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Article: Lack of Cardiac Nerve Sprouting after Intramyocardial Transplantation of Bone Marrow-Derived Stem Cells in a Swine Model of Chronic Ischemic Myocardium

TitleLack of Cardiac Nerve Sprouting after Intramyocardial Transplantation of Bone Marrow-Derived Stem Cells in a Swine Model of Chronic Ischemic Myocardium
Authors
KeywordsArrhythmia
Bone marrow cells
Connecxin 43
Ischemia
Nerve sprouting
Issue Date2012
PublisherSpringer New York
Citation
Journal Of Cardiovascular Translational Research, 2012, v. 5 n. 3, p. 359-365 How to Cite?
AbstractPrevious experimental studies suggested that mesenchymal stem cell transplantation causes cardiac nerve sprouting; however, whether bone marrow (BM)-derived mononuclear cells (MNC) and endothelial progenitor cells (EPC) can also lead to cardiac nerve sprouting and alter gap junction expression remains unclear. We investigated the effect of electroanatomical mapping-guided direct intramyocardial transplantation of BM-MNC (n = 8) and CD31 +EPC (n = 8) compared with saline control (n = 8) on cardiac nerve sprouting and gap junction expression in a swine model of chronic ischemic myocardium. At 12 weeks after transplantation, the distribution and density of cardiac nerve sprouting were determined by staining of tyrosine hydroxylase (TH) and growth associated protein 43(GAP-43) and expression of connexin 43 in the targeted ischemic and remote normal myocardium. After 12 weeks, no animal developed sudden death after the transplantation. There were no significant differences in the number of cells with positive staining of TH and GAP-43 in the ischemic and normal myocardium between three groups. Furthermore, expression of connexin 43 was also similar in the ischemic and normal myocardia in each group of animals (P > 0.05). The results of this study demonstrated that intramyocardial BM-derived MNC or EPC transplantation in a large animal model of chronic myocardial ischemia was not associated with increased cardiac nerve sprouting over the ischemic myocardium. © 2012 The Author(s).
Persistent Identifierhttp://hdl.handle.net/10722/147105
ISSN
2015 Impact Factor: 3.197
2015 SCImago Journal Rankings: 1.567
PubMed Central ID
ISI Accession Number ID
Funding AgencyGrant Number
Research Grants Council of Hong KongHKU 7594/05 M
HKU 7769/08 M
HKU 8/CRF/09
Funding Information:

This study was supported by Research Grants Council of Hong Kong, General Research Fund (No. HKU 7594/05 M, HKU 7769/08 M), Outstanding Researcher Award 2007-2008 (H.F.T) and Collaborative Research Fund of Hong Kong Research Grant Council (HKU 8/CRF/09).

References

Siu, C. W., Liao, S. Y., Liu, Y., Lian, Q., & Tse, H. F. (2010). Stem cells for myocardial repair. Thrombosis and Haemostasis, 104(1), 6–12. doi: 10.1160/TH09-05-0336

Fuchs, S., Kornowski, R., Weisz, G., et al. (2006). Safety and feasibility of transendocardial autologous bone marrow cell transplantation in patients with advanced heart disease. The American Journal of Cardiology, 97(6), 823–829. doi: 10.1016/j.amjcard.2005.09.132

Gavira, J. J., Nasarre, E., Abizanda, G., et al. (2010). Repeated implantation of skeletal myoblast in a swine model of chronic myocardial infarction. European Heart Journal, 31(8), 1013–1021. doi: 10.1093/eurheartj/ehp342

Tse, H. F., Siu, C. W., Zhu, S. G., et al. (2007). Paracrine effects of direct intramyocardial implantation of bone marrow derived cells to enhance neovascularization in chronic ischaemic myocardium. European Journal of Heart Failure, 9(8), 747–753. doi: 10.1016/j.ejheart.2007.03.008

Tse, H. F., Thambar, S., Kwong, Y. L., et al. (2007). Prospective randomized trial of direct endomyocardial implantation of bone marrow cells for treatment of severe coronary artery diseases (PROTECT-CAD trial). European Heart Journal, 28(24), 2998–3005. doi: 10.1093/eurheartj/ehm485

Van Ramshorst, J., Bax, J. J., Beeres, S. L., et al. (2009). Intramyocardial bone marrow cell injection for chronic myocardial ischemia: A randomized controlled trial. Journal of the American Medical Association, 301(19), 1997–2004. doi: 10.1001/jama.2009.685

Losordo, D. W., Henry, T. D., Davidson, C., et al. (2011). Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circulation Research, 109(4), 428–436. doi: 10.1161/CIRCRESAHA.111.245993

Liao, S. Y., Liu, Y., Siu, C. W., et al. (2010). Proarrhythmic risk of embryonic stem cell-derived cardiomyocyte transplantation in infarcted myocardium. Heart Rhythm, 7(12), 1852–1859. doi: 10.1016/j.hrthm.2010.09.006

