Intrinsic cardiac adrenergic cells contribute to LPS-induced myocardial dysfunction.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
25 01 2022
25 01 2022
Historique:
received:
06
04
2021
accepted:
23
12
2021
entrez:
26
1
2022
pubmed:
27
1
2022
medline:
25
3
2022
Statut:
epublish
Résumé
Intrinsic cardiac adrenergic (ICA) cells regulate both developing and adult cardiac physiological and pathological processes. However, the role of ICA cells in septic cardiomyopathy is unknown. Here we show that norepinephrine (NE) secretion from ICA cells is increased through activation of Toll-like receptor 4 (TLR4) to aggravate myocardial TNF-α production and dysfunction by lipopolysaccharide (LPS). In ICA cells, LPS activated TLR4-MyD88/TRIF-AP-1 signaling that promoted NE biosynthesis through expression of tyrosine hydroxylase, but did not trigger TNF-α production due to impairment of p65 translocation. In a co-culture consisting of LPS-treated ICA cells and cardiomyocytes, the upregulation and secretion of NE from ICA cells activated cardiomyocyte β
Identifiants
pubmed: 35079095
doi: 10.1038/s42003-022-03007-6
pii: 10.1038/s42003-022-03007-6
pmc: PMC8789803
doi:
Substances chimiques
Cardiovascular Agents
0
Lipopolysaccharides
0
Tlr4 protein, mouse
0
Toll-Like Receptor 4
0
Norepinephrine
X4W3ENH1CV
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
96Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 81871542
Informations de copyright
© 2022. The Author(s).
Références
Aneman, A. & Vieillard-Baron, A. Cardiac dysfunction in sepsis. Intensive Care Med. 42, 2073–2076 (2016).
pubmed: 27544139
doi: 10.1007/s00134-016-4503-4
Hollenberg, S. M. & Singer, M. Pathophysiology of sepsis-induced cardiomyopathy. Nat. Rev. Cardiol. 18, 424–434 (2021).
pubmed: 33473203
doi: 10.1038/s41569-020-00492-2
Avlas, O., Fallach, R., Shainberg, A., Porat, E. & Hochhauser, E. Toll-like receptor 4 stimulation initiates an inflammatory response that decreases cardiomyocyte contractility. Antioxid. Redox Signal. 15, 1895–1909 (2011).
pubmed: 21126202
doi: 10.1089/ars.2010.3728
van der Poll, T., van de Veerdonk, F. L., Scicluna, B. P. & Netea, M. G. The immunopathology of sepsis and potential therapeutic targets. Nat. Rev. Immunol. 17, 407–420 (2017).
pubmed: 28436424
doi: 10.1038/nri.2017.36
Lv, X. & Wang, H. Pathophysiology of sepsis-induced myocardial dysfunction. Military Med. Res. 3, 30 (2016).
doi: 10.1186/s40779-016-0099-9
Han, C. et al. Acute inflammation stimulates a regenerative response in the neonatal mouse heart. Cell Res. 25, 1137–1151 (2015).
pubmed: 26358185
pmcid: 4650627
doi: 10.1038/cr.2015.110
Honda, T., He, Q., Wang, F. & Redington, A. N. Acute and chronic remote ischemic conditioning attenuate septic cardiomyopathy, improve cardiac output, protect systemic organs, and improve mortality in a lipopolysaccharide-induced sepsis model. Basic Res. Cardiol. 114, 15 (2019).
pubmed: 30838474
doi: 10.1007/s00395-019-0724-3
Rudiger, A. & Singer, M. Mechanisms of sepsis-induced cardiac dysfunction. Crit. Care Med. 35, 1599–1608 (2007).
pubmed: 17452940
doi: 10.1097/01.CCM.0000266683.64081.02
Andreis, D. T. & Singer, M. Catecholamines for inflammatory shock: a Jekyll-and-Hyde conundrum. Intensive Care Med. 42, 1387–1397 (2016).
pubmed: 26873833
doi: 10.1007/s00134-016-4249-z
Staedtke, V. et al. Disruption of a self-amplifying catecholamine loop reduces cytokine release syndrome. Nature 564, 273–277 (2018).
