A novel mechanism by which sdf-1b protects cardiac cells from palmitate-induced endoplasmic reticulum stress and apoptosis via CXCR7 and AMPK/p38 MAPK-Mediated interleukin-6 generation

Diabetes

Volumn 62, Issue 7, 2013, Pages 2545-2558

  Zhao, Yuguang ^a,b   Tan, Yi ^b,c   Xi, Shugang ^a   Li, Yunqian ^a   Li, Cai ^a   Cui, Jiuwei ^a   Yan, Xiaoqing ^b,c   Li, Xiaokun ^c   Wang, Guanjun ^a   Li, Wei ^a   Cai, Lu ^a,b,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c WENZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CHEMOKINE RECEPTOR CXCR7; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PALMITIC ACID; PLASMINOGEN ACTIVATOR INHIBITOR 1; RECOMBINANT INTERLEUKIN 6; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STROMAL CELL DERIVED FACTOR 1BETA; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; ADENYLATE KINASE; CHEMOKINE RECEPTOR CXCR; CHEMOKINE RECEPTOR CXCR4; CMKOR1 PROTEIN, RAT; CXCR4 PROTEIN, RAT; HETEROCYCLIC COMPOUND; PLERIXAFOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DIABETIC CARDIOMYOPATHY; DOWN REGULATION; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; EXPOSURE; HEART MUSCLE CELL; HEART PROTECTION; HYPERTROPHY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LIPID DIET; LIPOTOXICITY; MALE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; UPREGULATION; ANIMAL; CELL LINE; DRUG ANTAGONISM; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION; WISTAR RAT;

ADENYLATE KINASE; ANIMALS; APOPTOSIS; CELL LINE; CHEMOKINE CXCL12; DIABETES MELLITUS, EXPERIMENTAL; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; HETEROCYCLIC COMPOUNDS; INTERLEUKIN-6; MALE; NADPH OXIDASE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PALMITIC ACID; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, CXCR; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION;

EID: 84883673564     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-1233     Document Type: Article

References (62)

