Intercellular cross-talk is a fundamental process for spreading cellular signals between
neighbouring and distant cells to properly regulate their metabolism, to coordinate
homeostasis, adaptation and survival as a functional tissue and organ. In this review,
we take a close molecular view of the underpinning molecular mechanisms of such complex
intercellular communications. There are several studied forms of cell-to-cell communications
considered crucial for the maintenance of multicellular organisms. The most explored
is paracrine signalling which is realised through the release of diffusible signalling
factors (e.g., hormones or growth factors) from a donor cell and taken up by a recipient
cell. More challenging is communication which also does not require the direct contact
of cells but is organised through the release of named signalling factors embedded
in membranous structures. This mode of cell-to-cell communication is executed through
the transfer of extracellular vesicles. Two other types of cellular cross-communication
require direct contact of communicating cells. In one type, cells are connected by
gap junctions which regulate permeation of chemical signals addressed to a neighbouring
cell. Another type of cell communication is organised to provide a cytosolic continuum
of adjacent cells joined by different tiny cell membrane extensions coined tunnelling
nanotubes. In this review, we consider the various cell communication modes in the
heart, and examples of processes in non-cardiac cells which may have mechanistic parallels
with cardiovascular cells.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Heart, Lung and CirculationAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Structural and functional characterisation of cardiac fibroblasts.Cardiovasc Res. 2005; 65: 40-51
- Intramyocardial fibroblast myocyte communication.Circ Res. 2010; 106: 47-57
- Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes).J Biol Chem. 1987; 262: 9412-9420
- Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.Nat Cell Biol. 2007; 9: 654-659
- Cardiac myocyte exosomes: stability, HSP60, and proteomics.Am J Physiol Heart Circ Physiol. 2013; 304: H954-H965
- Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier.Nat Commun. 2015; 6: 6716
- Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system.J Neurosci. 2008; 28: 11024-11029
- Ribosomes in axons--scrounging from the neighbors?.Trends Cell Biol. 2009; 19: 236-243
- Exosomes are endogenous nanoparticles that can deliver biological information between cells.Adv Drug Deliv Rev. 2013; 65: 342-347
- Alterations in prostaglandin production in spontaneously hypertensive rat smooth muscle cells.Hypertension. 1993; 21: 900-905
- Microparticles in health and disease: small mediators, large role?.Curr Vasc Pharmacol. 2011; 9: 490-500
- Microparticles in cardiovascular disease pathophysiology and outcomes.J Am Soc Hypertens. 2012; 6: 243-252
- Mesenchymal stem cell-derived exosomes increase ATP levels, decrease oxidative stress and activate PI3K/Akt pathway to enhance myocardial viability and prevent adverse remodeling after myocardial ischemia/reperfusion injury.Stem Cell Res. 2013; 10: 301-312
- Roles of exosomes in cardioprotection.Eur Heart J. 2017; 38: 1372-1379
- Gap junction channels and cardiac impulse propagation.J Membr Biol. 2007; 218: 13-28
- Atomic force microscopy and dissection of gap junctions.Science. 1991; 253: 1405-1408
- Cross-presentation by intercellular peptide transfer through gap junctions.Nature. 2005; 434: 83-88
- Cell-to-cell diffusion of glucose in the mammalian heart is disrupted by high glucose. Implications for the diabetic heart.Exp Cell Res. 2015; 334: 239-245
- Dissecting the roles of microRNAs in coronary heart disease via integrative genomic analyses.Arterioscler Thromb Vasc Biol. 2015; 35: 1011-1021
- Effect of intracellular injection of calcium and strontium on cell communication in heart.J Physiol. 1975; 250: 231-245
- Magnesium gating of cardiac gap junction channels.Prog Biophys Mol Biol. 2010; 103: 102-110
- MicroRNA-133a engineered mesenchymal stem cells augment cardiac function and cell survival in the infarct heart.J Cardiovasc Pharmacol. 2015; 65: 241-251
