Neuregulin‑1: An underlying protective force of cardiac dysfunction in sepsis (Review)
- Authors:
- Wen Kang
- Yue Cheng
- Xi Wang
- Fang Zhou
- Chenliang Zhou
- Long Wang
- Liang Zhong
-
Affiliations: Department of Anesthesiology, Renmin Hospital of Wuhan University, Wuhan, Hubei 430060, P.R. China, Department of Cardiology, Renmin Hospital of Wuhan University, Wuhan, Hubei 430060, P.R. China, Department of Critical Care Medicine, Renmin Hospital of Wuhan University, Wuhan, Hubei 430060, P.R. China, Department of Anesthesiology, Wuhan Medical and Healthcare Center for Women and Children, Wuhan, Hubei 430060, P.R. China - Published online on: March 20, 2020 https://doi.org/10.3892/mmr.2020.11034
- Pages: 2311-2320
-
Copyright: © Kang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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|
Kuang L, Zhu Y, Zhang J, Wu Y, Tian K, Chen X, Xue M, Tzang FC, Lau B, Wong BL, et al: A novel cross-linked haemoglobin-based oxygen carrier is beneficial to sepsis in rats. Artif Cells Nanomed Biotechnol. 47:1496–1504. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Moore JX, Donnelly JP, Griffin R, Howard G, Safford MM and Wang HE: Defining sepsis mortality clusters in the united states. Crit Care Med. 44:1380–1387. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Zaky A, Deem S, Bendjelid K and Treggiari MM: Characterization of cardiac dysfunction in sepsis: An ongoing challenge. Shock. 41:12–24. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Salvany S, Casanovas A, Tarabal O, Piedrafita L, Hernández S, Santafé M, Soto-Bernardini MC, Calderó J, Schwab MH and Esquerda JE: Localization and dynamic changes of neuregulin-1 at C-type synaptic boutons in association with motor neuron injury and repair. FASEB J. 33:7833–7851. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Seymour CW, Liu VX, Iwashyna TJ, Brunkhorst FM, Rea TD, Scherag A, Rubenfeld G, Kahn JM, Shankar-Hari M, Singer M, et al: Assessment of clinical criteria for sepsis: For the third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 315:762–774. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Shankar-Hari M, Phillips GS, Levy ML, Seymour CW, Liu VX, Deutschman CS, Angus DC, Rubenfeld GD and Singer M: Sepsis Definitions Task Force: Developing a new definition and assessing new clinical criteria for septic shock: For the third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 315:775–787. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, Bellomo R, Bernard GR, Chiche JD, Coopersmith CM, et al: The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 315:801–810. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Potz BA, Sellke FW and Abid MR: Endothelial ROS and impaired myocardial oxygen consumption in sepsis-induced cardiac dysfunction. J Intensive Crit Care. 2:202016. View Article : Google Scholar : PubMed/NCBI | |
|
Cimolai MC, Alvarez S, Bode C and Bugger H: Mitochondrial mechanisms in septic cardiomyopathy. Int J Mol Sci. 16:17763–17778. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Martin L, Derwall M, Thiemermann C and Schürholz T: Heart in sepsis: Molecular mechanisms, diagnosis and therapy of septic cardiomyopathy. Anaesthesist. 66:479–490. 2017.(In German). View Article : Google Scholar : PubMed/NCBI | |
|
DUva G, Aharonov A, Lauriola M, Kain D, Yahalom-Ronen Y, Carvalho S, Weisinger K, Bassat E, Rajchman D, Yifa O, et al: ERBB2 triggers mammalian heart regeneration by promoting cardiomyocyte dedifferentiation and proliferation. Nat Cell Biol. 17:627–638. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Brown D, Samsa LA, Ito C, Ma H, Batres K, Arnaout R, Qian L and Liu J: Neuregulin-1 is essential for nerve plexus formation during cardiac maturation. J Cell Mol Med. 22:2007–2017. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Hobai IA, Edgecomb J, LaBarge K and Colucci WS: Dysregulation of intracellular calcium transporters in animal models of sepsis-induced cardiomyopathy. Shock. 43:3–15. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yutzey KE: Regenerative biology: Neuregulin 1 makes heart muscle. Nature. 