Zinc rescues obesity-induced cardiac hypertrophy via stimulating metallothionein to suppress oxidative stress-activated BCL10/CARD9/p38 MAPK pathway

Journal of Cellular and Molecular Medicine

Volumn 21, Issue 6, 2017, Pages 1182-1192

  Wang, Shudong ^a,b   Gu, Junlian ^b   Xu, Zheng ^a,b   Zhang, Zhiguo ^a   Bai, Tao ^a   Xu, Jianxiang ^b   Cai, Jun ^b   Barnes, Gregory ^b,c   Liu, Qiu Ju ^a   Freedman, Jonathan H ^b   Wang, Yonggang ^a   Liu, Quan ^a   Zheng, Yang ^a   Cai, Lu ^b,c  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

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

^c UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

BCL10; CARD9; obesity related cardiac hypertrophy; p38 MAPK; zinc

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; ATRIAL NATRIURETIC FACTOR; CASPASE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; METALLOTHIONEIN; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; NUTRITION SUPPLEMENT; PALMITIC ACID; PROTEIN BCL 10; SMALL INTERFERING RNA; ZINC; B CELL LYMPHOMA/LEUKEMIA 10; BCL10 PROTEIN, MOUSE; CARD9 PROTEIN, MOUSE; IMIDAZOLE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE P38; PYRIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIAC MUSCLE CELL; CONTROLLED STUDY; GENETIC TRANSFECTION; HEART VENTRICLE HYPERTROPHY; IMMUNOFLUORESCENCE TEST; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; OBESITY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING; ZINC DEFICIENCY; ANIMAL; CARDIOMEGALY; COMPLICATION; DEFICIENCY; DIETARY SUPPLEMENT; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LIPID DIET; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; B-CELL CLL-LYMPHOMA 10 PROTEIN; CARD SIGNALING ADAPTOR PROTEINS; CARDIOMEGALY; DIET, HIGH-FAT; DIETARY SUPPLEMENTS; GENE EXPRESSION REGULATION; HUMANS; IMIDAZOLES; METALLOTHIONEIN; MICE; MYOCYTES, CARDIAC; OBESITY; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PYRIDINES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; ZINC;

EID: 85012974131     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.13050     Document Type: Article

References (50)

