Adiponectin protects the rats liver against chronic intermittent hypoxia induced injury through AMP-activated protein kinase pathway

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ding, Wenxiao ^a   Zhang, Qiang ^a   Dong, Yanbin ^a   Ding, Ning ^a   Huang, Hanpeng ^a   Zhu, Xianji ^a   Hutchinson, Sean ^b   Gao, Xingya ^c   Zhang, Xilong ^a  

^a THE FIRST AFFILIATED HOSPITAL OF NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84989856182     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep34151     Document Type: Article

References (65)

1. Garg, R. et al. A comparative study on the clinical and polysomnographic pattern of obstructive sleep apnea among obese and nonobese subjects. Annals of thoracic medicine 7, 26-30, doi: 10.4103/1817-1737.91561 (2012).
2. Kim, S. M., Cho, K. I., Kwon, J. H., Lee, H. G. & Kim, T. I. Impact of obstructive sleep apnea on left atrial functional and structural remodeling beyond obesity. J Cardiol 60, 475-483, doi: 10.1016/j.jjcc.2012.07.007 (2012).
3. Kasai, T. & Bradley, T. D. Obstructive sleep apnea and heart failure: pathophysiologic and therapeutic implications. J Am Coll Cardiol 57, 119-127, doi: 10.1016/j.jacc.2010.08.627 (2011).
4. Coughlin, S. R., Mawdsley, L., Mugarza, J. A., Calverley, P. M. & Wilding, J. P. Obstructive sleep apnoea is independently associated with an increased prevalence of metabolic syndrome. Eur Heart J 25, 735-741, doi: 10.1016/j.ehj.2004.02.021 (2004).
5. Drager, L. F. et al. Intermittent hypoxia inhibits clearance of triglyceride-rich lipoproteins and inactivates adipose lipoprotein lipase in a mouse model of sleep apnoea. Eur Heart J 33, 783-790, doi: 10.1093/eurheartj/ehr097 (2012).
6. West, S. D. et al. The prevalence of retinopathy in men with Type 2 diabetes and obstructive sleep apnoea. Diabetic medicine: a journal of the British Diabetic Association 27, 423-430, doi: 10.1111/j.1464-5491.2010.02962.x (2010).
7. Robinson, G. V., Pepperell, J. C., Segal, H. C., Davies, R. J. & Stradling, J. R. Circulating cardiovascular risk factors in obstructive sleep apnoea: data from randomised controlled trials. Thorax 59, 777-782, doi: 10.1136/thx.2003.018739 (2004).
8. Musso, G. et al. Association of obstructive sleep apnoea with the presence and severity of non-alcoholic fatty liver disease. A systematic review and meta-analysis. Obesity reviews: an official journal of the International Association for the Study of Obesity 14, 417-431, doi: 10.1111/obr.12020 (2013).
9. Nobili, V. et al. Obstructive sleep apnea syndrome affects liver histology and inflammatory cell activation in pediatric nonalcoholic fatty liver disease, regardless of obesity/insulin resistance. Am J Respir Crit Care Med 189, 66-76, doi: 10.1164/rccm.201307-1339OC (2014).
10. Hernandez-Guerra, M. et al. Chronic intermittent hypoxia aggravates intrahepatic endothelial dysfunction in cirrhotic rats. Hepatology 57, 1564-1574, doi: 10.1002/hep.26152 (2013).
11. Savransky, V. et al. Chronic intermittent hypoxia predisposes to liver injury. Hepatology 45, 1007-1013, doi: 10.1002/hep.21593 (2007).
12. Kim, M. K., Kim, H. S., Lee, I. K. & Park, K. G. Endoplasmic reticulum stress and insulin biosynthesis: a review. Experimental diabetes research 2012, 509437, doi: 10.1155/2012/509437 (2012).
13. Grimm, S. The ER-mitochondria interface: the social network of cell death. Biochim Biophys Acta 1823, 327-334, doi: 10.1016/j. bbamcr.2011.11.018 (2012).
14. Chiang, C. K., Nangaku, M., Tanaka, T., Iwawaki, T. & Inagi, R. Endoplasmic reticulum stress signal impairs erythropoietin production: a role for ATF4. Am J Physiol Cell Physiol 304, C342-C353, doi: 10.1152/ajpcell.00153.2012 (2013).
15. Xu, C., Bailly-Maitre, B. & Reed, J. C. Endoplasmic reticulum stress: cell life and death decisions. The Journal of clinical investigation 115, 2656-2664, doi: 10.1172/JCI26373 (2005).
16. Puri, P. et al. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 134, 568-576, doi: 10.1053/j.gastro.2007.10.039 (2008).
17. Mosbah, I. B. et al. IGL-1 solution reduces endoplasmic reticulum stress and apoptosis in rat liver transplantation. Cell Death Dis 3, e279, doi: 10.1038/cddis.2012.12 (2012).