Gepstein, L., Ding, C., Rehemedula, D., et al. (2010). In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells, 28(12), 2151–2161. doi: 10.1002/stem.545

Lai, A. C., Wallner, K., Cao, J. M., et al. (2000). Colocalization of tenascin and sympathetic nerves in a canine model of nerve sprouting and sudden cardiac death. Journal of Cardiovascular Electrophysiology, 11(12), 1345–1351. doi: 10.1046/j.1540-8167.2000.01345.x

Pak, H. N., Qayyum, M., Kim, D. T., et al. (2003). Mesenchymal stem cell injection induces cardiac nerve sprouting and increased tenascin expression in a swine model of myocardial infarction. Journal of Cardiovascular Electrophysiology, 14(8), 841–848. doi: 10.1046/j.1540-8167.2003.03124.x

Kim, S. K., Pak, H. N., Park, J. H., et al. (2010). Cardiac cell therapy with mesenchymal stem cell induces cardiac nerve sprouting, angiogenesis, and reduced connexin43-positive gap junctions, but concomitant electrical pacing increases connexin43-positive gap junctions in canine heart. Cardiology in the Young, 20(3), 308–317. doi: 10.1017/S1047951110000132

Meiri, K. F., Pfenninger, K. H., & Willard, M. B. (1986). Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp 46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci USA, 83(10), 3537–3541. doi: 10.1073/pnas.83.10.3537

Li, W., Knowlton, D., Van Winkle, D. M., & Habecker, B. A. (2004). Infarction alters both the distribution and noradrenergic properties of cardiac sympathetic neurons. American Journal of Physiology - Heart and Circulatory Physiology, 286(6), H2229–H2236. doi: 10.1152/ajpheart.00768.2003

Kim, S. U., & De Vellis, J. (2009). Stem cell-based cell therapy in neurological diseases: A review. Journal of Neuroscience Research, 87(10), 2183–2200. doi: 10.1002/jnr.22054

Wen, Z., Zheng, S., Zhou, C., Wang, J., & Wang, T. (2011). Repair mechanisms of bone marrow mesenchymal stem cells in myocardial infarction. Journal of Cellular and Molecular Medicine, 15(5), 1032–1043. doi: 10.1111/j.1582-4934.2010.01255.x

Decrock, E., Vinken, M., De Vuyst, E., et al. (2009). Connexin-related signaling in cell death: To live or let die? Cell Death and Differentiation, 16(4), 524–536. doi: 10.1038/cdd.2008.196

Miura, T., Miki, T., & Yano, T. (2010). Role of the gap junction in ischemic preconditioning in the heart. American Journal of Physiology - Heart and Circulatory Physiology, 298(4), H1115–H1125. doi: 10.1152/ajpheart.00879.2009

Grants

 