1. Zhou YT, Grayburn P, Karim A, et al. Lipotoxic heart disease in obese rats: implications for human obesity. Proc Natl Acad Sci U S A 2000;97:1784-1789
2. Kelly DP, Strauss AW. Inherited cardiomyopathies. N Engl J Med 1994;330: 913-919
3. Rabkin SW, Klassen SS. Palmitate-induced NO production has a dual action to reduce cell death through NO and accentuate cell death through peroxynitrite formation. Prostaglandins Leukot Essent Fatty Acids 2008; 78:147-155
4. Tsang MY, Cowie SE, Rabkin SW. Palmitate increases nitric oxide synthase activity that is involved in palmitate-induced cell death in cardiomyocytes. Nitric Oxide 2004;10:11-19
5. Listenberger LL, Ory DS, Schaffer JE. Palmitate-induced apoptosis can occur through a ceramide-independent pathway. J Biol Chem 2001;276: 14890-14895
6. Wei Y, Wang D, Topczewski F, Pagliassotti MJ. Saturated fatty acids induce endoplasmic reticulum stress and apoptosis independently of ceramide in liver cells. Am J Physiol Endocrinol Metab 2006;291:E275-E281
7. Wang XL, Zhang L, Youker K, et al. Free fatty acids inhibit insulin signalingstimulated endothelial nitric oxide synthase activation through upregulating PTEN or inhibiting Akt kinase. Diabetes 2006;55:2301-2310
8. Yuan H, Zhang X, Huang X, et al. NADPH oxidase 2-derived reactive oxygen species mediate FFAs-induced dysfunction and apoptosis of β-cells via JNK, p38 MAPK and p53 pathways. PLoS ONE 2010;5:e15726
9. Mayer CM, Belsham DD. Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 59 monophosphateactivated protein kinase activation. Endocrinology 2010;151:576-585
10. Kim DS, Jeong SK, Kim HR, Kim DS, Chae SW, Chae HJ. Metformin regulates palmitate-induced apoptosis and ER stress response in HepG2 liver cells. Immunopharmacol Immunotoxicol 2010;32:251-257
11. Terai K, Hiramoto Y, Masaki M, et al. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol Cell Biol 2005;25:9554-9575
12. Kewalramani G, Puthanveetil P, Wang F, et al. AMP-activated protein kinase confers protection against TNF-alpha-induced cardiac cell death. Cardiovasc Res 2009;84:42-53
13. Du JH, Xu N, Song Y, et al. AICAR stimulates IL-6 production via p38 MAPK in cardiac fibroblasts in adult mice: a possible role for AMPK. Biochem Biophys Res Commun 2005;337:1139-1144
14. Tang CH, Chiu YC, Tan TW, Yang RS, Fu WM. Adiponectin enhances IL-6 production in human synovial fibroblast via an AdipoR1 receptor, AMPK, p38, and NF-kappa B pathway. J Immunol 2007;179:5483-5492
15. Kim M, Tian R. Targeting AMPK for cardiac protection: opportunities and challenges. J Mol Cell Cardiol 2011;51:548-553
16. Jones RG, Plas DR, Kubek S, et al. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol Cell 2005;18:283-293
17. Okoshi R, Ozaki T, Yamamoto H, et al. Activation of AMP-activated protein kinase induces p53-dependent apoptotic cell death in response to energetic stress. J Biol Chem 2008;283:3979-3987
18. Calvert JW, Gundewar S, Jha S, et al. Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 2008;57:696-705
19. Paiva MA, Gonçalves LM, Providência LA, Davidson SM, Yellon DM, Mocanu MM. Transitory activation of AMPK at reperfusion protects the ischaemic-reperfused rat myocardium against infarction. Cardiovasc Drugs Ther 2010;24:25-32
20. Gerrits H, van Ingen Schenau DS, Bakker NE, et al. Early postnatal lethality and cardiovascular defects in CXCR7-deficient mice. Genesis 2008; 46:235-245
21. Tan Y, Li Y, Xiao J, et al. A novel CXCR4 antagonist derived from human SDF-1beta enhances angiogenesis in ischaemic mice. Cardiovasc Res 2009; 82:513-521
22. Dai X, Tan Y, Cai S, et al. The role of CXCR7 on the adhesion, proliferation and angiogenesis of endothelial progenitor cells. J Cell Mol Med 2011;15: 1299-1309
23. Yu L, Cecil J, Peng SB, et al. Identification and expression of novel isoforms of human stromal cell-derived factor 1. Gene 2006;374:174-179
24. Altenburg JD, Broxmeyer HE, Jin Q, Cooper S, Basu S, Alkhatib G. A naturally occurring splice variant of CXCL12/stromal cell-derived factor 1 is a potent human immunodeficiency virus type 1 inhibitor with weak chemotaxis and cell survival activities. J Virol 2007;81:8140-8148
25. De La Luz Sierra M, Yang F, Narazaki M, et al. Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood 2004;103:2452-2459
26. Janowski M. Functional diversity of SDF-1 splicing variants. Cell Adhes Migr 2009;3:243-249
27. Ho TK, Tsui J, Xu S, Leoni P, Abraham DJ, Baker DM. Angiogenic effects of stromal cell-derived factor-1 (SDF-1/CXCL12) variants in vitro and the in vivo expressions of CXCL12 variants and CXCR4 in human critical leg ischemia. J Vasc Surg 2010;51:689-699
28. Tang J, Wang J, Yang J, et al. Mesenchymal stem cells over-expressing SDF-1 promote angiogenesis and improve heart function in experimental myocardial infarction in rats. Eur J Cardiothorac Surg 2009;36:644-650
29. Ghadge SK, Mühlstedt S, Ozcelik C, Bader M. SDF-1a as a therapeutic stem cell homing factor in myocardial infarction. Pharmacol Ther 2011;129:97-108
30. Wang Y, Luther K. Genetically manipulated progenitor/stem cells restore function to the infarcted heart via the SDF-1a/CXCR4 signaling pathway. Prog Mol Biol Transl Sci 2012;111:265-284
31. Mu J, Woods J, Zhou YP, et al. Chronic inhibition of dipeptidyl peptidase-4 with a sitagliptin analog preserves pancreatic beta-cell mass and function in a rodent model of type 2 diabetes. Diabetes 2006;55:1695-1704
32. Si Y, Zhao Y, Hao H, et al. Infusion of mesenchymal stem cells ameliorates hyperglycemia in type 2 diabetic rats: identification of a novel role in improving insulin sensitivity. Diabetes 2012;61:1616-1625