18. Ding, W. et al. Adiponectin protects rat myocardium against chronic intermittent hypoxia-induced injury via inhibition of endoplasmic reticulum stress. PLoS One 9, e94545, doi: 10.1371/journal.pone.0094545 (2014).
19. Zhang, X. F. et al. Adiponectin protects the genioglossus of rats against chronic intermittent hypoxia-induced injury via inhibition of endoplasmic reticulum stress. Chin Med J (Engl) 126, 3270-3275 (2013).
20. Kadowaki, T. & Yamauchi, T. Adiponectin and adiponectin receptors. Endocrine reviews 26, 439-451, doi: 10.1210/er.2005-0005 (2005).
21. Yamauchi, T. et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nature medicine 8, 1288-1295, doi: 10.1038/nm788 (2002).
22. Gao, Y. et al. Silencing of ADIPOQ efficiently suppresses preadipocyte differentiation in porcine. Cell Physiol Biochem 31, 452-461, doi: 10.1159/000343381 (2013).
23. Baldasseroni, S. et al. Adiponectin, diabetes and ischemic heart failure: a challenging relationship. Cardiovasc Diabetol 11, 151, doi: 10.1186/1475-2840-11-151 (2012).
24. Wang, Y. et al. Cardiomyocyte-derived adiponectin is biologically active in protecting against myocardial ischemia-reperfusion injury. Am J Physiol Endocrinol Metab 298, E663-E670, doi: 10.1152/ajpendo.00663.2009 (2010).
25. OShea, K. M. et al. Effects of adiponectin deficiency on structural and metabolic remodeling in mice subjected to pressure overload. Am J Physiol Heart Circ Physiol 298, H1639-H1645, doi: 10.1152/ajpheart.00957.2009 (2010).
26. Huang, H. et al. Adiponectin alleviates genioglossal mitochondrial dysfunction in rats exposed to intermittent hypoxia. PLoS One 9, e109284, doi: 10.1371/journal.pone.0109284 (2014).
27. Norman, D. et al. Serum aminotransferase levels are associated with markers of hypoxia in patients with obstructive sleep apnea. Sleep 31, 121-126 (2008).
28. Singh, H. et al. Symptoms of obstructive sleep apnea in patients with nonalcoholic fatty liver disease. Dig Dis Sci 50, 2338-2343, doi: 10.1007/s10620-005-3058-y (2005).
29. Tanne, F. et al. Chronic liver injury during obstructive sleep apnea. Hepatology 41, 1290-1296, doi: 10.1002/hep.20725 (2005).
30. Chin, K. et al. Effects of obstructive sleep apnea syndrome on serum aminotransferase levels in obese patients. The American journal of medicine 114, 370-376 (2003).
31. Brenner, C. & Kroemer, G. Apoptosis. Mitochondria-the death signal integrators. Science 289, 1150-1151 (2000).
32. Bredesen, D. E. Apoptosis: overview and signal transduction pathways. J Neurotrauma 17, 801-810 (2000).
33. Li, H. J. et al. FasL-induced apoptosis in bovine oocytes via the Bax signal. Theriogenology 80, 248-255, doi: 10.1016/j. theriogenology.2013.04.002 (2013).
34. Pecina-Slaus, N. Wnt signal transduction pathway and apoptosis: a review. Cancer cell international 10, 22, doi: 10.1186/1475-2867- 10-22 (2010).
35. Tabas, I. & Ron, D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nature cell biology 13, 184-190, doi: 10.1038/ncb0311-184 (2011).
36. Ron, D. & Walter, P. Signal integration in the endoplasmic reticulum unfolded protein response. Nature reviews. Molecular cell biology 8, 519-529, doi: 10.1038/nrm2199 (2007).
37. Friedman, A. D. GADD153/CHOP, a DNA damage-inducible protein, reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res 56, 3250-3256 (1996).
38. Eymin, B., Dubrez, L., Allouche, M. & Solary, E. Increased gadd153 messenger RNA level is associated with apoptosis in human leukemic cells treated with etoposide. Cancer Res 57, 686-695 (1997).
39. Marciniak, S. J. et al. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes & development 18, 3066-3077, doi: 10.1101/gad.1250704 (2004).
40. Nguyen, M., Breckenridge, D. G., Ducret, A. & Shore, G. C. Caspase-resistant BAP31 inhibits fas-mediated apoptotic membrane fragmentation and release of cytochrome c from mitochondria. Molecular and cellular biology 20, 6731-6740 (2000).
41. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T. & Yasuhiko, Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. The Journal of biological chemistry 277, 34287-34294, doi: 10.1074/jbc.M204973200 (2002).
42. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y. & Holbrook, N. J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Molecular and cellular biology 21, 1249-1259, doi: 10.1128/ MCB.21.4.1249-1259.2001 (2001).
43. Shore, G. C., Papa, F. R. & Oakes, S. A. Signaling cell death from the endoplasmic reticulum stress response. Current opinion in cell biology 23, 143-149, doi: 10.1016/j.ceb.2010.11.003 (2011).
