RhNRG-1β protects the myocardium against irradiation-induced damage via the ErbB2-ERK-SIRT1 signaling pathway

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Gu, Anxin ^a   Jie, Yamin ^a   Sun, Liang ^a   Zhao, Shuping ^a   Mingyan, E ^a   You, Qingshan ^a  

^a HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C OXIDASE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; NEU DIFFERENTIATION FACTOR; RHNRG 1BETA; SIRTUIN 1; UNCLASSIFIED DRUG; CARDIOTONIC AGENT; ERBB2 PROTEIN, RAT; NEUREGULIN BETA; RADIOPROTECTIVE AGENT; RECOMBINANT PROTEIN; SIRT1 PROTEIN, RAT;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENERGY METABOLISM; FIBROSING ALVEOLITIS; HEART ASSIST DEVICE; HEART DISEASE; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART VENTRICLE REMODELING; IRRADIATION INDUCED HEART DISEASE; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; RAT; RESPIRATORY CHAIN; WESTERN BLOTTING; ANIMAL; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL CULTURE; DRUG EFFECTS; HEART; HEART DISEASES; HUMAN; METABOLISM; MITOCHONDRION; PATHOLOGY; RADIATION RESPONSE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CARDIOTONIC AGENTS; CELLS, CULTURED; HEART; HEART DISEASES; HUMANS; MALE; MAP KINASE SIGNALING SYSTEM; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, CARDIAC; NEUREGULIN-1; RADIATION-PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, ERBB-2; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; SIRTUIN 1;

EID: 84947475252     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137337     Document Type: Article

References (51)

1. Darby SC, Cutter DJ, Boerma M, Constine LS, Fajardo LF, Kodama K, et al. Radiation-related heart disease: current knowledge and future prospects. International journal of radiation oncology, biology, physics. 2010; 76(3):656-65. doi: 10.1016/j.ijrobp.2009.09.064 PMID: 20159360; PubMed Central PMCID: PMC3910096.
2. Sardaro A, Petruzzelli MF, D'Errico MP, Grimaldi L, Pili G, Portaluri M. Radiation-induced cardiac damage in early left breast cancer patients: risk factors, biological mechanisms, radiobiology, and dosimetric constraints. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 2012; 103(2):133-42. doi: 10.1016/j.radonc.2012.02.008 PMID: 22391054.
3. Corn BW, Trock BJ, Goodman RL. Irradiation-related ischemic heart disease. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 1990; 8(4):741-50. PMID: 2179483.
4. Tian Y, Morrisey EE. Importance of myocyte-nonmyocyte interactions in cardiac development and disease. Circulation research. 2012; 110(7):1023-34. doi: 10.1161/CIRCRESAHA.111.243899 PMID: 22461366; PubMed Central PMCID: PMC3366271.
5. Lemmens K, Segers VF, Demolder M, De Keulenaer GW. Role of neuregulin-1/ErbB2 signaling in endothelium-cardiomyocyte cross-talk. The Journal of biological chemistry. 2006; 281(28):19469-77. doi: 10.1074/jbc.M600399200 PMID: 16698793.
6. Lai D, Liu X, Forrai A, Wolstein O, Michalicek J, Ahmed I, et al. Neuregulin 1 sustains the gene regulatory network in both trabecular and nontrabecular myocardium. Circulation research. 2010; 107 (6):715-27. doi: 10.1161/CIRCRESAHA.110.218693 PMID: 20651287.
7. Bersell K, Arab S, Haring B, Kuhn B. Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell. 2009; 138(2):257-70. doi: 10.1016/j.cell.2009.04.060 PMID: 19632177.
8. Citri A, Yarden Y. EGF-ERBB signalling: towards the systems level. Nature reviews Molecular cell biology. 2006; 7(7):505-16. doi: 10.1038/nrm1962 PMID: 16829981.
9. D'Uva G, Aharonov A, Lauriola M, Kain D, Yahalom-Ronen Y, Carvalho S, et al. ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation. Nature cell biology. 2015. doi: 10.1038/ncb3149 PMID: 25848746.
10. Chan JY, Takeda M, Briggs LE, Graham ML, Lu JT, Horikoshi N, et al. Identification of cardiac-specific myosin light chain kinase. Circulation research. 2008; 102(5):571-80. doi: 10.1161/CIRCRESAHA. 107.161687 PMID: 18202317; PubMed Central PMCID: PMC2504503.
11. Okoshi K, Nakayama M, Yan X, Okoshi MP, Schuldt AJ, Marchionni MA, et al. Neuregulins regulate cardiac parasympathetic activity: muscarinic modulation of beta-adrenergic activity in myocytes from mice with neuregulin-1 gene deletion. Circulation. 2004; 110(6):713-7. doi: 10.1161/01.CIR. 0000138109.32748.80 PMID: 15289373.