pubmed: 30542164
pmcid: 6512810
doi: 10.1038/s41586-018-0774-y
Wang, Y. et al. Beta(1)-adrenoceptor stimulation promotes LPS-induced cardiomyocyte apoptosis through activating PKA and enhancing CaMKII and IkappaBalpha phosphorylation. Crit. Care 19, 76 (2015).
pubmed: 25887954
pmcid: 4383083
doi: 10.1186/s13054-015-0820-1
Morelli, A. et al. Effect of heart rate control with esmolol on hemodynamic and clinical outcomes in patients with septic shock: a randomized clinical trial. Jama 310, 1683–1691 (2013).
pubmed: 24108526
doi: 10.1001/jama.2013.278477
Kimmoun, A. et al. beta1-Adrenergic inhibition improves cardiac and vascular function in experimental septic shock. Crit. Care Med. 43, e332–e340 (2015).
pubmed: 25962080
doi: 10.1097/CCM.0000000000001078
Huang, M. H. et al. An intrinsic adrenergic system in mammalian heart. J. Clin. Investig. 98, 1298–1303 (1996).
pubmed: 8823294
pmcid: 507555
doi: 10.1172/JCI118916
Ebert, S. N. & Thompson, R. P. Embryonic epinephrine synthesis in the rat heart before innervation: association with pacemaking and conduction tissue development. Circ. Res. 88, 117–124 (2001).
pubmed: 11139483
doi: 10.1161/01.RES.88.1.117
Tamura, Y. et al. Neural crest-derived resident cardiac cells contribute to the restoration of adrenergic function of transplanted heart in rodent. Cardiovasc. Res. 109, 350–357 (2016).
pubmed: 26645983
doi: 10.1093/cvr/cvv267
Huang, M. H. et al. Reducing ischaemia/reperfusion injury through delta-opioid-regulated intrinsic cardiac adrenergic cells: adrenopeptidergic co-signalling. Cardiovasc. Res. 84, 452–460 (2009).
pubmed: 19581316
doi: 10.1093/cvr/cvp233
van Eif, V. W., Bogaards, S. J. & van der Laarse, W. J. Intrinsic cardiac adrenergic (ICA) cell density and MAO-A activity in failing rat hearts. J. Muscle Res. Cell Motility 35, 47–53 (2014).
doi: 10.1007/s10974-013-9373-6
Huang, M. H. et al. Mediating delta-opioid-initiated heart protection via the beta2-adrenergic receptor: role of the intrinsic cardiac adrenergic cell. Am. J. Physiol. Heart Circ. 293, H376–H384 (2007).
doi: 10.1152/ajpheart.01195.2006
Mahmoud, A. I. & Lee, R. T. Adrenergic function restoration in the transplanted heart: a role for neural crest-derived cells. Cardiovasc. Res. 109, 348–349 (2016).
pubmed: 26786156
pmcid: 4752047
doi: 10.1093/cvr/cvw013
Huang, M. H. et al. Neuroendocrine properties of intrinsic cardiac adrenergic cells in fetal rat heart. Am. J. Physiol. Heart Circ. 288, H497–H503 (2005).
doi: 10.1152/ajpheart.00591.2004
Yu, X. et al. adrenoceptor activation by norepinephrine inhibits LPS-induced cardiomyocyte TNF-α production via modulating ERK1/2 and NF-κB pathway. J. Cell. Mol. Med. 18, 263–273 (2014).
pubmed: 24304472
doi: 10.1111/jcmm.12184
Natarajan, A. R., Rong, Q., Katchman, A. N. & Ebert, S. N. Intrinsic cardiac catecholamines help maintain beating activity in neonatal rat cardiomyocyte cultures. Pediatr. Res. 56, 411–417 (2004).
pubmed: 15333759
doi: 10.1203/01.PDR.0000136279.80897.4C
Yang, D. et al. A new method for neonatal rat ventricular myocyte purification using superparamagnetic iron oxide particles. Int. J. Cardiol. 270, 293–301 (2018).
