Carbon nanotubes enhance intercalated disc assembly in cardiac myocytes via the β1-integrin-mediated signaling pathway

Biomaterials

Volumn 55, Issue , 2015, Pages 84-95

  Sun, Hongyu ^a,b   Lü, Shuanghong ^a   Jiang, Xiao Xia ^a   Li, Xia ^a   Li, Hong ^a   Lin, Qiuxia ^a   Mou, Yongchao ^a   Zhao, Yuwei ^a   Han, Yao ^a   Zhou, Jin ^a   Wang, Changyong ^a  

^a BEIJING INSTITUTE OF MICROBIOLOGY AND EPIDEMIOLOGY   (China)

^b CHENGDU MILITARY GENERAL HOSPITAL   (China)

Author keywords

Carbon nanotubes; Collagen; ERK; Intercalated disc; Neonatal cardiomyocytes; 1 integrin

Indexed keywords

CARBON; COLLAGEN; ELECTROPHYSIOLOGY; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; PROTEINS; SEMICONDUCTOR JUNCTIONS; TRANSIENT ANALYSIS; TRANSMISSION ELECTRON MICROSCOPY; YARN;

CARDIOMYOCYTES; ERK; IMMUNOHISTOCHEMICAL STAINING; INTEGRIN-MEDIATED SIGNALING; INTERCALATED DISC; INTRACELLULAR CALCIUM; MECHANICAL INTEGRITY; MYOCARDIAL INFARCTION;

CARBON NANOTUBES;

BETA1 INTEGRIN; COLLAGEN TYPE 1; FOCAL ADHESION KINASE; MESSENGER RNA; MOLECULAR SCAFFOLD; MYOCYTE ENHANCER FACTOR 2; NERVE CELL ADHESION MOLECULE; PLAKOGLOBIN; PLAKOPHILIN; PLAKOPHILIN 2; PROTEIN; PROTEIN C FOS; SINGLE WALLED NANOTUBE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR NKX2.5; TROPONIN I; UNCLASSIFIED DRUG; CALCIUM; CARBON NANOTUBE; COLLAGEN; CONNEXIN 43; CONNEXIN 43 PROTEIN, RAT; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL ADHESION; CELL GROWTH; CELL JUNCTION; CELL MATURATION; CELL MEMBRANE; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; DNA CONTENT; ELECTRIC CONDUCTIVITY; GAP JUNCTION; HEART MUSCLE CELL; IMMUNOHISTOCHEMISTRY; INTERCALATED DISC; INTRACELLULAR SIGNALING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; WESTERN BLOTTING; ANIMAL; CARDIAC MUSCLE CELL; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; MECHANICAL STRESS; METABOLISM; NANOMEDICINE; PROCEDURES; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TISSUE SCAFFOLD;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD29; CALCIUM; CELL ADHESION; CELL SURVIVAL; COLLAGEN; CONNEXIN 43; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GAP JUNCTIONS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MYOCYTES, CARDIAC; NANOMEDICINE; NANOTUBES, CARBON; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; STRESS, MECHANICAL; TISSUE SCAFFOLDS;

EID: 84932602833     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.03.030     Document Type: Article

References (49)