DC FieldValueLanguage
dc.contributor.authorLiu, Yen_HK
dc.contributor.authorLai, WHen_HK
dc.contributor.authorLiao, SYen_HK
dc.contributor.authorSiu, CWen_HK
dc.contributor.authorYang, YZen_HK
dc.contributor.authorTse, HFen_HK
dc.date.accessioned2012-05-28T08:17:13Z-
dc.date.available2012-05-28T08:17:13Z-
dc.date.issued2012en_HK
dc.identifier.citationJournal Of Cardiovascular Translational Research, 2012, v. 5 n. 3, p. 359-365en_HK
dc.identifier.issn1937-5387en_HK
dc.identifier.urihttp://hdl.handle.net/10722/147105-
dc.description.abstractPrevious experimental studies suggested that mesenchymal stem cell transplantation causes cardiac nerve sprouting; however, whether bone marrow (BM)-derived mononuclear cells (MNC) and endothelial progenitor cells (EPC) can also lead to cardiac nerve sprouting and alter gap junction expression remains unclear. We investigated the effect of electroanatomical mapping-guided direct intramyocardial transplantation of BM-MNC (n = 8) and CD31 +EPC (n = 8) compared with saline control (n = 8) on cardiac nerve sprouting and gap junction expression in a swine model of chronic ischemic myocardium. At 12 weeks after transplantation, the distribution and density of cardiac nerve sprouting were determined by staining of tyrosine hydroxylase (TH) and growth associated protein 43(GAP-43) and expression of connexin 43 in the targeted ischemic and remote normal myocardium. After 12 weeks, no animal developed sudden death after the transplantation. There were no significant differences in the number of cells with positive staining of TH and GAP-43 in the ischemic and normal myocardium between three groups. Furthermore, expression of connexin 43 was also similar in the ischemic and normal myocardia in each group of animals (P > 0.05). The results of this study demonstrated that intramyocardial BM-derived MNC or EPC transplantation in a large animal model of chronic myocardial ischemia was not associated with increased cardiac nerve sprouting over the ischemic myocardium. © 2012 The Author(s).en_HK
dc.languageengen_US
dc.publisherSpringer New Yorken_US
dc.relation.ispartofJournal of Cardiovascular Translational Researchen_HK
dc.rightsThe Author(s)en_US
dc.rightsCreative Commons: Attribution 3.0 Hong Kong Licenseen_US
dc.subjectArrhythmiaen_HK
dc.subjectBone marrow cellsen_HK
dc.subjectConnecxin 43en_HK
dc.subjectIschemiaen_HK
dc.subjectNerve sproutingen_HK
dc.titleLack of Cardiac Nerve Sprouting after Intramyocardial Transplantation of Bone Marrow-Derived Stem Cells in a Swine Model of Chronic Ischemic Myocardiumen_HK
dc.typeArticleen_HK
dc.identifier.openurlhttp://www.springerlink.com/link-out/?id=2104&code=11N88507322519JP&MUD=MPen_US
dc.identifier.emailSiu, CW:cwdsiu@hkucc.hku.hken_HK
dc.identifier.emailTse, HF:hftse@hkucc.hku.hken_HK
dc.identifier.authoritySiu, CW=rp00534en_HK
dc.identifier.authorityTse, HF=rp00428en_HK
dc.description.naturepublished_or_final_versionen_US
dc.identifier.doi10.1007/s12265-012-9350-2en_HK
dc.identifier.pmid22302631-
dc.identifier.pmcidPMC3349852-
dc.identifier.scopuseid_2-s2.0-84865842065en_HK
dc.identifier.hkuros205039-
dc.relation.referencesSiu, C. W., Liao, S. Y., Liu, Y., Lian, Q., & Tse, H. F. (2010). Stem cells for myocardial repair. Thrombosis and Haemostasis, 104(1), 6–12.en_US
dc.relation.referencesdoi: 10.1160/TH09-05-0336en_US
dc.relation.referencesFuchs, S., Kornowski, R., Weisz, G., et al. (2006). Safety and feasibility of transendocardial autologous bone marrow cell transplantation in patients with advanced heart disease. The American Journal of Cardiology, 97(6), 823–829.en_US
dc.relation.referencesdoi: 10.1016/j.amjcard.2005.09.132en_US
dc.relation.referencesGavira, J. J., Nasarre, E., Abizanda, G., et al. (2010). Repeated implantation of skeletal myoblast in a swine model of chronic myocardial infarction. European Heart Journal, 31(8), 1013–1021.en_US
dc.relation.referencesdoi: 10.1093/eurheartj/ehp342en_US
dc.relation.referencesTse, H. F., Siu, C. W., Zhu, S. G., et al. (2007). Paracrine effects of direct intramyocardial implantation of bone marrow derived cells to enhance neovascularization in chronic ischaemic myocardium. European Journal of Heart Failure, 9(8), 747–753.en_US
dc.relation.referencesdoi: 10.1016/j.ejheart.2007.03.008en_US
dc.relation.referencesTse, H. F., Thambar, S., Kwong, Y. L., et al. (2007). Prospective randomized trial of direct endomyocardial implantation of bone marrow cells for treatment of severe coronary artery diseases (PROTECT-CAD trial). European Heart Journal, 28(24), 2998–3005.en_US
dc.relation.referencesdoi: 10.1093/eurheartj/ehm485en_US
dc.relation.referencesVan Ramshorst, J., Bax, J. J., Beeres, S. L., et al. (2009). Intramyocardial bone marrow cell injection for chronic myocardial ischemia: A randomized controlled trial. Journal of the American Medical Association, 301(19), 1997–2004.en_US
