E94-E102, 2002.
43. Sztalryd C, Kraemer FB. Regulation of hormone-sensitive lipase in streptozotocin-induced diabetic rats. Metabolism 44: 1391-1396, 1995.
44. Unger RH, Orci L. Diseases of liporegulation: new perspective on obesity and related disorders. FASEB J 15: 312-321, 2001.
45. Uno K, Katagiri H, Yamada T, Ishigaki Y, Ogihara T, Imai J, Hasegawa Y, Gao J, Kaneko K, Iwasaki H, Ishihara H, Sasano H, Inukai K, Mizuguchi H, Asano T, Shiota M, Nakazato M, Oka Y. Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity. Science 312: 1656-1659, 2006.
46. Valmaseda A, Carmona MC, Barbera MJ, Vinas O, Mampel T, Iglesias R, Villarroya F, Giralt M. Opposite regulation of PPAR-alpha and -gamma gene expression by both their ligands and retinoic acid in brown adipocytes. Mol Cell Endocrinol 154: 101-109, 1999.
47. Westermann D, Rutschow S, Jager S, Linderer A, Anker S, Riad A, Unger T, Schultheiss HP, Pauschinger M, Tschope C. Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy: the role of angiotensin type 1 receptor antagonism. Diabetes 56: 641-646, 2007.
48. Winzell MS, Svensson H, Enerback S, Ravnskjaer K, Mandrup S, Esser V, Arner P, Alves-Guerra MC, Miroux B, Sundler F, Ahren B, Holm C. Pancreatic beta-cell lipotoxicity induced by overexpression of hormone-sensitive lipase. Diabetes 52: 2057-2065, 2003.
49. 2+ cycling proteins, NADPH oxidase, poly(ADP-Ribose) polymerase and myosin heavy chain isozyme. Free Radic Biol Med 40: 1419-1429, 2006.
50. Yagyu H, Chen G, Yokoyama M, Hirata K, Augustus A, Kako Y, Seo T, Hu Y, Lutz EP, Merkel M, Bensadoun A, Homma S, Goldberg IJ. Lipoprotein lipase (LpL) on the surface of cardiomyocytes increases lipid uptake and produces a cardiomyopathy. J Clin Invest 111: 419-426, 2003.
51. Zhou YT, Grayburn P, Karim A, Shimabukuro M, Higa M, Baetens D, Orci L, Unger RH. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci USA 97: 1784-1789, 2000.
52. Zimmermann R, Strauss JG, Haemmerle G, Schoiswohl G, Birner-Gruenberger R, Riederer M, Lass A, Neuberger G, Eisenhaber F, Hermetter A, Zechner R. Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306: 1383-1386, 2004.