Myoblast cell grafting into heart muscle: cellular biology and potential applications.

This review surveys a wide range of cellular and molecular approaches to strengthening the injured or weakened heart, focusing on strategies to replace dysfunctional, necrotic, or apoptotic cardiomyocytes with new cells of mesodermal origin. A variety of cell types, including myogenic cell lines, adult skeletal myoblasts, immoratalized atrial cells, embryonic and adult cardiomyocytes, embryonic stem cells, tetratoma cells, genetically altered fibroblasts, smooth muscle cells, and bone marrow-derived cells have all been proposed as useful cells in cardiac repair and may have the capacity to perform cardiac work. We focus on the implantation of mesodermally derived cells, the best developed of the options. We review the developmental and cell biology that have stimulated these studies, examine the limitations of current knowledge, and identify challenges for the future, which we believe are considerable.

[1]  Doris A Taylor,et al.  Regenerating functional myocardium: Improved performance after skeletal myoblast transplantation , 1998, Nature Medicine.

[2]  M. Soonpaa,et al.  Survey of studies examining mammalian cardiomyocyte DNA synthesis. , 1998, Circulation research.

[3]  J. Seidman,et al.  Congenital heart disease caused by mutations in the transcription factor NKX2-5. , 1998, Science.

[4]  P. Anversa,et al.  Myocyte cell death in the diseased heart. , 1998, Circulation research.

[5]  R. Michler,et al.  Triple immunosuppression reduces mononuclear cell infiltration and prolongs graft life in pig-to-newborn baboon cardiac xenotransplantation. , 1998, The Journal of thoracic and cardiovascular surgery.

[6]  D. Smith,et al.  Cardiomyocyte transplantation in a porcine myocardial infarction model. , 1998, Cell transplantation.

[7]  R. Virmani,et al.  Arrhythmogenic right ventricular cardiomyopathy and fatty replacement of the right ventricular myocardium: are they different diseases? , 1998, Circulation.

[8]  P. McCarthy,et al.  One hundred patients with the HeartMate left ventricular assist device: evolving concepts and technology. , 1998, The Journal of thoracic and cardiovascular surgery.

[9]  D. Prockop,et al.  Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats--similarities to astrocyte grafts. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[10]  N J Izzo,et al.  HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[11]  G Cossu,et al.  Muscle regeneration by bone marrow-derived myogenic progenitors. , 1998, Science.

[12]  T Walther,et al.  Minimally invasive port-access mitral valve surgery. , 1998, The Journal of thoracic and cardiovascular surgery.

[13]  R. Class,et al.  Marrow stromal cells as a source of progenitor cells for nonhematopoietic tissues in transgenic mice with a phenotype of osteogenesis imperfecta. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  C. Harley,et al.  Extension of life-span by introduction of telomerase into normal human cells. , 1998, Science.

[15]  H. Sucov,et al.  Molecular insights into cardiac development. , 1998, Annual review of physiology.

[16]  S. Hauschka,et al.  P19 embryonal carcinoma cells: a model system for studying neural tube induction of skeletal myogenesis. , 1997, Developmental biology.

[17]  R R Markwald,et al.  Mixed cultures of avian blastoderm cells and the quail mesoderm cell line QCE-6 provide evidence for the pluripotentiality of early mesoderm. , 1997, Developmental biology.

[18]  A. Hagège,et al.  Does transplantation of cardiomyocytes improve function of infarcted myocardium? , 1997, Circulation.

[19]  R. Weisel,et al.  Natural history of fetal rat cardiomyocytes transplanted into adult rat myocardial scar tissue. , 1997, Circulation.

[20]  N. Smedira,et al.  Early results with partial left ventriculectomy. , 1997, The Journal of thoracic and cardiovascular surgery.

[21]  M. Frasch,et al.  ladybird, a new component of the cardiogenic pathway in Drosophila required for diversification of heart precursors. , 1997, Development.

[22]  L. Kunkel,et al.  The fate of individual myoblasts after transplantation into muscles of DMD patients , 1997, Nature Medicine.

[23]  H. Zakon,et al.  Transdifferentiation of muscle to electric organ: regulation of muscle-specific proteins is independent of patterned nerve activity. , 1997, Developmental biology.

[24]  K. Saigo,et al.  Requirements of DFR1/Heartless, a mesoderm-specific Drosophila FGF-receptor, for the formation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in CNS. , 1997, Development.

[25]  G. Koh,et al.  Cyclin D1 overexpression promotes cardiomyocyte DNA synthesis and multinucleation in transgenic mice. , 1997, The Journal of clinical investigation.

[26]  M. Fishman,et al.  Fashioning the vertebrate heart: earliest embryonic decisions. , 1997, Development.

[27]  W. Kraus,et al.  Delivery of primary autologous skeletal myoblasts into rabbit heart by coronary infusion: a potential approach to myocardial repair. , 1997, Proceedings of the Association of American Physicians.