- MicroRNA-26a regulates pathological and physiological angiogenesis by targeting BMP/SMAD1 signaling.Circ Res. 2013; 113: 1231-1241
- Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis.Proc Natl Acad Sci USA. 2008; 105: 13027-13032
- Nanotubular highways for intercellular organelle transport.Science. 2004; 303: 1007-1010
- Lipid droplets as a novel cargo of tunnelling nanotubes in endothelial cells.Sci Rep. 2015; 5: 11453
- Emerging physiological and pathological implications of tunneling nanotubes formation between cells.Eur J Cell Biol. 2015; 94: 429-443
- Membrane nanotubes physically connect T cells over long distances presenting a novel route for HIV-1 transmission.Nat Cell Biol. 2008; 10: 211-219
- Animal cells connected by nanotubes can be electrically coupled through interposed gap-junction channels.Proc Natl Acad Sci USA. 2010; 107: 17194-17199
- Selective block of tunneling nanotube (TNT) formation inhibits intercellular organelle transfer between PC12 cells.FEBS Lett. 2009; 583: 1481-1488
- Structurally distinct membrane nanotubes between human macrophages support long-distance vesicular traffic or surfing of bacteria.J Immunol. 2006; 177: 8476-8483
- Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture.J Cell Mol Med. 2008; 12: 1622-1631
- Networks of nanotubes and containers.Nature. 2001; 409: 150-152
- Routes and mechanisms of extracellular vesicle uptake.J Extracell Vesicles. 2014; 3
- Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells.Exp Cell Res. 2014; 323: 178-188
- Myocyte-fibroblast communication in cardiac fibrosis and arrhythmias: Mechanisms and model systems.J Mol Cell Cardiol. 2016; 94: 22-31
- The role of cholesterol-sphingomyelin membrane nanodomains in the stability of intercellular membrane nanotubes.Int J Nanomedicine. 2012; 7: 1891-1902
- Lipid rafts and B cell signaling.Semin Cell Dev Biol. 2007; 18: 616-626
- Sarcolemmal cholesterol and caveolin-3 dependence of cardiac function, ischemic tolerance, and opioidergic cardioprotection.Am J Physiol Heart Circ Physiol. 2014; 307: H895-H903
- A novel paradigm for heart failure with preserved ejection fraction: comorbidities drive myocardial dysfunction and remodeling through coronary microvascular endothelial inflammation.J Am Coll Cardiol. 2013; 62: 263-271
- The inflammatory response in myocardial injury, repair, and remodelling.Nat Rev Cardiol. 2014; 11: 255-265
- Cardiac inflammation contributes to changes in the extracellular matrix in patients with heart failure and normal ejection fraction.Circ Heart Fail. 2011; 4: 44-52
- A synaptic basis for T-lymphocyte activation.Ann Immunol (Paris). 1984; 135D: 113-134
- Adhesion-activating phorbol ester increases the mobility of leukocyte integrin LFA-1 in cultured lymphocytes.J Clin Invest. 1996; 97: 2139-2144
- Leukocyte polarization in cell migration and immune interactions.EMBO J. 1999; 18: 501-511
- The immunological synapse.Annu Rev Immunol. 2001; 19: 375-396
- Cell Fate through Metabolic Programming.Cell. 2016; 166: 63-76
- Leukocytes Crossing the Endothelium: A Matter of Communication.Int Rev Cell Mol Biol. 2016; 322: 281-329
- Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity.Cell. 1991; 67: 1033-1036
- Breaching multiple barriers: leukocyte motility through venular walls and the interstitium.Nat Rev Mol Cell Biol. 2010; 11: 366-378
- Cross-talk between macrophages and smooth muscle cells impairs collagen and metalloprotease synthesis and promotes angiogenesis.Biochim Biophys Acta. 2016; 1863: 1568-1578
- Endothelial and Smooth Muscle Cell Interactions in the Pathobiology of Pulmonary Hypertension.Am J Respir Cell Mol Biol. 2016; 54: 451-460
- Smooth muscle cells orchestrate the endothelial cell response to flow and injury.Circulation. 2010; 121: 2192-2199
- Regulation of cellular communication by signaling microdomains in the blood vessel wall.Pharmacol Rev. 2014; 66: 513-569
- Epistemology of the origin of cancer: a new paradigm.BMC Cancer. 2014; 14: 331
- Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential.Cardiovasc Res. 2010; 87: 300-310
- Cell-cell communication in the tumor microenvironment, carcinogenesis, and anticancer treatment.Cell Physiol Biochem. 2014; 34: 213-243