dc.relation.referencesdoi: 10.1001/jama.2009.685en_US
dc.relation.referencesLosordo, D. W., Henry, T. D., Davidson, C., et al. (2011). Intramyocardial, autologous CD34+ cell therapy for refractory angina. Circulation Research, 109(4), 428–436.en_US
dc.relation.referencesdoi: 10.1161/CIRCRESAHA.111.245993en_US
dc.relation.referencesLiao, S. Y., Liu, Y., Siu, C. W., et al. (2010). Proarrhythmic risk of embryonic stem cell-derived cardiomyocyte transplantation in infarcted myocardium. Heart Rhythm, 7(12), 1852–1859.en_US
dc.relation.referencesdoi: 10.1016/j.hrthm.2010.09.006en_US
dc.relation.referencesGepstein, L., Ding, C., Rehemedula, D., et al. (2010). In vivo assessment of the electrophysiological integration and arrhythmogenic risk of myocardial cell transplantation strategies. Stem Cells, 28(12), 2151–2161.en_US
dc.relation.referencesdoi: 10.1002/stem.545en_US
dc.relation.referencesCao, J. M., Chen, L. S., Kenknight, B. H., et al. (2000). Nerve sprouting and sudden cardiac death. Circulation Research, 86(7), 816–821.en_US
dc.relation.referencesLai, A. C., Wallner, K., Cao, J. M., et al. (2000). Colocalization of tenascin and sympathetic nerves in a canine model of nerve sprouting and sudden cardiac death. Journal of Cardiovascular Electrophysiology, 11(12), 1345–1351.en_US
dc.relation.referencesdoi: 10.1046/j.1540-8167.2000.01345.xen_US
dc.relation.referencesCao, J. M., Fishbein, M. C., Han, J. B., et al. (2000). Relationship between regional cardiac hyperinnervation and ventricular arrhythmia. Circulation, 101(16), 1960–1969.en_US
dc.relation.referencesPak, H. N., Qayyum, M., Kim, D. T., et al. (2003). Mesenchymal stem cell injection induces cardiac nerve sprouting and increased tenascin expression in a swine model of myocardial infarction. Journal of Cardiovascular Electrophysiology, 14(8), 841–848.en_US
dc.relation.referencesdoi: 10.1046/j.1540-8167.2003.03124.xen_US
dc.relation.referencesKim, S. K., Pak, H. N., Park, J. H., et al. (2010). Cardiac cell therapy with mesenchymal stem cell induces cardiac nerve sprouting, angiogenesis, and reduced connexin43-positive gap junctions, but concomitant electrical pacing increases connexin43-positive gap junctions in canine heart. Cardiology in the Young, 20(3), 308–317.en_US
dc.relation.referencesdoi: 10.1017/S1047951110000132en_US
dc.relation.referencesMeiri, K. F., Pfenninger, K. H., & Willard, M. B. (1986). Growth-associated protein, GAP-43, a polypeptide that is induced when neurons extend axons, is a component of growth cones and corresponds to pp 46, a major polypeptide of a subcellular fraction enriched in growth cones. Proc Natl Acad Sci USA, 83(10), 3537–3541.en_US
dc.relation.referencesdoi: 10.1073/pnas.83.10.3537en_US
dc.relation.referencesLi, W., Knowlton, D., Van Winkle, D. M., & Habecker, B. A. (2004). Infarction alters both the distribution and noradrenergic properties of cardiac sympathetic neurons. American Journal of Physiology - Heart and Circulatory Physiology, 286(6), H2229–H2236.en_US
dc.relation.referencesdoi: 10.1152/ajpheart.00768.2003en_US
dc.relation.referencesKim, S. U., & De Vellis, J. (2009). Stem cell-based cell therapy in neurological diseases: A review. Journal of Neuroscience Research, 87(10), 2183–2200.en_US
dc.relation.referencesdoi: 10.1002/jnr.22054en_US
dc.relation.referencesWen, Z., Zheng, S., Zhou, C., Wang, J., & Wang, T. (2011). Repair mechanisms of bone marrow mesenchymal stem cells in myocardial infarction. Journal of Cellular and Molecular Medicine, 15(5), 1032–1043.en_US
dc.relation.referencesdoi: 10.1111/j.1582-4934.2010.01255.xen_US
dc.relation.referencesDecrock, E., Vinken, M., De Vuyst, E., et al. (2009). Connexin-related signaling in cell death: To live or let die? Cell Death and Differentiation, 16(4), 524–536.en_US
dc.relation.referencesdoi: 10.1038/cdd.2008.196en_US
dc.relation.referencesMiura, T., Miki, T., & Yano, T. (2010). Role of the gap junction in ischemic preconditioning in the heart. American Journal of Physiology - Heart and Circulatory Physiology, 298(4), H1115–H1125.en_US
dc.relation.referencesdoi: 10.1152/ajpheart.00879.2009en_US
dc.identifier.volume5en_US
dc.identifier.issue3en_US
dc.identifier.spage1en_HK
dc.identifier.epage7en_HK
dc.identifier.eissn1937-5395en_US
dc.identifier.isiWOS:000304111300015-
dc.description.otherSpringer Open Choice, 28 May 2012en_US
dc.relation.projectPluripotent Human Stem Cell Platform for Tissue Regeneration and Drug Screening for Cardiovascular Diseases-
dc.identifier.scopusauthoridLiu, Y=54936707200en_HK
dc.identifier.scopusauthoridLai, WH=18434390500en_HK
dc.identifier.scopusauthoridLiao, SY=22433820700en_HK
dc.identifier.scopusauthoridSiu, CW=7006550690en_HK
dc.identifier.scopusauthoridYang, YZ=54934733400en_HK
dc.identifier.scopusauthoridTse, HF=7006070805en_HK
dc.identifier.citeulike10330369-

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