520:445–446. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou Q, Pan X, Wang L, Wang X and Xiong D: The protective role of neuregulin-1: A potential therapy for sepsis-induced cardiomyopathy. Eur J Pharmacol. 788:234–240. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Takasu O, Gaut JP, Watanabe E, To K, Fagley RE, Sato B, Jarman S, Efimov IR, Janks DL, Srivastava A, et al: Mechanisms of cardiac and renal dysfunction in patients dying of sepsis. Am J Respir Crit Care Med. 187:509–517. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Wang F, Wang H, Liu X, Yu H, Zuo B, Song Z, Wang N, Huang W and Wang G: Pharmacological postconditioning with Neuregulin-1 mimics the cardioprotective effects of ischaemic postconditioning via ErbB4-dependent activation of reperfusion injury salvage kinase pathway. Mol Med. 24:392018. View Article : Google Scholar : PubMed/NCBI | |
|
Galindo CL, Kasasbeh E, Murphy A, Ryzhov S, Lenihan S, Ahmad FA, Williams P, Nunnally A, Adcock J, et al: Anti-remodeling and anti-fibrotic effects of the neuregulin-1beta glial growth factor 2 in a large animal model of heart failure. J Am Heart Assoc. 4:e5282015. | |
|
Fang SJ, Li PY, Wang CM, Xin Y, Lu WW, Zhang XX, Zuo S, Ma CS, Tang CS, Nie SP, et al: Inhibition of endoplasmic reticulum stress by neuregulin-1 protects against myocardial ischemia/reperfusion injury. Peptides. 88:196–207. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Cai MX, Shi XC, Chen T, Tan ZN, Lin QQ, Du SJ and Tian ZJ: Exercise training activates neuregulin 1/ErbB signaling and promotes cardiac repair in a rat myocardial infarction model. Life Sci. 149:1–9. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Formiga FR, Pelacho B, Garbayo E, Imbuluzqueta I, Díaz-Herráez P, Abizanda G, Gavira JJ, Simón-Yarza T, Albiasu E, Tamayo E, et al: Controlled delivery of fibroblast growth factor-1 and neuregulin-1 from biodegradable microparticles promotes cardiac repair in a rat myocardial infarction model through activation of endogenous regeneration. J Control Release. 173:132–139. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Cohen JE, Purcell BP, MacArthur JW Jr, Mu A, Shudo Y, Patel JB, Brusalis CM, Trubelja A, Fairman AS, Edwards BB, et al: A bioengineered hydrogel system enables targeted and sustained intramyocardial delivery of neuregulin, activating the cardiomyocyte cell cycle and enhancing ventricular function in a murine model of ischemic cardiomyopathy. Circ Heart Fail. 7:619–626. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Sepúlveda M, Gonano LA, Viotti M, Morell M, Blanco P, López Alarcón M, Peroba Ramos I, Bastos Carvalho A, Medei E and Vila Petroff M: Calcium/Calmodulin protein kinase II-dependent ryanodine receptor phosphorylation mediates cardiac contractile dysfunction associated with sepsis. Crit Care Med. 45:e399–e408. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Brero A, Ramella R, Fitou A, Dati C, Alloatti G, Gallo MP and Levi R: Neuregulin-1beta1 rapidly modulates nitric oxide synthesis and calcium handling in rat cardiomyocytes. Cardiovasc Res. 88:443–452. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Candel FJ, Borges Sá M, Belda S, Bou G, Del Pozo JL, Estrada O, Ferrer R, González Del Castillo J, Julián-Jiménez A, Martín-Loeches I, et al: Current aspects in sepsis approach. Turning things around. Rev Esp Quimioter. 31:298–315. 2018.PubMed/NCBI | |
|
Bermejo-Martin JF, Martín-Fernandez M, López-Mestanza C, Duque P and Almansa R: Shared features of endothelial dysfunction between Sepsis and its preceding risk factors (Aging and Chronic Disease). J Clin Med. 7:4002018. View Article : Google Scholar : | |
|
