Deep sequence analysis of gene expression identifies osteopontin as a downstream effector of integrin-linked kinase (ILK) in cardiac-specific ILK knockout mice

Circulation: Heart Failure

Volumn 7, Issue 1, 2014, Pages 184-193

  Dai, Jing ^a,b   Matsui, Takashi ^c   Abel, E Dale ^d   Dedhar, Shoukat ^e   Gerszten, Robert E ^b   Seidman, Christine E ^f,g   Seidman, J G ^b   Rosenzweig, Anthony ^a,b  

^a BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF HAWAII   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Cardiomyopathy, dilated; Gene expression profiling; Integrin linked kinase; Osteopontin

Indexed keywords

BLOCKING ANTIBODY; CHEMOKINE; COMPLEMENTARY DNA; CRE RECOMBINASE; INTEGRIN LINKED KINASE; MYOSIN HEAVY CHAIN; OSTEOPONTIN; SERINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; CARDITIS; CELL DEATH; CONGESTIVE CARDIOMYOPATHY; CONTROLLED STUDY; FIBROSIS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENOTYPE; HEART FAILURE; HEART MUSCLE CELL; HEAVY CHAIN; KNOCKOUT MOUSE; MOLECULAR CLONING; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TRANSDUCER;

CARDIOMYOPATHY, DILATED; GENE EXPRESSION PROFILING; INTEGRIN-LINKED KINASE; OSTEOPONTIN;

ANIMALS; ANTIBODIES; APOPTOSIS; CARDIOMYOPATHY, DILATED; DISEASE MODELS, ANIMAL; FEMALE; GENOTYPE; HEART FAILURE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCYTES, CARDIAC; NECROSIS; OSTEOPONTIN; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTOME;

EID: 84896040762     PISSN: 19413289     EISSN: 19413297     Source Type: Journal    
DOI: 10.1161/CIRCHEARTFAILURE.113.000649     Document Type: Article

References (42)

1. Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J, Bell JC, Dedhar S. Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature. 1996;379:91-96.
2. Legate KR, Montañez E, Kudlacek O, Fässler R. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol. 2006;7:20-31.
3. Lu H, Fedak PW, Dai X, Du C, Zhou YQ, Henkelman M, Mongroo PS, Lau A, Yamabi H, Hinek A, Husain M, Hannigan G, Coles JG. Integrinlinked kinase expression is elevated in human cardiac hypertrophy and induces hypertrophy in transgenic mice. Circulation. 2006;114:2271-2279.
4. Knöll R, Postel R, Wang J, Krätzner R, Hennecke G, Vacaru AM, Vakeel P, Schubert C, Murthy K, Rana BK, Kube D, Knöll G, Schäfer K, Hayashi T, Holm T, Kimura A, Schork N, Toliat MR, Nürnberg P, Schultheiss HP, Schaper W, Schaper J, Bos E, Den Hertog J, van Eeden FJ, Peters PJ, Hasenfuss G, Chien KR, Bakkers J. Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation. 2007;116:515-525.
5. Bendig G, Grimmler M, Huttner IG, Wessels G, Dahme T, Just S, Trano N, Katus HA, Fishman MC, Rottbauer W. Integrin-linked kinase, a novel component of the cardiac mechanical stretch sensor, controls contractility in the zebrafish heart. Genes Dev. 2006;20:2361-2372.
6. Wickström SA, Lange A, Montanez E, Fässler R. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 2010;29:281-291.
7. White DE, Coutu P, Shi YF, Tardif JC, Nattel S, St Arnaud R, Dedhar S, Muller WJ. Targeted ablation of ILK from the murine heart results in dilated cardiomyopathy and spontaneous heart failure. Genes Dev. 2006;20:2355-2360.
8. Wang HV, Chang LW, Brixius K, Wickström SA, Montanez E, Thievessen I, Schwander M, Müller U, Bloch W, Mayer U, Fässler R. Integrin-linked kinase stabilizes myotendinous junctions and protects muscle from stress-induced damage. J Cell Biol. 2008;180:1037-1049.
9. Pereira JA, Benninger Y, Baumann R, Gonçalves AF, Ozçelik M, Thurnherr T, Tricaud N, Meijer D, Fässler R, Suter U, Relvas JB. Integrin-linked kinase is required for radial sorting of axons and Schwann cell remyelination in the peripheral nervous system. J Cell Biol. 2009;185:147-161.
10. Lange A, Wickström SA, Jakobson M, Zent R, Sainio K, Fässler R. Integrin-linked kinase is an adaptor with essential functions during mouse development. Nature. 2009;461:1002-1006.
11. Peng X, Kraus MS, Wei H, Shen TL, Pariaut R, Alcaraz A, Ji G, Cheng L, Yang Q, Kotlikoff MI, Chen J, Chien K, Gu H, Guan JL. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J Clin Invest. 2006;116:217-227.
12. Yang ZZ, Tschopp O, Hemmings-Mieszczak M, Feng J, Brodbeck D, Perentes E, Hemmings BA. Protein kinase B alpha/Akt1 regulates placental development and fetal growth. J Biol Chem. 2003;278:32124-32131.
13. Chen WS, Xu PZ, Gottlob K, Chen ML, Sokol K, Shiyanova T, Roninson I, Weng W, Suzuki R, Tobe K, Kadowaki T, Hay N. Growth retardation and increased apoptosis in mice with homozygous disruption of the Akt1 gene. Genes Dev. 2001;15:2203-2208.
14. Liang X, Sun Y, Ye M, Scimia MC, Cheng H, Martin J, Wang G, Rearden A, Wu C, Peterson KL, Powell HC, Evans SM, Chen J. Targeted ablation of PINCH1 and PINCH2 from murine myocardium results in dilated cardiomyopathy and early postnatal lethality. Circulation. 2009;120:568-576.
15. Shai SY, Harpf AE, Babbitt CJ, Jordan MC, Fishbein MC, Chen J, Omura M, Leil TA, Becker KD, Jiang M, Smith DJ, Cherry SR, Loftus JC, Ross RS. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res. 2002;90:458-464.
16. Kim JB, Porreca GJ, Song L, Greenway SC, Gorham JM, Church GM, Seidman CE, Seidman JG. Polony multiplex analysis of gene expression (PMAGE) in mouse hypertrophic cardiomyopathy. Science. 2007;316:1481-1484.
17. Satoh M, Nakamura M, Akatsu T, Shimoda Y, Segawa I, Hiramori K. Myocardial osteopontin expression is associated with collagen fibrillogenesis in human dilated cardiomyopathy. Eur J Heart Fail. 2005;7:755-762.
18. Rosenberg M, Zugck C, Nelles M, Juenger C, Frank D, Remppis A, Giannitsis E, Katus HA, Frey N. Osteopontin, a new prognostic biomarker in patients with chronic heart failure. Circ Heart Fail. 2008;1:43-49.
19. Renault MA, Robbesyn F, Réant P, Douin V, Daret D, Allières C, Belloc I, Couffinhal T, Arnal JF, Klingel K, Desgranges C, Dos Santos P, Charpentier F, Gadeau AP. Osteopontin expression in cardiomyocytes induces dilated cardiomyopathy. Circ Heart Fail. 2010;3:431-439.
20. Abel ED, Kaulbach HC, Tian R, Hopkins JC, Duffy J, Doetschman T, Minnemann T, Boers ME, Hadro E, Oberste-Berghaus C, Quist W, Lowell BB, Ingwall JS, Kahn BB. Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart. J Clin Invest. 1999;104:1703-1714.