12. Liu X, Gu X, Li Z, Li X, Li H, Chang J, et al. Neuregulin-1/erbB-activation improves cardiac function and survival in models of ischemic, dilated, and viral cardiomyopathy. Journal of the American College of Cardiology. 2006; 48(7):1438-47. doi: 10.1016/j.jacc.2006.05.057 PMID: 17010808.
13. An T, Zhang Y, Huang Y, Zhang R, Yin S, Guo X, et al. Neuregulin-1 protects against doxorubicininduced apoptosis in cardiomyocytes through an Akt-dependent pathway. Physiological research / Academia Scientiarum Bohemoslovaca. 2013; 62(4):379-85. PMID: 23590603.
14. Polizzotti BD, Ganapathy B, Walsh S, Choudhury S, Ammanamanchi N, Bennett DG, et al. Neuregulin stimulation of cardiomyocyte regeneration in mice and human myocardium reveals a therapeutic window. Science translational medicine. 2015; 7(281):281ra45. doi: 10.1126/scitranslmed.aaa5171 PMID: 25834111.
15. Gao R, Zhang J, Cheng L, Wu X, Dong W, Yang X, et al. A Phase II, randomized, double-blind, multicenter, based on standard therapy, placebo-controlled study of the efficacy and safety of recombinant human neuregulin-1 in patients with chronic heart failure. Journal of the American College of Cardiology. 2010; 55(18):1907-14. doi: 10.1016/j.jacc.2009.12.044 PMID: 20430261.
16. Sridharan V, Tripathi P, Sharma S, Corry PM, Moros EG, Singh A, et al. Effects of late administration of pentoxifylline and tocotrienols in an image-guided rat model of localized heart irradiation. PloS one. 2013; 8(7):e68762. doi: 10.1371/journal.pone.0068762 PMID: 23894340; PubMed Central PMCID: PMC3718790.
17. Tony H, Yu K, Qiutang Z. MicroRNA-208a Silencing Attenuates Doxorubicin Induced Myocyte Apoptosis and Cardiac Dysfunction. Oxidative medicine and cellular longevity. 2015; 2015:597032. doi: 10. 1155/2015/597032 PMID: 26137188; PubMed Central PMCID: PMC4475537.
18. Wang JX, Zhang XJ, Feng C, Sun T, Wang K, Wang Y, et al. MicroRNA-532-3p regulates mitochondrial fission through targeting apoptosis repressor with caspase recruitment domain in doxorubicin cardiotoxicity. Cell death & disease. 2015; 6:e1677. doi: 10.1038/cddis.2015.41 PMID: 25766316; PubMed Central PMCID: PMC4385919.
19. Srinivasan S, Spear J, Chandran K, Joseph J, Kalyanaraman B, Avadhani NG. Oxidative stress induced mitochondrial protein kinase A mediates cytochrome c oxidase dysfunction. PloS one. 2013; 8 (10):e77129. doi: 10.1371/journal.pone.0077129 PMID: 24130844; PubMed Central PMCID: PMC3795003.
20. Zhang M, Wei J, Shan H, Wang H, Zhu Y, Xue J, et al. Calreticulin-STAT3 signaling pathway modulates mitochondrial function in a rat model of furazolidone-induced dilated cardiomyopathy. PloS one. 2013; 8(6):e66779. doi: 10.1371/journal.pone.0066779 PMID: 23818963; PubMed Central PMCID: PMC3688564.
21. Sun L, Liu S, Sun Q, Li Z, Xu F, Hou C, et al. Inhibition of TROY promotes OPC differentiation and increases therapeutic efficacy of OPC graft for spinal cord injury. Stem cells and development. 2014; 23(17):2104-18. doi: 10.1089/scd.2013.0563 PMID: 24749558; PubMed Central PMCID: PMC4142779.
22. Akman-Anderson L, Olivier M, Luckhart S. Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infection and immunity. 2007; 75 (8):4012-9. doi: 10.1128/IAI.00645-07 PMID: 17526741; PubMed Central PMCID: PMC1952000.
23. Hill MF, Patel AV, Murphy A, Smith HM, Galindo CL, Pentassuglia L, et al. Intravenous glial growth factor 2 (GGF2) isoform of neuregulin-1beta improves left ventricular function, gene and protein expression in rats after myocardial infarction. PloS one. 2013; 8(2):e55741. doi: 10.1371/journal.pone. 0055741 PMID: 23437060; PubMed Central PMCID: PMC3578842.