- Cross talk between cardiac myocytes and fibroblasts: from multiscale investigative approaches to mechanisms and functional consequences.Am J Physiol Heart Circ Physiol. 2012; 303: H1385-H1396
- Tumour-microenvironmental interactions: paths to progression and targets for treatment.Semin Cancer Biol. 2010; 20: 128-138
- Re-evaluation of fibroblasts and fibroblast-like cells.Anat Embryol (Berl). 1990; 182: 103-112
- Heterogeneity of myofibroblast phenotypic features: an example of fibroblastic cell plasticity.Virchows Arch. 1994; 425: 3-24
- The Biological Basis for Cardiac Repair After Myocardial Infarction: From Inflammation to Fibrosis.Circ Res. 2016; 119: 91-112
- Mitochondrial genome acquisition restores respiratory function and tumorigenic potential of cancer cells without mitochondrial DNA.Cell Metab. 2015; 21: 81-94
- Catapult-like release of mitochondrial DNA by eosinophils contributes to antibacterial defense.Nat Med. 2008; 14: 949-953
- Mitochondrial transplantation for therapeutic use.Clin Transl Med. 2016; 5: 16
- Evaluation of cardiac involvement during dengue viral infection.Clin Infect Dis. 2013; 57: 812-819
- West Nile virus myocarditis causing a fatal arrhythmia: a case report.Cases J. 2009; 2: 7147
- Myocarditis and cardiomyopathy after arbovirus infections (dengue and chikungunya fever).Br Heart J. 1972; 34: 821-827
- A clathrin, caveolae, and dynamin-independent endocytic pathway requiring free membrane cholesterol drives HIV-1 internalization and infection in polarized trophoblastic cells.J Mol Biol. 2007; 368: 1267-1283
- The Placenta as a Barrier to Viral Infections.Annu Rev Virol. 2014; 1: 133-146
- Stem cells and their niche: a matter of fate.Cell Mol Life Sci. 2006; 63: 760-766
- Two sides of the same coin: stem cells in cancer and regenerative medicine.FASEB J. 2014; 28: 2748-2761
- The hematopoietic stem-cell niche in health and leukemia.Cell Mol Life Sci. 2017; 74: 579-590
- Emerging Concepts in Paracrine Mechanisms in Regenerative Cardiovascular Medicine and Biology.Circ Res. 2016; 118: 95-107
- Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy.Annu Rev Physiol. 2015; 77: 13-27
- Extracellular vesicles: potential roles in regenerative medicine.Front Immunol. 2014; 5: 608
- Mesenchymal stem cell exosomes.Semin Cell Dev Biol. 2015; 40: 82-88
- Stem cells for the treatment of heart failure.Curr Res Transl Med. 2016; 64: 97-106
- Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles.Annu Rev Cell Dev Biol. 2014; 30: 255-289
- Polarization of human hematopoietic progenitors during contact with multipotent mesenchymal stromal cells: effects on proliferation and clonogenicity.Stem Cells Dev. 2006; 15: 815-829
- Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes?.Circ Res. 2005; 96: 1039-1041
- Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture.Exp Cell Res. 2010; 316: 2447-2455
- When cells become organelle donors.Physiology (Bethesda). 2013; 28: 414-422
- Mitochondrial transfer from bone-marrow-derived stromal cells to pulmonary alveoli protects against acute lung injury.Nat Med. 2012; 18: 759-765
- Miro1 regulates intercellular mitochondrial transport & enhances mesenchymal stem cell rescue efficacy.EMBO J. 2014; 33: 994-1010
- Mitochondrial transfer of induced pluripotent stem cell-derived mesenchymal stem cells to airway epithelial cells attenuates cigarette smoke-induced damage.Am J Respir Cell Mol Biol. 2014; 51: 455-465
- Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells.Blood. 2009; 113: 4197-4205
- Vascular smooth muscle cells initiate proliferation of mesenchymal stem cells by mitochondrial transfer via tunneling nanotubes.Stem Cells Dev. 2012; 21: 3104-3113
- Human mesenchymal stem cells reprogram adult cardiomyocytes toward a progenitor-like state through partial cell fusion and mitochondria transfer.Stem Cells. 2011; 29: 812-824
- The cardiac fibroblast: functional and electrophysiological considerations in healthy and diseased hearts.J Cardiovasc Pharmacol. 2011; 57: 380-388
- Molecular mechanisms of myocardial remodeling.Physiol Rev. 1999; 79: 215-262
- Perspectives on mammalian cardiovascular aging: humans to molecules.Comp Biochem Physiol A Mol Integr Physiol. 2002; 132: 699-721
- Cardiac fibroblasts: friend or foe?.Am J Physiol Heart Circ Physiol. 2006; 291: H1015-H1026