1. Laflamme M.A., Murry C.E. Heart regeneration. Nature 2011, 473:326-335.
2. Steinhauser M.L., Lee R.T. Regeneration of the heart. EMBO Mol Med 2011, 3:701-712.
3. Zimmermann W.H., Melnychenko I., Wasmeier G., Didié M., Naito H., Nixdorff U., et al. Engineered heart tissue grafts improve systolic and diastolic function in infarcted rat hearts. Nat Med 2006, 12:452-458.
4. Engelmayr G.C., Cheng M., Bettinger C.J., Borenstein J.T., Langer R., Freed L.E. Accordion-like honeycombs for tissue engineering of cardiac anisotropy. Nat Mater 2008, 7:1003-1010.
5. Ott H.C., Matthiesen T.S., Goh S.K., Black L.D., Kren S.M., Netoff T.I., et al. Perfusion-decellularized matrix: using nature's platform to engineer a bioartificial heart. Nat Med 2008, 14:213-221.
6. Fujimoto K.L., Tobita K., Merryman W.D., Guan J., Momoi N., Stolz D.B., et al. An elastic, biodegradable cardiac patch induces contractile smooth muscle and improves cardiac remodeling and function in subacute myocardial infarction. JAm Coll Cardiol 2007, 49:2292-2300.
7. Forbes M.S., Sperelakis N. Intercalated discs of mammalian heart: a review of structure and function. Tissue Cell 1985, 17:605-648.
8. Persidis A. Tissue engineering. Nat Biotechnol 1999, 17:508-510.
9. Zhou J., Shu Y., Lü S.H., Li J.J., Sun H.Y., Tang R.Y., et al. The spatiotemporal development of intercalated disk in three-dimensional engineered heart tissues based on collagen/matrigel matrix. PLoS One 2013, 8. e81420.
10. Dvir T., Timko B.P., Kohane D.S., Langer R. Nanotechnological strategies for engineering complex tissues. Nat Nanotechnol 2011, 6:13-22.
11. Dvir T., Timko B.P., Brigham M.D., Naik S.R., Karajanagi S.S., Levy O., et al. Nanowired three-dimensional cardiac patches. Nat Nanotechnol 2011, 6:720-725.
12. Tian B., Liu J., Dvir T., Jin L., Tsui J.H., Qing Q., et al. Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. Nat Mater 2012, 11:986-994.
13. Martinelli V., Cellot G., Toma F.M., Long C.S., Caldwell J.H., Zentilin L., et al. Carbon nanotubes promote growth and spontaneous electrical activity in cultured cardiac myocytes. Nano Lett 2012, 12:1831-1838.
14. Martinelli V., Cellot G., Maria Toma F., Long C.S., Caldwell J.H., Zentilin L., et al. Carbon nanotubes instruct physiological growth and functionally mature syncytia: nongenetic engineering of cardiac myocytes. ACS Nano 2013, 7:5746-5756.
15. Shin S.R., Jung S.M., Zalabany M., Kim K., Zorlutuna P., Kim S.B., et al. Carbon-Nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators. ACS Nano 2013, 7:2369-2380.
16. Kharaziha M., Shin S.R., Nikkhah M., Topkaya S.N., Masoumi N., Annabi N., et al. Tough and flexible CNT-polymeric hybrid scaffolds for engineering cardiac constructs. Biomaterials 2014, 35:7346-7354.
17. Pok S., Vitale F., Eichmann S.L., Benavides O.M., Pasquali M., Jacot J.G. Biocompatible carbon nanotube-chitosan scaffold matching the electrical conductivity of the heart. ACS Nano 2014, 8:9822-9832.
18. Zhou J., Chen J., Sun H., Qiu X., Mou Y., Liu Z., et al. Engineering the heart: evaluation of conductive nanomaterials for improving implant integration and cardiac function. Sci Rep 2014, 4:3733.
19. Li X., Zhou J., Liu Z., Chen J., Lü S., Sun H., et al. APNIPAAm-based thermosensitive hydrogel containing SWCNTs for stem cell transplantation in myocardial repair. Biomaterials 2014, 35:5679-5688.
20. Robinson K.A., Li J., Mathison M., Redkar A., Cui J., Chronos N.A., et al. Extracellular matrix scaffold for cardiac repair. Circulation 2005, 112:I135-I143.
21. Friedland J.C., Lee M.H., Boettiger D. Mechanically activated integrin switch controls alpha5beta1 function. Science 2009, 323:642-644.
22. Ross R.S., Borg T.K. Integrins and the myocardium. Circ Res 2001, 88:1112-1119.
23. Israeli-Rosenberg S., Manso A.M., Okada H., Ross R.S. Integrins and integrin-associated proteins in the cardiac myocyte. Circ Res 2014, 114:572-586.
24. Shanker A.J., Green K.G., Saffitz J.E. Matrix protein-specific regulation of Cx43 expression in cardiac myocytes subjected to mechanical load. Circ Res 2005, 96:567-575.
25. Yamada K., Green K.G., Samarel A.M., Saffitz J.E. Distinct pathways regulate expression of cardiac electrical and mechanical junction proteins in response to stretch. Circ Res 2005, 97:346-353.