pubmed: 29908831
doi: 10.1016/j.ijcard.2018.05.133
Flierl, M. A. et al. Phagocyte-derived catecholamines enhance acute inflammatory injury. Nature 449, 721–725 (2007).
pubmed: 17914358
doi: 10.1038/nature06185
Rittirsch, D., Flierl, M. A. & Ward, P. A. Harmful molecular mechanisms in sepsis. Nat. Rev. Immunol. 8, 776–787 (2008).
pubmed: 18802444
pmcid: 2786961
doi: 10.1038/nri2402
Frantz, S. et al. Toll4 (TLR4) expression in cardiac myocytes in normal and failing myocardium. J. Clin. Investig. 104, 271–280 (1999).
pubmed: 10430608
pmcid: 408420
doi: 10.1172/JCI6709
Lysakova-Devine, T. et al. Viral inhibitory peptide of TLR4, a peptide derived from vaccinia protein A46, specifically inhibits TLR4 by directly targeting MyD88 adaptor-like and TRIF-related adaptor molecule. J. Immunol. 185, 4261–4271 (2010).
pubmed: 20802145
doi: 10.4049/jimmunol.1002013
Nagamoto-Combs, K., Piech, K. M., Best, J. A., Sun, B. & Tank, A. W. Tyrosine hydroxylase gene promoter activity is regulated by both cyclic AMP-responsive element and AP1 sites following calcium influx. Evidence for cyclic amp-responsive element binding protein-independent regulation. J. Biol. Chem. 272, 6051–6058 (1997).
pubmed: 9038229
doi: 10.1074/jbc.272.9.6051
Anest, V. et al. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 423, 659–663 (2003).
pubmed: 12789343
doi: 10.1038/nature01648
Mittal, M. et al. TNFα-stimulated gene-6 (TSG6) activates macrophage phenotype transition to prevent inflammatory lung injury. Proc. Natl Acad. Sci. USA 113, E8151–E8158 (2016).
pubmed: 27911817
pmcid: 5167170
doi: 10.1073/pnas.1614935113
Whelan, R. S., Konstantinidis, K., Xiao, R. P. & Kitsis, R. N. Cardiomyocyte life-death decisions in response to chronic beta-adrenergic signaling. Circ. Res. 112, 408–410 (2013).
pubmed: 23371896
doi: 10.1161/CIRCRESAHA.113.300805
Gonzalez, G. A. & Montminy, M. R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675–680 (1989).
pubmed: 2573431
doi: 10.1016/0092-8674(89)90013-5
Grimm, M. & Brown, J. H. β-Adrenergic receptor signaling in the heart: role of CaMKII. J. Mol. Cell. Cardiol. 48, 322–330 (2010).
pubmed: 19883653
doi: 10.1016/j.yjmcc.2009.10.016
Sepúlveda, M. et al. Calcium/calmodulin protein kinase II-dependent ryanodine receptor phosphorylation mediates cardiac contractile dysfunction associated with sepsis. Crit. Care Med. 45, e399–e408 (2017).
pubmed: 27648519
doi: 10.1097/CCM.0000000000002101
Stapel, B. et al. Low STAT3 expression sensitizes to toxic effects of beta-adrenergic receptor stimulation in peripartum cardiomyopathy. Eur. Heart J. 38, 349–361 (2017).
pubmed: 28201733
Wang, W. et al. Sustained beta1-adrenergic stimulation modulates cardiac contractility by Ca2+/calmodulin kinase signaling pathway. Circ. Res. 95, 798–806 (2004).
pubmed: 15375008
doi: 10.1161/01.RES.0000145361.50017.aa
Wagner, D. R. et al. Adenosine inhibits lipopolysaccharide-induced cardiac expression of tumor necrosis factor-alpha. Circ. Res. 82, 47–56 (1998).
pubmed: 9440704
doi: 10.1161/01.RES.82.1.47
Zhang, F. F. et al. Stimulation of spinal dorsal horn beta2-adrenergic receptor ameliorates neuropathic mechanical hypersensitivity through a reduction of phosphorylation of microglial p38 MAP kinase and astrocytic c-jun N-terminal kinase. Neurochem. Int. 101, 144–155 (2016).