- Cardiac fibroblasts: at the heart of myocardial remodeling.Pharmacol Ther. 2009; 123: 255-278
- Communication signals between cardiac fibroblasts and cardiac myocytes.J Cardiovasc Pharmacol. 2011; 57: 513-521
- CTGF expression is induced by TGF- beta in cardiac fibroblasts and cardiac myocytes: a potential role in heart fibrosis.J Mol Cell Cardiol. 2000; 32: 1805-1819
- IL-33 and ST2 comprise a critical biomechanically induced and cardioprotective signaling system.J Clin Invest. 2007; 117: 1538-1549
- Interleukin-33 prevents apoptosis and improves survival after experimental myocardial infarction through ST2 signaling.Circ Heart Fail. 2009; 2: 684-691
- Basic fibroblast growth factor activates calcium channels in neonatal rat cardiomyocytes.J Biol Chem. 1995; 270: 17361-17367
- Fibroblast growth factor-2 decreases metabolic coupling and stimulates phosphorylation as well as masking of connexin43 epitopes in cardiac myocytes.Circ Res. 1996; 79: 647-658
- Structural coupling of cardiomyocytes and noncardiomyocytes: quantitative comparisons using a novel micropatterned cell pair assay.Am J Physiol Heart Circ Physiol. 2008; 295: H390-H400
- P2Y6 receptor-Galpha12/13 signalling in cardiomyocytes triggers pressure overload-induced cardiac fibrosis.EMBO J. 2008; 27: 3104-3115
- Pannexins and gap junction protein diversity.Cell Mol Life Sci. 2008; 65: 376-394
- Patterned growth of neonatal rat heart cells in culture. Morphological and electrophysiological characterization.Circ Res. 1991; 68: 114-130
- Connexin43 silencing in myofibroblasts prevents arrhythmias in myocardial cultures: role of maximal diastolic potential.Cardiovasc Res. 2012; 93: 434-444
- Cardiac alternans induced by fibroblast-myocyte coupling: mechanistic insights from computational models.Am J Physiol Heart Circ Physiol. 2009; 297: H775-H784
- Autonomic cardiac innervation: development and adult plasticity.Organogenesis. 2013; 9: 176-193
- The neurovascular unit, matrix proteases, and innate inflammation.Ann N Y Acad Sci. 2010; 1207: 46-49
- Protection of Neurovascular Unit Cells with Lithium Chloride and Sodium Valproate Prevents Brain Damage in Neonatal Ischemia/Hypoxia.Bull Exp Biol Med. 2016; 160: 313-318
- Volume transmission as a key feature of information handling in the central nervous system possible new interpretative value of the Turing's B-type machine.Prog Brain Res. 2000; 125: 3-19
- Hundred-fold increase in neuronal vulnerability to glutamate toxicity in astrocyte-poor cultures of rat cerebral cortex.Neurosci Lett. 1989; 103: 162-168
- Astrocytes from familial and sporadic ALS patients are toxic to motor neurons.Nat Biotechnol. 2011; 29: 824-828
- Transcellular degradation of axonal mitochondria.Proc Natl Acad Sci USA. 2014; 111: 9633-9638
- Transfer of mitochondria from astrocytes to neurons after stroke.Nature. 2016; 535: 551-555
- Intracoronary Delivery of Mitochondria to the Ischemic Heart for Cardioprotection.PLoS One. 2016; 11: e0160889
- Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury.Am J Physiol Heart Circ Physiol. 2013; 304: H966-H982
- Astrocytes shed large membrane vesicles that contain mitochondria, lipid droplets and ATP.Histochem Cell Biol. 2013; 139: 221-231
- Gap junctions mediate intercellular spread of sodium between hippocampal astrocytes in situ.Glia. 2012; 60: 239-252
- Astrocyte sodium signaling and neuro-metabolic coupling in the brain.Neuroscience. 2016; 323: 121-134
- Differential expression of three gap junction proteins in developing and mature brain tissues.Proc Natl Acad Sci USA. 1989; 86: 10148-10152
- Connexin30 in rodent, cat and human brain: selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance.Neuroscience. 1999; 88: 447-468
- Connexin43 null mice reveal that astrocytes express multiple connexins.Brain Res Brain Res Rev. 2000; 32: 45-56
- Hemichannels: new roles in astroglial function.Front Physiol. 2014; 5: 193
- Glomerular endothelial cell injury and cross talk in diabetic kidney disease.Am J Physiol Renal Physiol. 2015; 308: F287-F297
- Podocyte detachment and reduced glomerular capillary endothelial fenestration promote kidney disease in type 2 diabetic nephropathy.Kidney Int. 2012; 82: 1010-1017