33. Cai L, Wang J, Li Y, et al. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 2005;54:1829-1837
34. Cai L, Li W, Wang G, Guo L, Jiang Y, Kang YJ. Hyperglycemia-induced apoptosis in mouse myocardium: mitochondrial cytochrome C-mediated caspase-3 activation pathway. Diabetes 2002;51:1938-1948
35. Cai L, Wang Y, Zhou G, et al. Attenuation by metallothionein of early cardiac cell death via suppression of mitochondrial oxidative stress results in a prevention of diabetic cardiomyopathy. J Am Coll Cardiol 2006;48: 1688-1697
36. Borradaile NM, Han X, Harp JD, Gale SE, Ory DS, Schaffer JE. Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death. J Lipid Res 2006;47:2726-2737
37. Borradaile NM, Buhman KK, Listenberger LL, et al. A critical role for eukaryotic elongation factor 1A-1 in lipotoxic cell death. Mol Biol Cell 2006; 17:770-778
38. Wang X, McLennan SV, Allen TJ, Tsoutsman T, Semsarian C, Twigg SM. Adverse effects of high glucose and free fatty acid on cardiomyocytes are mediated by connective tissue growth factor. Am J Physiol Cell Physiol 2009;297:C1490-C1500
39. Craig R, Larkin A, Mingo AM, et al. p38 MAPK and NF-kappa B collaborate to induce interleukin-6 gene expression and release. Evidence for a cytoprotective autocrine signaling pathway in a cardiac myocyte model system. J Biol Chem 2000;275:23814-23824
40. Kalatskaya I, Berchiche YA, Gravel S, Limberg BJ, Rosenbaum JS, Heveker N. AMD3100 is a CXCR7 ligand with allosteric agonist properties. Mol Pharmacol 2009;75:1240-1247
41. Sierro F, Biben C, Martínez-Muñoz L, et al. Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A 2007;104:14759-14764
42. Cai L, Kang YJ. Cell death and diabetic cardiomyopathy. Cardiovasc Toxicol 2003;3:219-228
43. Gürtl B, Kratky D, Guelly C, et al. Apoptosis and fibrosis are early features of heart failure in an animal model of metabolic cardiomyopathy. Int J Exp Pathol 2009;90:338-346
44. Colamussi ML, Secchiero P, Gonelli A, Marchisio M, Zauli G, Capitani S. Stromal derived factor-1 alpha (SDF-1 alpha) induces CD4+ T cell apoptosis via the functional up-regulation of the Fas (CD95)/Fas ligand (CD95L) pathway. J Leukoc Biol 2001;69:263-270
45. Kortesidis A, Zannettino A, Isenmann S, Shi S, Lapidot T, Gronthos S. Stromal-derived factor-1 promotes the growth, survival, and development of human bone marrow stromal stem cells. Blood 2005;105:3793-3801
46. Hu X, Dai S, Wu WJ, et al. Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation 2007;116:654-663
47. Yano T, Liu Z, Donovan J, Thomas MK, Habener JF. Stromal cell derived factor-1 (SDF-1)/CXCL12 attenuates diabetes in mice and promotes pancreatic beta-cell survival by activation of the prosurvival kinase Akt. Diabetes 2007;56:2946-2957
48. Yin Q, Jin P, Liu X, et al. SDF-1a inhibits hypoxia and serum deprivationinduced apoptosis in mesenchymal stem cells through PI3K/Akt and ERK1/ 2 signaling pathways. Mol Biol Rep 2011;38:9-16
49. Cuadrado A, Nebreda AR. Mechanisms and functions of p38 MAPK signalling. Biochem J 2010;429:403-417
50. Saurin AT, Martin JL, Heads RJ, et al. The role of differential activation of p38-mitogen-activated protein kinase in preconditioned ventricular myocytes. FASEB J 2000;14:2237-2246
51. Huang Y, Zheng J, Fan P, Zhang X. Transfection of antisense p38 alpha gene ameliorates myocardial cell injury mediated by hypoxia and burn serum. Burns 2007;33:599-605
52. Liu H, Pedram A, Kim JK. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38a-mediated activation of p53 and by down-regulating p53 inhibition on p38b. Cardiovasc Res 2011;89:119-128
53. Venkatakrishnan CD, Tewari AK, Moldovan L, et al. Heat shock protects cardiac cells from doxorubicin-induced toxicity by activating p38 MAPK and phosphorylation of small heat shock protein 27. Am J Physiol Heart Circ Physiol 2006;291:H2680-H2691
54. Smart N, Mojet MH, Latchman DS, Marber MS, Duchen MR, Heads RJ. IL-6 induces PI 3-kinase and nitric oxide-dependent protection and preserves mitochondrial function in cardiomyocytes. Cardiovasc Res 2006;69:164-177
55. Cacicedo JM, Benjachareonwong S, Chou E, Yagihashi N, Ruderman NB, Ido Y. Activation of AMP-activated protein kinase prevents lipotoxicity in retinal pericytes. Invest Ophthalmol Vis Sci 2011;52:3630-3639
56. Bakondi B, Shimada IS, Peterson BM, Spees JL. SDF-1a secreted by human CD133-derived multipotent stromal cells promotes neural progenitor cell survival through CXCR7. Stem Cells Dev 2011;20:1021-1029
57. Hattermann K, Held-Feindt J, Lucius R, et al. The chemokine receptor CXCR7 is highly expressed in human glioma cells and mediates antiapoptotic effects. Cancer Res 2010;70:3299-3308
58. Ménard SL, Croteau E, Sarrhini O, et al. Abnormal in vivo myocardial energy substrate uptake in diet-induced type 2 diabetic cardiomyopathy in rats. Am J Physiol Endocrinol Metab 2010;298:E1049-E1057
59. Ti Y, Xie GL, Wang ZH, et al. TRB3 gene silencing alleviates diabetic cardiomyopathy in a type 2 diabetic rat model. Diabetes 2011;60:2963-2974
60. Bai SZ, Sun J, Wu H, et al. Decrease in calcium-sensing receptor in the progress of diabetic cardiomyopathy. Diabetes Res Clin Pract 2012;95:378- 385
61. Huang C, Gu H, Zhang W, Manukyan MC, Shou W, Wang M. SDF-1/CXCR4 mediates acute protection of cardiac function through myocardial STAT3 signaling following global ischemia/reperfusion injury. Am J Physiol Heart Circ Physiol 2011;301:H1496-H1505
62. Ziegler M, Elvers M, Baumer Y, et al. The bispecific SDF1-GPVI fusion protein preserves myocardial function after transient ischemia in mice. Circulation 2012;125:685-696