26. Van der Heyden M.A., Rook M.B., Hermans M.M., Rijksen G., Boonstra J., Defize L.H., et al. Identification of connexin43 as a functional target for Wnt signaling. JCell Sci 1998, 111:1741-1749.
27. Jia G., Cheng G., Gangahar D.M., Agrawal D.K. Involvement of connexin 43 in angiotensin II-induced migration and proliferation of saphenous vein smooth muscle cells via the MAPK-AP-1 signaling pathway. JMol Cell Cardiol 2008, 44:882-890.
28. Sirnes S., Kjenseth A., Leithe E., Rivedal E. Interplay between PKC and the MAPkinase pathway in connexin43 phosphorylation and inhibition of gap junction intercellular communication. Biochem Biophys Res Commun 2009, 382:41-45.
29. Dunn C.A., Su V., Lau A.F., Lampe P.D. Activation of Akt, not connexin 43 protein ubiquitination, regulates gap junction stability. JBiol Chem 2012, 287:2600-2607.
30. Samarel A.M. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am J Physiol Heart Circ Physiol 2005, 289:H2291-H2301.
31. Mitra S.K., Hanson D.A., Schlaepfer D.D. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol 2005, 6:56-68.
32. Oyamada M., Takebe K., Oyamada Y. Regulation of connexin expression by transcription factors and epigenetic mechanisms. Biochim Biophys Acta 2013, 1828:118-133.
33. Liu D., Yi C., Zhang D., Zhang J., Yang M. Inhibition of proliferation and differentiation of mesenchymal stem cells by carboxylated carbon nanotubes. ACS Nano 2010, 4:2185-2195.
34. Liu D., Zhao M., Li Y., Bian Z., Zhang L., Shang Y., et al. Solid-state, polymer-based fiber solar cells with carbon nanotube electrodes. ACS Nano 2012, 6:11027-11034.
35. Shao S., Zhou S., Li L., Li J., Luo C., Wang J., et al. Osteoblast function on electrically conductive electrospun PLA/MWCNTs nanofibers. Biomaterials 2011, 32:2821-2833.
36. Zimmermann W.H., Schneiderbanger K., Schubert P., Didié M., Münzel F., Heubach J.F., et al. Tissue engineering of a differentiated cardiac muscle construct. Circ Res 2002, 90:223-230.
37. Cho Y., Borgens R.B. The effect of an electrically conductive carbon nanotube/collagen composite on neurite outgrowth of PC12 cells. JBiomed Mater Res A 2010, 95:510-517.
38. Hsiao C.W., Bai M.Y., Chang Y., Chung M.F., Lee T.Y., Wu C.T., et al. Electrical coupling of isolated cardiomyocyte clusters grown on aligned conductive nanofibrous meshes for their synchronized beating. Biomaterials 2013, 34:1063-1072.
39. Noorman M., van der Heyden M.A., van Veen T.A., Cox M.G., Hauer R.N., de Bakker J.M., et al. Cardiac cell-cell junctions in health and disease: electrical versus mechanical coupling. JMol Cell Cardiol 2009, 47:23-31.
40. Oxford E.M., Musa H., Maass K., Coombs W., Taffet S.M., Delmar M. Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ Res 2007, 101:703-711.
41. Li J., Levin M.D., Xiong Y., Petrenko N., Patel V.V., Radice G.L. N-cadherin haploinsufficiency affects cardiac gap junctions and arrhythmic susceptibility. JMol Cell Cardiol 2008, 44:597-606.
42. Kostin S., Hein S., Bauer E.P., Schaper J. Spatiotemporal development and distribution of intercellular junctions in adult rat cardiomyocytes in culture. Circ Res 1999, 85:154-167.
43. Hynes R.O. Integrins: bidirectional, allosteric signaling machines. Cell 2002, 110:673-687.
44. Valencik M.L., Zhang D., Punske B., Hu P., McDonald J.A., Litwin S.E. Integrin activation in the heart: a link between electrical and contractile dysfunction?. Circ Res 2006, 99:1403-1410.
45. Hu H., Ni Y., Montana V., Haddon R.C., Parpura V. Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett 2004, 4:507-511.
46. Linhares V.L., Almeida N.A., Menezes D.C., Elliott D.A., Lai D., Beyer E.C., et al. Transcriptional regulation of the murine connexin40 promoter by cardiac factors Nkx2-5, GATA4 and Tbx5. Cardiovasc Res 2004, 64:402-411.
47. Yamada S., Nelson W.J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. JCell Biol 2007, 178:517-527.
48. Price L.S., Leng J., Schwartz M.A., Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol Biol Cell 1998, 9:1863-1871.
49. Costa P., Scales T.M., Ivaska J., Parsons M. Integrin-specific control of focal adhesion kinase and RhoA regulates membrane protrusion and invasion. PLoS One 2013, 8. e74659.