Wu L, Walas S, Leung W, Sykes DB, Wu J, Lo EH and Lok J: Neuregulin1-β decreases IL-1β-induced neutrophil adhesion to human brain microvascular endothelial cells. Transl Stroke Res. 6:116–124. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Burger D and Touyz RM: Cellular biomarkers of endothelial health: Microparticles, endothelial progenitor cells, and circulating endothelial cells. J Am Soc Hypertens. 6:85–99. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Parodi EM and Kuhn B: Signalling between microvascular endothelium and cardiomyocytes through neuregulin. Cardiovasc Res. 102:194–204. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Hedhli N, Dobrucki LW, Kalinowski A, Zhuang ZW, Wu X, Russell RR III, Sinusas AJ and Russell KS: Endothelial-derived neuregulin is an important mediator of ischaemia-induced angiogenesis and arteriogenesis. Cardiovasc Res. 93:516–524. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Stefanou C, Karatzanos E, Mitsiou G, Psarra K, Angelopoulos E, Dimopoulos S, Gerovasili V, Boviatsis E, Routsi C and Nanas S: Neuromuscular electrical stimulation acutely mobilizes endothelial progenitor cells in critically ill patients with sepsis. Ann Intensive Care. 6:212016. View Article : Google Scholar : PubMed/NCBI | |
|
Awada HK, Hwang MP and Wang Y: Towards comprehensive cardiac repair and regeneration after myocardial infarction: Aspects to consider and proteins to deliver. Biomaterials. 82:94–112. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Lemmens K, Segers VF, Demolder M and De Keulenaer GW: Role of neuregulin-1/ErbB2 signaling in endothelium-cardiomyocyte cross-talk. J Biol Chem. 281:19469–19477. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Wu C, Gui C, Li L, Pang Y, Tang Z and Wei J: Expression and secretion of neuregulin-1 in cardiac microvascular endothelial cells treated with angiogenic factors. Exp Ther Med. 15:3577–3581. 2018.PubMed/NCBI | |
|
Fernandes CJ Jr and de Assuncao MS: Myocardial dysfunction in sepsis: A large, unsolved puzzle. Crit Care Res Pract. 2012:8964302012.PubMed/NCBI | |
|
Pathan N, Franklin JL, Eleftherohorinou H, Wright VJ, Hemingway CA, Waddell SJ, Griffiths M, Dennis JL, Relman DA, Harding SE, et al: Myocardial depressant effects of interleukin 6 in meningococcal sepsis are regulated by p38 mitogen-activated protein kinase. Crit Care Med. 39:1692–1711. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Pathan N, Hemingway CA, Alizadeh AA, Stephens AC, Boldrick JC, Oragui EE, McCabe C, Welch SB, Whitney A, OGara P, et al: Role of interleukin 6 in myocardial dysfunction of meningococcal septic shock. Lancet. 363:203–209. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Waage A, Brandtzaeg P, Halstensen A, Kierulf P and Espevik T: The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med. 169:333–338. 1989. View Article : Google Scholar : PubMed/NCBI | |
|
Leblais V, Jo SH, Chakir K, Maltsev V, Zheng M, Crow MT, Wang W, Lakatta EG and Xiao RP: Phosphatidylinositol 3-kinase offsets cAMP-mediated positive inotropic effect via inhibiting Ca2+ influx in cardiomyocytes. Circ Res. 95:1183–1190. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Britsch S: The neuregulin-I/ErbB signaling system in development and disease. Adv Anat Embryol Cell Biol. 190:1–65. 2007.PubMed/NCBI | |
|
Mencel M, Nash M and Jacobson C: Neuregulin upregulates microglial α7 nicotinic acetylcholine receptor expression in immortalized cell lines: Implications for regulating neuroinflammation. PLoS One. 8:e703382013. View Article : Google Scholar : PubMed/NCBI | |
|
Li Y, Lein PJ, Ford GD, Liu C, Stovall KC, White TE, Bruun DA, Tewolde T, Gates AS, Distel TJ, et al: Neuregulin-1 inhibits neuroinflammatory responses in a rat model of organophosphate-nerve agent-induced delayed neuronal injury. J Neuroinflammation. 12:642015. View Article : Google Scholar : PubMed/NCBI | |
|
Solomon W, Wilson NO, Anderson L, Pitts S, Patrickson J, Liu M, Ford BD and Stiles JK: Neuregulin-1 attenuates mortality associated with experimental cerebral malaria. J Neuroinflammation. 11:92014. View Article : Google Scholar : PubMed/NCBI | |
|
Gholami M, Mazaheri P, Mohamadi A, Dehpour T, Safari F, Hajizadeh S, Moore KP and Mani AR: Endotoxemia is associated with partial uncoupling of cardiac pacemaker from cholinergic neural control in rats. Shock. 37:219–227. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Fernandez R, Nardocci G, Navarro C, Reyes EP, Acuña-Castillo C and Cortes PP: Neural reflex regulation of systemic inflammation: Potential new targets for sepsis therapy. Front Physiol. 5:4892014. View Article : Google Scholar : PubMed/NCBI | |