21. Troussard AA, Mawji NM, Ong C, Mui A, St -Arnaud R, Dedhar S. Conditional knock-out of integrin-linked kinase demonstrates an essential role in protein kinase B/Akt activation. J Biol Chem. 2003;278:22374-22378.
22. Dai J, Li W, Chang L, Zhang Z, Tang C, Wang N, Zhu Y, Wang X. Role of redox factor-1 in hyperhomocysteinemia-accelerated atherosclerosis. Free Radic Biol Med. 2006;41:1566-1577.
23. Aoyama T, Matsui T, Novikov M, Park J, Hemmings B, Rosenzweig A. Serum and glucocorticoid-responsive kinase-1 regulates cardiomyocyte survival and hypertrophic response. Circulation. 2005;111:1652-1659.
24. Cook SA, Matsui T, Li L, Rosenzweig A. Transcriptional effects of chronic Akt activation in the heart. J Biol Chem. 2002;277:22528-22533.
25. Christodoulou DC, Gorham JM, Kawana M, DePalma SR, Herman DS, Wakimoto H. Quantification of gene transcripts with deep sequencing analysis of gene expression (DSAGE) using 1 to 2 microg total RNA. Curr Protoc Mol Biol. 2011;25:25B.9.1-25B.9.16.
26. Audic S, Claverie JM. The significance of digital gene expression profiles. Genome Res. 1997;7:986-995.
27. Whelan RS, Kaplinskiy V, Kitsis RN. Cell death in the pathogenesis of heart disease: mechanisms and significance. Annu Rev Physiol. 2010;72:19-44.
28. Ashkar S, Weber GF, Panoutsakopoulou V, Sanchirico ME, Jansson M, Zawaideh S, Rittling SR, Denhardt DT, Glimcher MJ, Cantor H. Eta-1 (osteopontin): an early component of type-1 (cell-mediated) immunity. Science. 2000;287:860-864.
29. Xie Z, Singh M, Singh K. Osteopontin modulates myocardial hypertrophy in response to chronic pressure overload in mice. Hypertension. 2004;44:826-831.
30. Graf K, Do YS, Ashizawa N, Meehan WP, Giachelli CM, Marboe CC, Fleck E, Hsueh WA. Myocardial osteopontin expression is associated with left ventricular hypertrophy. Circulation. 1997;96:3063-3071.
31. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ. Akt1 is required for physiological cardiac growth. Circulation. 2006;113:2097-2104.
32. Ashizawa N, Graf K, Do YS, Nunohiro T, Giachelli CM, Meehan WP, Tuan TL, Hsueh WA. Osteopontin is produced by rat cardiac fibroblasts and mediates A(II)-induced DNA synthesis and collagen gel contraction. J Clin Invest. 1996;98:2218-2227.
33. Singh K, Balligand JL, Fischer TA, Smith TW, Kelly RA. Glucocorticoids increase osteopontin expression in cardiac myocytes and microvascular endothelial cells. Role in regulation of inducible nitric oxide synthase. J Biol Chem. 1995;270:28471-28478.
34. Murry CE, Giachelli CM, Schwartz SM, Vracko R. Macrophages express osteopontin during repair of myocardial necrosis. Am J Pathol. 1994;145:1450-1462.
35. Caglayan E, Stauber B, Collins AR, Lyon CJ, Yin F, Liu J, Rosenkranz S, Erdmann E, Peterson LE, Ross RS, Tangirala RK, Hsueh WA. Differential roles of cardiomyocyte and macrophage peroxisome proliferator-activated receptor gamma in cardiac fibrosis. Diabetes. 2008;57:2470-2479.
36. Subramanian V, Krishnamurthy P, Singh K, Singh M. Lack of osteopontin improves cardiac function in streptozotocin-induced diabetic mice. Am J Physiol Heart Circ Physiol. 2007;292:H673-H683.
37. Deschamps AM, Spinale FG. Pathways of matrix metalloproteinase induction in heart failure: bioactive molecules and transcriptional regulation. Cardiovasc Res. 2006;69:666-676.
38. Philip S, Kundu GC. Osteopontin induces nuclear factor kappa B-mediated promatrix metalloproteinase-2 activation through I kappa B alpha/IKK signaling pathways, and curcumin (diferulolylmethane) down-regulates these pathways. J Biol Chem. 2003;278:14487-14497.
39. Rangaswami H, Bulbule A, Kundu GC. Nuclear factor-inducing kinase plays a crucial role in osteopontin-induced MAPK/IkappaBalpha kinase- dependent nuclear factor kappaB-mediated promatrix metalloproteinase- 9 activation. J Biol Chem. 2004;279:38921-38935.
40. Gkretsi V, Mars WM, Bowen WC, Barua L, Yang Y, Guo L, St-Arnaud R, Dedhar S, Wu C, Michalopoulos GK. Loss of integrin linked kinase from mouse hepatocytes in vitro and in vivo results in apoptosis and hepatitis. Hepatology. 2007;45:1025-1034.
41. Hortelano S, López-Fontal R, Través PG, Villa N, Grashoff C, Boscá L, Luque A. ILK mediates LPS-induced vascular adhesion receptor expression and subsequent leucocyte trans-endothelial migration. Cardiovasc Res. 2010;86:283-292.
42. Assi K, Patterson S, Dedhar S, Owen D, Levings M, Salh B. Role of epithelial integrin-linked kinase in promoting intestinal inflammation: effects on CCL2, fibronectin and the T cell repertoire. BMC Immunol. 2011;12:42.