1. Leopold JA. Obesity-related cardiomyopathy is an adipocyte-mediated paracrine disease. Trends Cardiovasc Med. 2015; 25: 127–8.
2. Daniels SR, Jacobson MS, McCrindle BW, et al. American Heart Association childhood obesity research summit: executive summary. Circulation. 2009; 119: 2114–23.
3. Pearson G, Robinson F, Beers Gibson T, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001; 22: 153–83.
4. Qi Y, Xu Z, Zhu Q, et al. Myocardial loss of IRS1 and IRS2 causes heart failure and is controlled by p38alpha MAPK during insulin resistance. Diabetes. 2013; 62: 3887–900.
5. Yang J, Mou Y, Wu T, et al. Cardiac-specific overexpression of farnesyl pyrophosphate synthase induces cardiac hypertrophy and dysfunction in mice. Cardiovasc Res. 2013; 97: 490–9.
6. Wang S, Luo M, Zhang Z, et al. Zinc deficiency exacerbates while zinc supplement attenuates cardiac hypertrophy in high-fat diet-induced obese mice through modulating p38 MAPK-dependent signaling. Toxicol Lett. 2016; 258: 134–46.
7. Bertin J, Guo Y, Wang L, et al. CARD9 is a novel caspase recruitment domain-containing protein that interacts with BCL10/CLAP and activates NF-kappa B. J Biol Chem. 2000; 275: 41082–6.
8. Hsu YM, Zhang Y, You Y, et al. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat Immunol. 2007; 8: 198–205.
9. Ashwell JD. The many paths to p38 mitogen-activated protein kinase activation in the immune system. Nat Rev Immunol. 2006; 6: 532–40.
10. Willis TG, Jadayel DM, Du MQ, et al. Bcl10 is involved in t(1;14)(p22;q32) of MALT B cell lymphoma and mutated in multiple tumor types. Cell. 1999; 96: 35–45.
11. Ruland J, Duncan GS, Elia A, et al. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-kappaB and neural tube closure. Cell. 2001; 104: 33–42.
12. Borthakur A, Bhattacharyya S, Dudeja PK, et al. Carrageenan induces interleukin-8 production through distinct Bcl10 pathway in normal human colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol. 2007; 292: G829–38.
13. Wang D, You Y, Lin PC, et al. Bcl10 plays a critical role in NF-kappaB activation induced by G protein-coupled receptors. Proc Natl Acad Sci USA. 2007; 104: 145–50.
14. Bhattacharyya S, Xue L, Devkota S, et al. Carrageenan-induced colonic inflammation is reduced in Bcl10 null mice and increased in IL-10-deficient mice. Mediators Inflamm. 2013; 2013: 397642.
15. Van Beek M, Oravecz-Wilson KI, Delekta PC, et al. Bcl10 links saturated fat overnutrition with hepatocellular NF-kB activation and insulin resistance. Cell Rep. 2012; 1: 444–52.
16. Zhao XQ, Zhu LL, Chang Q, et al. C-type lectin receptor dectin-3 mediates trehalose 6,6′-dimycolate (TDM)-induced Mincle expression through CARD9/Bcl10/MALT1-dependent nuclear factor (NF)-kappaB activation. J Biol Chem. 2014; 289: 30052–62.
17. Jayawardena R, Ranasinghe P, Galappatthy P, et al. Effects of zinc supplementation on diabetes mellitus: a systematic review and meta-analysis. Diabetol Metab Syndr. 2012; 4: 13.
18. Khan MI, Siddique KU, Ashfaq F, et al. Effect of high-dose zinc supplementation with oral hypoglycemic agents on glycemic control and inflammation in type-2 diabetic nephropathy patients. J Nat Sci Biol Med. 2013; 4: 336–40.
19. Liang T, Zhang Q, Sun W, et al. Zinc treatment prevents type 1 diabetes-induced hepatic oxidative damage, endoplasmic reticulum stress, and cell death, and even prevents possible steatohepatitis in the OVE26 mouse model: important role of metallothionein. Toxicol Lett. 2015; 233: 114–24.
20. Li B, Cui W, Tan Y, et al. Zinc is essential for the transcription function of Nrf2 in human renal tubule cells in vitro and mouse kidney in vivo under the diabetic condition. J Cell Mol Med. 2014; 18: 895–906.
21. Wu H, Kong L, Cheng Y, et al. Metallothionein plays a prominent role in the prevention of diabetic nephropathy by sulforaphane via up-regulation of Nrf2. Free Radic Biol Med. 2015; 89: 431–42.
22. Wang YH, Cai L. Diabetes/obesity-related inflammation, cardiac cell death and cardiomyopathy. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2006; 31: 814–8.
23. Sun W, Miao X, Zhou S, et al. Zinc rescue of Akt2 gene deletion-linked murine cardiac dysfunction and pathological changes is metallothionein-dependent. J Mol Cell Cardiol. 2014; 74: 88–97.
24. Mechan AO, Wyss A, Rieger H, et al. A comparison of learning and memory characteristics of young and middle-aged wild-type mice in the IntelliCage. J Neurosci Methods. 2009; 180: 43–51.
25. Zhang Z, Wang S, Zhou S, et al. Sulforaphane prevents the development of cardiomyopathy in type 2 diabetic mice probably by reversing oxidative stress-induced inhibition of LKB1/AMPK pathway. J Mol Cell Cardiol. 2014; 77: 42–52.