|
Rosas-Ballina M, Valdés-Ferrer SI, Dancho ME, Ochani M, Katz D, Cheng KF, Olofsson PS, Chavan SS, Al-Abed Y, Tracey KJ, et al: Xanomeline suppresses excessive pro-inflammatory cytokine responses through neural signal-mediated pathways and improves survival in lethal inflammation. Brain Behav Immun. 44:19–27. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Matsukawa R, Hirooka Y, Ito K, Honda N and Sunagawa K: Central neuregulin-1/ErbB signaling modulates cardiac function via sympathetic activity in pressure overload-induced heart failure. J Hypertens. 32:817–825. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Schmidt H, Müller-Werdan U, Hoffmann T, Francis DP, Piepoli MF, Rauchhaus M, Prondzinsky R, Loppnow H, Buerke M, Hoyer D, et al: Autonomic dysfunction predicts mortality in patients with multiple organ dysfunction syndrome of different age groups. Crit Care Med. 33:1994–2002. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Jabbour A, Gao L, Kwan J, Watson A, Sun L, Qiu MR, Liu X, Zhou MD, Graham RM, Hicks M, et al: A recombinant human neuregulin-1 peptide improves preservation of the rodent heart after prolonged hypothermic storage. Transplantation. 91:961–967. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Fattahi F, Kalbitz M, Malan EA, Abe E, Jajou L, Huber-Lang MS, Bosmann M, Russell MW, Zetoune FS and Ward PA: Complement-induced activation of MAPKs and Akt during sepsis: role in cardiac dysfunction. FASEB J. 31:4129–4139. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Checchia PA, Schierding W, Polpitiya A, Dixon D, Macmillan S, Muenzer J, Stromberg P, Coopersmith CM, Buchman TG and Cobb JP: Myocardial transcriptional profiles in a murine model of sepsis: Evidence for the importance of age. Pediatr Crit Care Med. 9:530–535. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou H, Qian J, Li C, Li J, Zhang X, Ding Z, Gao X, Han Z, Cheng Y and Liu L: Attenuation of cardiac dysfunction by HSPA12B in endotoxin-induced sepsis in mice through a PI3K-dependent mechanism. Cardiovasc Res. 89:109–118. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Cvijanovich N, Shanley TP, Lin R, Allen GL, Thomas NJ, Checchia P, Anas N, Freishtat RJ, Monaco M, Odoms K, et al: Genomics of Pediatric SIRS/Septic Shock Investigators: Validating the genomic signature of pediatric septic shock. Physiol Genomics. 34:127–134. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Preau S, Delguste F, Yu Y, Remy-Jouet I, Richard V, Saulnier F, Boulanger E and Neviere R: Endotoxemia engages the RhoA kinase pathway to impair cardiac function by altering cytoskeleton, mitochondrial fission, and autophagy. Antioxid Redox Signal. 24:529–542. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Ky B, Kimmel SE, Safa RN, Putt ME, Sweitzer NK, Fang JC, Sawyer DB and Cappola TP: Neuregulin-1 beta is associated with disease severity and adverse outcomes in chronic heart failure. Circulation. 120:310–317. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Odiete O, Hill MF and Sawyer DB: Neuregulin in cardiovascular development and disease. Circ Res. 111:1376–1385. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Chen XL, Xia ZF, Wei D, Han S, Ben DF and Wang GQ: Role of p38 mitogen-activated protein kinase in Kupffer cell secretion of the proinflammatory cytokines after burn trauma. Burns. 29:533–539. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Mockridge JW, Marber MS and Heads RJ: Activation of Akt during simulated ischemia/reperfusion in cardiac myocytes. Biochem Biophys Res Commun. 270:947–952. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Talmor D, Applebaum A, Rudich A, Shapira Y and Tirosh A: Activation of mitogen-activated protein kinases in human heart during cardiopulmonary bypass. Circ Res. 86:1004–1007. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Dong X, Liu Y, Du M, Wang Q, Yu CT and Fan X: P38 mitogen-activated protein kinase inhibition attenuates pulmonary inflammatory response in a rat cardiopulmonary bypass model. Eur J Cardiothorac Surg. 30:77–84. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Menon R and Papaconstantinou J: p38 Mitogen activated protein kinase (MAPK): A new therapeutic target for reducing the risk of adverse pregnancy outcomes. Expert Opin Ther Targets. 20:1397–1412. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Antoon JW, Bratton MR, Guillot LM, Wadsworth S, Salvo VA, Elliott S, McLachlan JA and Burow ME: Pharmacology and anti-tumor activity of RWJ67657, a novel inhibitor of p38 mitogen activated protein kinase. Am J Cancer Res. 2:446–458. 2012.PubMed/NCBI | |