pubmed: 27840124
doi: 10.1016/j.neuint.2016.11.004
Tibayan, F. A., Chesnutt, A. N., Folkesson, H. G., Eandi, J. & Matthay, M. A. Dobutamine increases alveolar liquid clearance in ventilated rats by beta-2 receptor stimulation. Am. J. Resp. Crit. Care Med. 156, 438–444 (1997).
pubmed: 9279221
doi: 10.1164/ajrccm.156.2.9609141
Liao, R., Podesser, B. K. & Lim, C. C. The continuing evolution of the Langendorff and ejecting murine heart: new advances in cardiac phenotyping. Am. J. Physiol. Heart Circ. 303, H156–H167 (2012).
doi: 10.1152/ajpheart.00333.2012
Bell, R. M., Mocanu, M. M. & Yellon, D. M. Retrograde heart perfusion: the Langendorff technique of isolated heart perfusion. J. Mol. Cell Cardiol. 50, 940–950 (2011).
pubmed: 21385587
doi: 10.1016/j.yjmcc.2011.02.018
Zhou, Q. Y., Quaife, C. J. & Palmiter, R. D. Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development. Nature 374, 640–643 (1995).
pubmed: 7715703
doi: 10.1038/374640a0
Thomas, S. A., Matsumoto, A. M. & Palmiter, R. D. Noradrenaline is essential for mouse fetal development. Nature 374, 643–646 (1995).
pubmed: 7715704
doi: 10.1038/374643a0
Fedele, L. & Brand, T. The intrinsic cardiac nervous system and its role in cardiac pacemaking and conduction. J Cardiovasc. Dev. Dis. 7, 54 (2020).
pmcid: 7712215
doi: 10.3390/jcdd7040054
Ebert, S. N. & Taylor, D. G. Catecholamines and development of cardiac pacemaking: an intrinsically intimate relationship. Cardiovasc. Res. 72, 364–374 (2006).
pubmed: 17022958
doi: 10.1016/j.cardiores.2006.08.013
Nguyen, V. T. et al. Delta-opioid augments cardiac contraction through beta-adrenergic and CGRP-receptor co-signaling. Peptides 33, 77–82 (2012).
pubmed: 22108711
doi: 10.1016/j.peptides.2011.11.010
Huang, M. H., Poh, K. K., Tan, H. C., Welt, F. G. & Lui, C. Y. Therapeutic synergy and complementarity for ischemia/reperfusion injury: beta1-adrenergic blockade and phosphodiesterase-3 inhibition. Int. J. Cardiol. 214, 374–380 (2016).
pubmed: 27085132
doi: 10.1016/j.ijcard.2016.03.200
Saygili, E. et al. Irregular electrical activation of intrinsic cardiac adrenergic cells increases catecholamine-synthesizing enzymes. Biochem. Biophys. Res. Commun. 413, 432–435 (2011).
pubmed: 21907185
doi: 10.1016/j.bbrc.2011.08.113
Sreejit, P., Kumar, S. & Verma, R. S. An improved protocol for primary culture of cardiomyocyte from neonatal mice. In Vitro Cell. Dev. Biol. - Animal 44, 45–50 (2008).
doi: 10.1007/s11626-007-9079-4
Zhao, J. et al. The different response of cardiomyocytes and cardiac fibroblasts to mitochondria inhibition and the underlying role of STAT3. Basic Res. Cardiol. 114, 12 (2019).
pubmed: 30767143
doi: 10.1007/s00395-019-0721-6
Sorriento, D. et al. Endothelial cells are able to synthesize and release catecholamines both in vitro and in vivo. Hypertension 60, 129–136 (2012).
pubmed: 22665130
doi: 10.1161/HYPERTENSIONAHA.111.189605
Jiménez, N., Krouwer, V. J. D. & Post, J. A. A new, rapid and reproducible method to obtain high quality endothelium in vitro. Cytotechnology 65, 1–14 (2013).
pubmed: 22573289
doi: 10.1007/s10616-012-9459-9
Zhao, M., Zhou, A., Xu, L. & Zhang, X. The role of TLR4-mediated PTEN/PI3K/AKT/NF-κB signaling pathway in neuroinflammation in hippocampal neurons. Neuroscience 269, 93–101 (2014).