26. Zuo L, Du Y, Lu M, et al. Atorvastatin inhibits hyperglycemia-induced expression of osteopontin in the diabetic rat kidney via the p38 MAPK pathway. Mol Biol Rep. 2014; 41: 2551–8.
27. Wang Y, Zhang Z, Sun W, et al. Sulforaphane attenuation of type 2 diabetes-induced aortic damage was associated with the upregulation of Nrf2 expression and function. Oxid Med Cell Longev. 2014; 2014: 123963.
28. Bai Y, Cui WP, Xin Y, et al. Prevention by sulforaphane of diabetic cardiomyopathy is associated with up-regulation of Nrf2 expression and transcription activation. J Mol Cell Cardiol. 2013; 57: 82–95.
29. Zhang C, Huang Z, Gu J, et al. Fibroblast growth factor 21 protects the heart from apoptosis in a diabetic mouse model via extracellular signal-regulated kinase 1/2-dependent signalling pathway. Diabetologia. 2015; 58: 1937–48.
30. Huang W, Bansode RR, Bal NC, et al. Protein kinase Cbeta deficiency attenuates obesity syndrome of ob/ob mice by promoting white adipose tissue remodeling. J Lipid Res. 2012; 53: 368–78.
31. Cao L, Qin X, Peterson MR, et al. CARD9 knockout ameliorates myocardial dysfunction associated with high fat diet-induced obesity. J Mol Cell Cardiol. 2016; 92: 185–95.
32. Zhao Y, Tan Y, Dai J, et al. Exacerbation of diabetes-induced testicular apoptosis by zinc deficiency is most likely associated with oxidative stress, p38 MAPK activation, and p53 activation in mice. Toxicol Lett. 2011; 200: 100–6.
33. Zago MP, Mackenzie GG, Adamo AM, et al. Differential modulation of MAP kinases by zinc deficiency in IMR-32 cells: role of H(2)O(2). Antioxid Redox Signal. 2005; 7: 1773–82.
34. Wessels I, Haase H, Engelhardt G, et al. Zinc deficiency induces production of the proinflammatory cytokines IL-1beta and TNFalpha in promyeloid cells via epigenetic and redox-dependent mechanisms. J Nutr Biochem. 2013; 24: 289–97.
35. Ruland J. CARD9 signaling in the innate immune response. Ann N Y Acad Sci. 2008; 1143: 35–44.
36. Marko L, Henke N, Park JK, et al. Bcl10 mediates angiotensin II-induced cardiac damage and electrical remodeling. Hypertension. 2014; 64: 1032–9.
37. Liu Y, Wang Y, Shi H, et al. CARD9 mediates necrotic smooth muscle cell-induced inflammation in macrophages contributing to neointima formation of vein grafts. Cardiovasc Res. 2015; 108: 148–58.
38. Han J, Ulevitch RJ. Limiting inflammatory responses during activation of innate immunity. Nat Immunol. 2005; 6: 1198–205.
39. Dong C, Davis RJ, Flavell RA. MAP kinases in the immune response. Annu Rev Immunol. 2002; 20: 55–72.
40. Hara H, Ishihara C, Takeuchi A, et al. The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-associated and Toll-like receptors. Nat Immunol. 2007; 8: 619–29.
41. Gross O, Gewies A, Finger K, et al. Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature. 2006; 442: 651–6.
42. Ren J, Yang M, Qi G, et al. Proinflammatory protein CARD9 is essential for infiltration of monocytic fibroblast precursors and cardiac fibrosis caused by Angiotensin II infusion. Am J Hypertens. 2011; 24: 701–7.
43. Kang YJ, Zhou ZX, Wang GW, et al. Suppression by metallothionein of doxorubicin-induced cardiomyocyte apoptosis through inhibition of p38 mitogen-activated protein kinases. J Biol Chem. 2000; 275: 13690–8.
44. Miao X, Wang Y, Sun J, et al. Zinc protects against diabetes-induced pathogenic changes in the aorta: roles of metallothionein and nuclear factor (erythroid-derived 2)-like 2. Cardiovasc Diabetol. 2013; 12: 54.
45. Pahwa R, Nallasamy P, Jialal I. Toll-like receptors 2 and 4 mediate hyperglycemia induced macrovascular aortic endothelial cell inflammation and perturbation of the endothelial glycocalyx. J Diabetes Complications. 2016; 30: 563–72.
46. Liu Y, Dong W, Chen L, et al. BCL10 mediates lipopolysaccharide/toll-like receptor-4 signaling through interaction with Pellino2. J Biol Chem. 2004; 279: 37436–44.
47. Bhattacharyya S, Gill R, Chen ML, et al. Toll-like receptor 4 mediates induction of the Bcl10-NFkappaB-interleukin-8 inflammatory pathway by carrageenan in human intestinal epithelial cells. J Biol Chem. 2008; 283: 10550–8.
48. Bradfield CJ, Kim BH, MacMicking JD. Crossing the Rubicon: new roads lead to host defense. Cell Host Microbe. 2012; 11: 221–3.
49. Zhang Y, Bao M, Dai M, et al. Cardiospecific CD36 suppression by lentivirus-mediated RNA interference prevents cardiac hypertrophy and systolic dysfunction in high-fat-diet induced obese mice. Cardiovasc Diabetol. 2015; 14: 69.
50. Xie Q, Wei T, Huang C, et al. Nebivolol ameliorates cardiac NLRP3 inflammasome activation in a Juvenile-adolescent animal model of diet-induced obesity. Sci Rep. 2016; 6: 34326.