24. Liu S, Li Z, Fu J, Sun L, Xu F, Harada T, et al. The effects of harvesting media on biological characteristics and repair potential of neural stem cells after traumatic brain injury. PloS one. 2014; 9(9):e107865. doi: 10.1371/journal.pone.0107865 PMID: 25247595; PubMed Central PMCID: PMC4172630.
25. Rizk SM, El-Maraghy SA, Nassar NN. A novel role for SIRT-1 in L-arginine protection against STZ induced myocardial fibrosis in rats. PloS one. 2014; 9(12):e114560. doi: 10.1371/journal.pone. 0114560 PMID: 25501750; PubMed Central PMCID: PMC4264750.
26. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, et al. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science. 2007; 316(5828):1198-202. doi: 10.1126/science. 1139516 PMID: 17525341; PubMed Central PMCID: PMC2706583.
27. Shukla PC, Singh KK, Quan A, Al-Omran M, Teoh H, Lovren F, et al. BRCA1 is an essential regulator of heart function and survival following myocardial infarction. Nature communications. 2011; 2:593. doi: 10.1038/ncomms1601 PMID: 22186889; PubMed Central PMCID: PMC3247816.
28. Baban B, Liu JY, Qin X, Weintraub NL, Mozaffari MS. Upregulation of Programmed Death-1 and Its Ligand in Cardiac Injury Models: Interaction with GADD153. PloS one. 2015; 10(4):e0124059. doi: 10. 1371/journal.pone.0124059 PMID: 25902191; PubMed Central PMCID: PMC4406739.
29. Sridharan V, Aykin-Burns N, Tripathi P, Krager KJ, Sharma SK, Moros EG, et al. Radiation-induced alterations in mitochondria of the rat heart. Radiation research. 2014; 181(3):324-34. doi: 10.1667/ RR13452.1 PMID: 24568130; PubMed Central PMCID: PMC4029615.
30. Schwarz K, Siddiqi N, Singh S, Neil CJ, Dawson DK, Frenneaux MP. The breathing heart-mitochondrial respiratory chain dysfunction in cardiac disease. International journal of cardiology. 2014; 171 (2):134-43. doi: 10.1016/j.ijcard.2013.12.014 PMID: 24377708.
31. Ong SB, Hall AR, Hausenloy DJ. Mitochondrial dynamics in cardiovascular health and disease. Antioxidants & redox signaling. 2013; 19(4):400-14. doi: 10.1089/ars.2012.4777 PMID: 22793879; PubMed Central PMCID: PMC3699895.
32. Yu H, Tigchelaar W, Koonen DP, Patel HH, de Boer RA, van Gilst WH, et al. AKIP1 expression modulates mitochondrial function in rat neonatal cardiomyocytes. PloS one. 2013; 8(11):e80815. doi: 10. 1371/journal.pone.0080815 PMID: 24236204; PubMed Central PMCID: PMC3827472.
33. Bassino E, Fornero S, Gallo MP, Gallina C, Femmino S, Levi R, et al. Catestatin exerts direct protective effects on rat cardiomyocytes undergoing ischemia/reperfusion by stimulating PI3K-Akt-GSK3beta pathway and preserving mitochondrial membrane potential. PloS one. 2015; 10(3):e0119790. doi: 10. 1371/journal.pone.0119790 PMID: 25774921; PubMed Central PMCID: PMC4361546.
34. Kim YC, Wikstrom M, Hummer G. Kinetic gating of the proton pump in cytochrome c oxidase. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106(33):13707-12. doi: 10.1073/pnas.0903938106 PMID: 19666617; PubMed Central PMCID: PMC2728958.
35. Cervera AM, Bayley JP, Devilee P, McCreath KJ. Inhibition of succinate dehydrogenase dysregulates histone modification in mammalian cells. Molecular cancer. 2009; 8:89. doi: 10.1186/1476-4598-8-89 PMID: 19849834; PubMed Central PMCID: PMC2770992.
36. Nogueiras R, Habegger KM, Chaudhary N, Finan B, Banks AS, Dietrich MO, et al. Sirtuin 1 and sirtuin 3: physiological modulators of metabolism. Physiological reviews. 2012; 92(3):1479-514. doi: 10.1152/ physrev.00022.2011 PMID: 22811431; PubMed Central PMCID: PMC3746174.
37. Polidoro L, Properzi G, Marampon F, Gravina GL, Festuccia C, Di Cesare E, et al. Vitamin D protects human endothelial cells from H(2)O(2) oxidant injury through the Mek/Erk-Sirt1 axis activation. Journal of cardiovascular translational research. 2013; 6(2):221-31. doi: 10.1007/s12265-012-9436-x PMID: 23247634.
38. Wadugu B, Kuhn B. The role of neuregulin/ErbB2/ErbB4 signaling in the heart with special focus on effects on cardiomyocyte proliferation. American journal of physiology Heart and circulatory physiology. 2012; 302(11):H2139-47. doi: 10.1152/ajpheart.00063.2012 PMID: 22427524; PubMed Central PMCID: PMC3378290.