pubmed: 24680857
doi: 10.1016/j.neuroscience.2014.03.039
Huang, H. P. et al. Physiology of quantal norepinephrine release from somatodendritic sites of neurons in locus coeruleus. Front. Mol. Neurosci. 5, 29 (2012).
pubmed: 22408604
pmcid: 3295224
doi: 10.3389/fnmol.2012.00029
Girard-Joyal, O. & Ismail, N. Effect of LPS treatment on tyrosine hydroxylase expression and Parkinson-like behaviors. Hormones Behavior 89, 1–12 (2017).
pubmed: 28025041
doi: 10.1016/j.yhbeh.2016.12.009
Zhu, W. Z. et al. Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J. Clin. Investig. 111, 617–625 (2003).
pubmed: 12618516
pmcid: 151893
doi: 10.1172/JCI200316326
Singh, M. V. et al. MyD88 mediated inflammatory signaling leads to CaMKII oxidation, cardiac hypertrophy and death after myocardial infarction. J. Mol. Cell. Cardiol. 52, 1135–1144 (2012).
pubmed: 22326848
pmcid: 3327770
doi: 10.1016/j.yjmcc.2012.01.021
National Research Council Committee for the Update of the Guide for the, C. & Use of Laboratory, A. The National Academies Collection: Reports funded by National Institutes of Health. in Guide for the Care and Use of Laboratory Animals (National Academies Press (US) Copyright © 2011, National Academy of Sciences., Washington (DC), 2011).
Choudhry, M. A., Bland, K. I. & Chaudry, I. H. Gender and susceptibility to sepsis following trauma. Endocrine, Metabolic Immune Disorders Drug Targets 6, 127–135 (2006).
pubmed: 16787286
doi: 10.2174/187153006777442422
van Eijk, L. T. et al. Gender differences in the innate immune response and vascular reactivity following the administration of endotoxin to human volunteers. Crit. Care Med. 35, 1464–1469 (2007).
pubmed: 17452928
doi: 10.1097/01.CCM.0000266534.14262.E8
Yu, X. et al. alpha2A-adrenergic blockade attenuates septic cardiomyopathy by increasing cardiac norepinephrine concentration and inhibiting cardiac endothelial activation. Sci. Rep. 8, 5478 (2018).
pubmed: 29615637
pmcid: 5882799
doi: 10.1038/s41598-018-23304-7
Stanley, W. C. et al. Catecholamine modulatory effects of nepicastat (RS-25560-197), a novel, potent and selective inhibitor of dopamine-beta-hydroxylase. Br. J. Pharmacol. 121, 1803–1809 (1997).
pubmed: 9283721
pmcid: 1564872
doi: 10.1038/sj.bjp.0701315
Golden, H. B. et al. Isolation of cardiac myocytes and fibroblasts from neonatal rat pups. Methods Mol. Biol. 843, 205–214 (2012).
pubmed: 22222535
doi: 10.1007/978-1-61779-523-7_20
Dimitriadis, G., Neto, J. P. & Kampff, A. R. t-SNE visualization of large-scale neural recordings. Neural Comput. 30, 1750–1774 (2018).
pubmed: 29894653
doi: 10.1162/neco_a_01097
You, F. et al. ELF4 is critical for induction of type I interferon and the host antiviral response. Nat. Immunol. 14, 1237–1246 (2013).
pubmed: 24185615
pmcid: 3939855
doi: 10.1038/ni.2756
Hu, Y., O’Boyle, K., Auer, J. & Raju, S. Multiple UBXN family members inhibit retrovirus and lentivirus production and canonical NFκΒ signaling by stabilizing IκBα. PLoS Pathogens 13, e1006187 (2017).
pubmed: 28152074
pmcid: 5308826
doi: 10.1371/journal.ppat.1006187
Zhang, X., Goncalves, R. & Mosser, D. M. The isolation and characterization of murine macrophages. Curr. Protocols Immunol. Chapter 14, Unit 14.11 (2008).