44. Danial, N. N. & Korsmeyer, S. J. Cell death: critical control points. Cell 116, 205-219 (2004).
45. Yaoita, H., Ogawa, K., Maehara, K. & Maruyama, Y. Apoptosis in relevant clinical situations: contribution of apoptosis in myocardial infarction. Cardiovasc Res 45, 630-641, doi: S0008-6363(99)00349-1 (2000).
46. Hochhauser, E. et al. Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol Heart Circ Physiol 284, H2351-H2359, doi: 10.1152/ajpheart.00783.2002284/6/H2351 (2003).
47. Lopez-Hernandez, F. J., Ortiz, M. A. & Piedrafita, F. J. The extrinsic and intrinsic apoptotic pathways are differentially affected by temperature upstream of mitochondrial damage. Apoptosis: an international journal on programmed cell death 11, 1339-1347, doi: 10.1007/s10495-006-7689-z (2006).
48. Shi, Y. Caspase activation: revisiting the induced proximity model. Cell 117, 855-858, doi: 10.1016/j.cell.2004.06.007 (2004).
49. Circu, M. L. & Aw, T. Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48, 749-762, doi: 10.1016/j.freeradbiomed.2009.12.022 (2010).
50. Liu, Z. W. et al. Protein kinase RNA-like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)-mediated endoplasmic reticulum stress-induced apoptosis in diabetic cardiomyopathy. Cardiovasc Diabetol 12, 158, doi: 10.1186/1475-2840-12-158 (2013).
51. Liu, Z. W. et al. Protein kinase RNA- like endoplasmic reticulum kinase (PERK) signaling pathway plays a major role in reactive oxygen species (ROS)- mediated endoplasmic reticulum stress- induced apoptosis in diabetic cardiomyopathy. Cardiovasc Diabetol 12, 158, doi: 10.1186/1475-2840-12-158 (2013).
52. Wang, Y., Zhang, S. X. & Gozal, D. Reactive oxygen species and the brain in sleep apnea. Respiratory physiology & neurobiology 174, 307-316, doi: 10.1016/j.resp.2010.09.001 (2010).
53. Ma, H. et al. Effects of a low-fat diet on the hepatic expression of adiponectin and its receptors in rats with NAFLD. Annals of hepatology 14, 108-117 (2015).
54. Goldstein, B. J., Scalia, R. G. & Ma, X. L. Protective vascular and myocardial effects of adiponectin. Nat Clin Pract Cardiovasc Med 6, 27-35, doi: 10.1038/ncpcardio1398 (2009).
55. Magalang, U. J. et al. Adiponectin inhibits superoxide generation by human neutrophils. Antioxid Redox Signal 8, 2179-2186, doi: 10.1089/ars.2006.8.2179 (2006).
56. Hardie, D. G., Ross, F. A. & Hawley, S. A. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nature reviews. Molecular cell biology 13, 251-262, doi: 10.1038/nrm3311 (2012).
57. Mihaylova, M. M. & Shaw, R. J. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nature cell biology 13, 1016-1023, doi: 10.1038/ncb2329 (2011).
58. Zheng, Z. et al. Sirtuin 1-mediated cellular metabolic memory of high glucose via the LKB1/AMPK/ROS pathway and therapeutic effects of metformin. Diabetes 61, 217-228, doi: 10.2337/db11-0416 (2012).
59. Li, X. N. et al. Activation of the AMPK-FOXO3 pathway reduces fatty acid-induced increase in intracellular reactive oxygen species by upregulating thioredoxin. Diabetes 58, 2246-2257, doi: 10.2337/db08-1512 (2009).
60. Colombo, S. L. & Moncada, S. AMPKalpha1 regulates the antioxidant status of vascular endothelial cells. Biochem J 421, 163-169, doi: 10.1042/BJ20090613 (2009).
61. Ix, J. H. & Sharma, K. Mechanisms linking obesity, chronic kidney disease, and fatty liver disease: the roles of fetuin-A, adiponectin, and AMPK. J Am Soc Nephrol 21, 406-412, doi: 10.1681/ASN.2009080820 (2010).
62. Shimano, M. et al. Adiponectin deficiency exacerbates cardiac dysfunction following pressure overload through disruption of an AMPK-dependent angiogenic response. J Mol Cell Cardiol 49, 210-220, doi: 10.1016/j.yjmcc.2010.02.021 (2010).
63. Winder, W. W. & Hardie, D. G. AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. The American journal of physiology 277, E1-10 (1999).
64. Jenkins, Y. et al. AMPK activation through mitochondrial regulation results in increased substrate oxidation and improved metabolic parameters in models of diabetes. PLoS One 8, e81870, doi: 10.1371/journal.pone.0081870 (2013).
65. Folch, J., Lees, M. & Sloane Stanley, G. H. A simple method for the isolation and purification of total lipides from animal tissues. The Journal of biological chemistry 226, 497-509 (1957).