- Deterioration of glomerular endothelial surface layer induced by oxidative stress is implicated in altered permeability of macromolecules in Zucker fatty rats.Diabetologia. 2010; 53: 2056-2065
- Vascular endothelial growth factor is increased during early stage of diabetic nephropathy in type II diabetic rats.J Endocrinol. 2004; 183: 183-194
- Podocyte-derived vascular endothelial growth factor mediates the stimulation of alpha3(IV) collagen production by transforming growth factor-beta1 in mouse podocytes.Diabetes. 2004; 53: 2939-2949
- Endothelin system: the double-edged sword in health and disease.Annu Rev Pharmacol Toxicol. 2001; 41: 851-876
- Roles of angiopoietins in kidney development and disease.J Am Soc Nephrol. 2009; 20: 239-244
- The endothelium as part of the integrative glomerular barrier complex.Kidney Int. 2014; 85: 8-11
- TNF-mediated damage to glomerular endothelium is an important determinant of acute kidney injury in sepsis.Kidney Int. 2014; 85: 72-81
- eNOS deficiency predisposes podocytes to injury in diabetes.J Am Soc Nephrol. 2012; 23: 1810-1823
- Overexpression of cyclooxygenase-2 predisposes to podocyte injury.J Am Soc Nephrol. 2007; 18: 551-559
- Atheroprotective communication between endothelial cells and smooth muscle cells through miRNAs.Nat Cell Biol. 2012; 14: 249-256
- Involvement of inducible nitric oxide synthase in the inflammatory process of myocardial infarction.Int J Cardiol. 1995; 50: 253-261
- Nitric oxide-dependent parasympathetic signaling is due to activation of constitutive endothelial (type III) nitric oxide synthase in cardiac myocytes.J Biol Chem. 1995; 270: 14582-14586
- Role of local production of endothelium-derived nitric oxide on cGMP signaling and S-nitrosylation.Am J Physiol Heart Circ Physiol. 2010; 298: H112-H118
- Soluble guanylate cyclase: the forgotten sibling.Trends Pharmacol Sci. 1997; 18: 484-491
- NO donors potentiate the beta-adrenergic stimulation of I(Ca,L) and the muscarinic activation of I(K,ACh) in rat cardiac myocytes.J Physiol. 2002; 540: 411-424
- Endogenous nitric oxide mechanisms mediate the stretch dependence of Ca2+ release in cardiomyocytes.Nat Cell Biol. 2001; 3: 867-873
- Involvement of lipid rafts and caveolae in cardiac ion channel function.Cardiovasc Res. 2006; 69: 798-807
- Mitochondria-localized caveolin in adaptation to cellular stress and injury.FASEB J. 2012; 26: 4637-4649
- Cardioprotective trafficking of caveolin to mitochondria is Gi-protein dependent.Anesthesiology. 2014; 121: 538-548
- Cell-specific targeting of caveolin-1 to caveolae, secretory vesicles, cytoplasm or mitochondria.J Cell Sci. 2001; 114: 1397-1408
- Caveolae as organizers of pharmacologically relevant signal transduction molecules.Annu Rev Pharmacol Toxicol. 2008; 48: 359-391
- Cardiac-specific overexpression of caveolin-3 induces endogenous cardiac protection by mimicking ischemic preconditioning.Circulation. 2008; 118: 1979-1988
- Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore.J Clin Invest. 2004; 113: 1535-1549
- Translocation of connexin 43 to the inner mitochondrial membrane of cardiomyocytes through the heat shock protein 90-dependent TOM pathway and its importance for cardioprotection.Circ Res. 2006; 99: 93-101
- Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo.J Biol Chem. 1997; 272: 25437-25440
- Recent insights in the paracrine modulation of cardiomyocyte contractility by cardiac endothelial cells.Biomed Res Int. 2014; 2014: 923805
- In vivo electrophysiologic studies in endothelial nitric oxide synthase (eNOS)-deficient mice.J Cardiovasc Electrophysiol. 2001; 12: 1295-1301
- Molecular mechanisms in endothelial regulation of cardiac function.Mol Cell Biochem. 2003; 253: 113-123
- Nitric oxide synthases in heart failure.Antioxid Redox Signal. 2013; 18: 1078-1099
- The role of the paracrine/autocrine mediator endothelin-1 in regulation of cardiac contractility and growth.Br J Pharmacol. 2013; 168: 296-317
- Endothelial cell-to-cell junctions: molecular organization and role in vascular homeostasis.Physiol Rev. 2004; 84: 869-901
McClanahan B, Nao BS, Wolke LJ, Martin BJ, Metz TE, and Gallagher KP. Brief renal occlusion and reperfusion reduces myocardial infarct size in rabbits. FASEB J. 7.