|
Kim SJ, Baek KS, Park HJ, Jung YH and Lee SM: Compound 9a, a novel synthetic histone deacetylase inhibitor, protects against septic injury in mice by suppressing MAPK signalling. Br J Pharmacol. 173:1045–1057. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Su J, Cui X, Li Y, Mani H, Ferreyra GA, Danner RL, Hsu LL, Fitz Y and Eichacker PQ: SB203580, a p38 inhibitor, improved cardiac function but worsened lung injury and survival during Escherichia coli pneumonia in mice. J Trauma. 68:1317–1327. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Zhou J, Wang Y, Yang C, Fu M, Zhang J, Han X, Li Z, Hu K and Ge J: Qiliqiangxin protects against anoxic injury in cardiac microvascular endothelial cells via NRG-1/ErbB-PI3K/Akt/mTOR pathway. J Cell Mol Med. 21:1905–1914. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Vessey DA, Li L and Kelley M: Ischemic preconditioning requires opening of pannexin-1/P2X(7) channels not only during preconditioning but again after index ischemia at full reperfusion. Mol Cell Biochem. 351:77–84. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhuo C, Wang Y, Wang X, Wang Y and Chen Y: Cardioprotection by ischemic postconditioning is abolished in depressed rats: Role of Akt and signal transducer and activator of transcription-3. Mol Cell Biochem. 346:39–47. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Kirabo A, Ryzhov S, Gupte M, Sengsayadeth S, Gumina RJ, Sawyer DB and Galindo CL: Neuregulin-1β induces proliferation, survival and paracrine signaling in normal human cardiac ventricular fibroblasts. J Mol Cell Cardiol. 105:59–69. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bopassa JC, Ferrera R, Gateau-Roesch O, Couture-Lepetit E and Ovize M: PI 3-kinase regulates the mitochondrial transition pore in controlled reperfusion and postconditioning. Cardiovasc Res. 69:178–185. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Rahman S, Li J, Bopassa JC, Umar S, Iorga A, Partownavid P and Eghbali M: Phosphorylation of GSK-3β mediates intralipid-induced cardioprotection against ischemia/reperfusion injury. Anesthesiology. 115:242–253. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Guo LW, Gao L, Rothschild J, Su B and Gelman IH: Control of protein kinase C activity, phorbol ester-induced cytoskeletal remodeling, and cell survival signals by the scaffolding protein SSeCKS/GRAVIN/AKAP12. J Biol Chem. 286:38356–38366. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Siafakas NM, Antoniou KM and Tzortzaki EG: Role of angiogenesis and vascular remodeling in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2:453–462. 2007.PubMed/NCBI | |
|
Mount PF, Kemp BE and Power DA: Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol. 42:271–279. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sawada N and Liao JK: Targeting eNOS and beyond: Emerging heterogeneity of the role of endothelial Rho proteins in stroke protection. Expert Rev Neurother. 9:1171–1186. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Rana MK and Worthylake RA: Novel mechanism for negatively regulating Rho-kinase (ROCK) signaling through Coronin1B protein in neuregulin 1 (NRG-1)-induced tumor cell motility. J Biol Chem. 287:21836–21845. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