39. Puente BN, Kimura W, Muralidhar SA, Moon J, Amatruda JF, Phelps KL, et al. The oxygen-rich postnatal environment induces cardiomyocyte cell-cycle arrest through DNA damage response. Cell. 2014; 157(3):565-79. doi: 10.1016/j.cell.2014.03.032 PMID: 24766806; PubMed Central PMCID: PMC4104514.
40. Barjaktarovic Z, Shyla A, Azimzadeh O, Schulz S, Haagen J, Dorr W, et al. Ionising radiation induces persistent alterations in the cardiac mitochondrial function of C57BL/6 mice 40 weeks after local heart exposure. Radiotherapy and oncology: journal of the European Society for Therapeutic Radiology and Oncology. 2013; 106(3):404-10. doi: 10.1016/j.radonc.2013.01.017 PMID: 23522698.
41. Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Molecular biology of the cell. 2005; 16(10):4623-35. doi: 10.1091/mbc.E05-01-0033 PMID: 16079181; PubMed Central PMCID: PMC1237069.
42. Tanno M, Sakamoto J, Miura T, Shimamoto K, Horio Y. Nucleocytoplasmic shuttling of the NAD +-dependent histone deacetylase SIRT1. The Journal of biological chemistry. 2007; 282(9):6823-32. doi: 10.1074/jbc.M609554200 PMID: 17197703.
43. Planavila A, Dominguez E, Navarro M, Vinciguerra M, Iglesias R, Giralt M, et al. Dilated cardiomyopathy and mitochondrial dysfunction in Sirt1-deficient mice: a role for Sirt1-Mef2 in adult heart. Journal of molecular and cellular cardiology. 2012; 53(4):521-31. doi: 10.1016/j.yjmcc.2012.07.019 PMID: 22986367.
44. Li J, Feng L, Xing Y, Wang Y, Du L, Xu C, et al. Radioprotective and antioxidant effect of resveratrol in hippocampus by activating Sirt1. International journal of molecular sciences. 2014; 15(4):5928-39. doi: 10.3390/ijms15045928 PMID: 24722566; PubMed Central PMCID: PMC4013605.
45. Yamagata K, Kitabayashi I. Sirt1 physically interacts with Tip60 and negatively regulates Tip60-mediated acetylation of H2AX. Biochemical and biophysical research communications. 2009; 390(4):1355-60. doi: 10.1016/j.bbrc.2009.10.156 PMID: 19895790.
46. Erven K, Florian A, Slagmolen P, Sweldens C, Jurcut R, Wildiers H, et al. Subclinical cardiotoxicity detected by strain rate imaging up to 14 months after breast radiation therapy. International journal of radiation oncology, biology, physics. 2013; 85(5):1172-8. doi: 10.1016/j.ijrobp.2012.09.022 PMID: 23149005.
47. Chua YL, Ito Y, Pole JC, Newman S, Chin SF, Stein RC, et al. The NRG1 gene is frequently silenced by methylation in breast cancers and is a strong candidate for the 8p tumour suppressor gene. Oncogene. 2009; 28(46):4041-52. doi: 10.1038/onc.2009.259 PMID: 19802002; PubMed Central PMCID: PMC2789334.
48. Tsai MS, Shamon-Taylor LA, Mehmi I, Tang CK, Lupu R. Blockage of heregulin expression inhibits tumorigenicity and metastasis of breast cancer. Oncogene. 2003; 22(5):761-8. doi: 10.1038/sj.onc. 1206130 PMID: 12569369.
49. Zhao YY, Sawyer DR, Baliga RR, Opel DJ, Han X, Marchionni MA, et al. Neuregulins promote survival and growth of cardiac myocytes. Persistence of ErbB2 and ErbB4 expression in neonatal and adult ventricular myocytes. The Journal of biological chemistry. 1998; 273(17):10261-9. PMID: 9553078.
50. Ghobadi G, van der Veen S, Bartelds B, de Boer RA, Dickinson MG, de Jong JR, et al. Physiological interaction of heart and lung in thoracic irradiation. International journal of radiation oncology, biology, physics. 2012; 84(5):e639-46. doi: 10.1016/j.ijrobp.2012.07.2362 PMID: 22975617.
51. Lenarczyk M, Lam V, Jensen E, Fish BL, Su J, Koprowski S, et al. Cardiac injury after 10 gy total body irradiation: indirect role of effects on abdominal organs. Radiation research. 2013; 180(3):247-58. doi: 10.1667/RR3292.1 PMID: 23919311; PubMed Central PMCID: PMC4042860.