- Remote ischemic preconditioning: a novel protective method from ischemia reperfusion injury--a review.J Surg Res. 2008; 150: 304-330
- The mitochondria-targeted antioxidants and remote kidney preconditioning ameliorate brain damage through kidney-to-brain cross-talk.PLoS One. 2012; 7: e51553
- Acute kidney injury leads to inflammation and functional changes in the brain.J Am Soc Nephrol. 2008; 19: 1360-1370
- Kidney-brain crosstalk in the acute and chronic setting.Nat Rev Nephrol. 2015; 11: 707-719
- Ischaemic conditioning and reperfusion injury.Nat Rev Cardiol. 2016; 13: 193-209
- Remote ischemic conditioning.J Am Coll Cardiol. 2015; 65: 177-195
- Erythropoietin reduces myocardial infarction and left ventricular functional decline after coronary artery ligation in rats.Proc Natl Acad Sci USA. 2003; 100: 11612-11617
- Erythropoietin and the heart: physiological effects and the therapeutic perspective.Int J Cardiol. 2014; 171: 116-125
- Heart failure in patients with chronic kidney disease: a systematic integrative review.Biomed Res Int. 2014; 2014: 937398
- Heart failure and kidney dysfunction: epidemiology, mechanisms and management.Nat Rev Nephrol. 2016; 12: 610-623
- Cardiac abnormalities in liver cirrhosis.West J Med. 1989; 151: 530-535
- Cirrhotic cardiomyopathy.World J Gastroenterol. 2015; 21: 11502-11521
- Cardiovascular dysautonomia in Parkinson disease: from pathophysiology to pathogenesis.Neurobiol Dis. 2012; 46: 572-580
- Rhabdomyolosis and its pathogenesis.World J Emerg Med. 2012; 3: 11-15
- Blood exchange and hormonic reactions in parabiotic rats.Exptl. Zool. 1932; 63: 203-234
- Molecular and cellular interactions between mother and fetus. Pregnancy as a rejuvenating factor.Biochemistry (Mosc). 2016; 81: 1480-1487
- Studies on the mechanism of erythropoietic stimulation in parabiotic rats during hypoxia.Blood. 1950; 5: 372-380
- Aging, stem cells and tissue regeneration: lessons from muscle.Cell Cycle. 2005; 4: 407-410
- Rejuvenation of aged progenitor cells by exposure to a young systemic environment.Nature. 2005; 433: 760-764
- The ageing systemic milieu negatively regulates neurogenesis and cognitive function.Nature. 2011; 477: 90-94
- Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors.Science. 2014; 344: 630-634
- Young blood reverses age-related impairments in cognitive function and synaptic plasticity in mice.Nat Med. 2014; 20: 659-663
- Growth differentiation factor 11 is a circulating factor that reverses age-related cardiac hypertrophy.Cell. 2013; 153: 828-839
- Young capillary vessels rejuvenate aged pancreatic islets.Proc Natl Acad Sci USA. 2014; 111: 17612-17617
- Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle.Science. 2014; 344: 649-652
- Association of growth differentiation factor 11/8, putative anti-ageing factor, with cardiovascular outcomes and overall mortality in humans: analysis of the Heart and Soul and HUNT3 cohorts.Eur Heart J. 2015; 36: 3426-3434
- GDF11 does not rescue aging-related pathological hypertrophy.Circ Res. 2015; 117: 926-932
- Role of a paracrine action of mesenchymal stem cells in the improvement of left ventricular function after coronary artery occlusion in rats.Regen Med. 2007; 2: 63-68
- Growth and differentiation factor 11 (GDF11): Functions in the regulation of erythropoiesis and cardiac regeneration.Pharmacol Ther. 2015; 156: 26-33
- Pro-youthful” factors in the “labyrinth” of cardiac rejuvenation.Exp Gerontol. 2016; 83: 1-5
Article info
Publication history
Published online: January 23, 2017
Accepted:
December 6,
2016
Received in revised form:
November 22,
2016
Received:
November 6,
2016
Identification
Copyright
© 2017 Australian and New Zealand Society of Cardiac and Thoracic Surgeons (ANZSCTS) and the Cardiac Society of Australia and New Zealand (CSANZ). Published by Elsevier B.V. All rights reserved.