van Nieuw Amerongen GP, Koolwijk P, Versteilen A and van Hinsbergh VW: Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler Thromb Vasc Biol. 23:211–217. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Anwar KN, Fazal F, Malik AB and Rahman A: RhoA/Rho-associated kinase pathway selectively regulates thrombin-induced intercellular adhesion molecule-1 expression in endothelial cells via activation of I kappa B kinase beta and phosphorylation of RelA/p65. J Immunol. 173:6965–6972. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Chang W, Xie JF, Xu JY and Yang Y: Effect of levosimendan on mortality in severe sepsis and septic shock: A meta-analysis of randomised trials. BMJ Open. 8:e0193382018. View Article : Google Scholar : PubMed/NCBI | |
|
Bonner JM and Boulianne GL: Diverse structures, functions and uses of FK506 binding proteins. Cell Signal. 38:97–105. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Bruno F, Xavier W and Ricard F: Safety and pharmacodynamic activity of a novel TREM-1 pathway inhibitory peptide in septic shock patients: Phase IIa clinical trial results. Intensive Care Med Exp. 6 (Suppl 1):1–33. 2018. | |
|
Fang SJ, Wu XS, Han ZH, Zhang XX, Wang CM, Li XY, Lu LQ and Zhang JL: Neuregulin-1 preconditioning protects the heart against ischemia/reperfusion injury through a PI3K/Akt-dependent mechanism. Chin Med J (Engl). 123:3597–3604. 2010.PubMed/NCBI | |
|
Zhou Z, Guo F, Dou Y, Tang J and Huan J: Guanine nucleotide exchange factor-H1 signaling is involved in lipopolysaccharide-induced endothelial barrier dysfunction. Surgery. 154:621–631. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Liu X, Gu X, Li Z, Li X, Li H, Chang J, Chen P, Jin J, Xi B, Chen D, et al: Neuregulin-1/erbB-activation improves cardiac function and survival in models of ischemic, dilated, and viral cardiomyopathy. J Am Coll Cardiol. 48:1438–1447. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Galindo CL, Kasasbeh E, Murphy A, Ryzhov S, Lenihan S, Ahmad FA, Williams P, Nunnally A, Adcock J, Song Y, et al: Anti-remodeling and anti-fibrotic effects of the neuregulin-1β glial growth factor 2 in a large animal model of heart failure. J Am Heart Assoc. 4:e0005282015.PubMed/NCBI | |
|
Bersell K, Arab S, Haring B and Kühn B: Neuregulin1/ErbB4 signaling induces cardiomyocyte proliferation and repair of heart injury. Cell. 138:257–270. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Sawyer DB, Zuppinger C, Miller TA, Eppenberger HM and Suter TM: Modulation of anthracycline-induced myofibrillar disarray in rat ventricular myocytes by neuregulin-1beta and anti-erbB2: Potential mechanism for trastuzumab-induced cardiotoxicity. Circulation. 105:1551–1554. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Grazette LP, Boecker W, Matsui T, Semigran M, Force TL, Hajjar RJ and Rosenzweig A: Inhibition of ErbB2 causes mitochondrial dysfunction in cardiomyocytes: Implications for herceptin-induced cardiomyopathy. J Am Coll Cardiol. 44:2231–2238. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Caillaud K, Boisseau N, Ennequin G, Chavanelle V, Etienne M, Li X, Denis P, Dardevet D, Lacampagne A and Sirvent P: Neuregulin 1 improves glucose tolerance in adult and old rats. Diabetes Metab. 42:96–104. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Zhuo X, Gao J, Liu H, Lin F and Ma A: Neuregulin-1β partially improves cardiac function in volume-overload heart failure through regulation of abnormal calcium handing. Front Pharmacol. 10:6162019. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Liu Z, Duan HN and Wang L: Therapeutic potential of neuregulin in cardiovascular system: Can we ignore the effects of neuregulin on electrophysiology? Mini Rev Med Chem. 16:867–871. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Jabbour A, Hayward CS, Keogh AM, Kotlyar E, McCrohon JA, England JF, Amor R, Liu X, Li XY, Zhou MD, et al: Parenteral administration of recombinant human neuregulin-1 to patients with stable chronic heart failure produces favourable acute and chronic haemodynamic responses. Eur J Heart Fail. 13:83–92. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Gao R, Zhang J, Cheng L, Wu X, Dong W, Yang X, Li T, Liu X, Xu Y, Li 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. J Am Coll Cardiol. 55:1907–1914. 2010. View Article : Google Scholar : PubMed/NCBI |