[28]  E. Olson,et al.  Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. , 1997, Genes & development.

[29]  K Sigrist,et al.  GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. , 1997, Genes & development.

[30]  J. Brockes,et al.  Amphibian Limb Regeneration: Rebuilding a Complex Structure , 1997, Science.

[31]  D. Prockop.  Marrow Stromal Cells as Stem Cells for Nonhematopoietic Tissues , 1997, Science.

[32]  E. Olson.  Things are developing in cardiology. , 1997, Circulation research.

[33]  L. Leinwand,et al.  Report of the National Heart, Lung, and Blood Institute Special Emphasis Panel on Heart Failure Research. , 1997, Circulation.

[34]  A. Lassar,et al.  A role for bone morphogenetic proteins in the induction of cardiac myogenesis. , 1997, Genes & development.

[35]  Takayuki Asahara,et al.  Isolation of Putative Progenitor Endothelial Cells for Angiogenesis , 1997, Science.

[36]  M. Aoki,et al.  Survival of grafts of genetically modified cardiac myocytes transfected with FITC-labeled oligodeoxynucleotides and the β-galactosidase gene in the noninfarcted area, but not the myocardial infarcted area , 1997, Gene Therapy.

[37]  A. Gann,et al.  Newt Myotubes Reenter the Cell Cycle by Phosphorylation of the Retinoblastoma Protein , 1997, The Journal of cell biology.

[38]  G. Michalopoulos,et al.  Liver Regeneration , 1997, Science.

[39]  S. Kitamura,et al.  Transplantation of genetically marked cardiac muscle cells. , 1997, The Journal of thoracic and cardiovascular surgery.

[40]  M. Soonpaa,et al.  Assessment of cardiomyocyte DNA synthesis in normal and injured adult mouse hearts. , 1997, The American journal of physiology.

[41]  R. P. Thompson,et al.  Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. , 1997, Circulation research.

[42]  Kyu-Ho Lee,et al.  A new tinman-related gene, nkx2.7, anticipates the expression of nkx2.5 and nkx2.3 in zebrafish heart and pharyngeal endoderm. , 1996, Developmental biology.

[43]  Stephen S. Gisselbrecht,et al.  heartless encodes a fibroblast growth factor receptor (DFR1/DFGF-R2) involved in the directional migration of early mesodermal cells in the Drosophila embryo. , 1996, Genes & development.

[44]  J. A. Bowers,et al.  Carvedilol inhibits clinical progression in patients with mild symptoms of heart failure. US Carvedilol Heart Failure Study Group. , 1996, Circulation.

[45]  P. Sanberg,et al.  Testis-derived Sertoli cells survive and provide localized immunoprotection for xenografts in rat brain , 1996, Nature Biotechnology.

[46]  M. Fishman,et al.  Zebrafish tinman homolog demarcates the heart field and initiates myocardial differentiation. , 1996, Development.

[47]  S M Schwartz,et al.  Skeletal myoblast transplantation for repair of myocardial necrosis. , 1996, The Journal of clinical investigation.

[48]  B. Byrne,et al.  Gene delivery to skeletal muscle results in sustained expression and systemic delivery of a therapeutic protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[49]  S M Schwartz,et al.  Muscle differentiation during repair of myocardial necrosis in rats via gene transfer with MyoD. , 1996, The Journal of clinical investigation.

[50]  M. Franklin,et al.  Cardiomyocyte DNA synthesis and binucleation during murine development. , 1996, The American journal of physiology.

[51]  R. Schwartz,et al.  Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription , 1996, Molecular and cellular biology.

[52]  L. Kedes,et al.  Transplantation of fetal myocardial tissue into the infarcted myocardium of rat. A potential method for repair of infarcted myocardium? , 1996, Circulation.

[53]  M. Abdellatif,et al.  Human E2F-1 reactivates cell cycle progression in ventricular myocytes and represses cardiac gene transcription. , 1996, Developmental biology.

[54]  P. Krieg,et al.  Overexpression of the tinman-related genes XNkx-2.5 and XNkx-2.3 in Xenopus embryos results in myocardial hyperplasia. , 1996, Development.

[55]  X. Zhu,et al.  Combined BMP-2 and FGF-4, but neither factor alone, induces cardiogenesis in non-precardiac embryonic mesoderm. , 1996, Developmental biology.

[56]  R. Weisel,et al.  Cardiomyocyte transplantation improves heart function. , 1996, The Annals of thoracic surgery.

[57]  T. Mikawa,et al.  The fate diversity of mesodermal cells within the heart field during chicken early embryogenesis. , 1996, Developmental biology.

[58]  G. Koh,et al.  Genetically selected cardiomyocytes from differentiating embronic stem cells form stable intracardiac grafts. , 1996, The Journal of clinical investigation.

[59]  J. Cohn,et al.  The effect of carvedilol on morbidity and mortality in patients with chronic heart failure. U.S. Carvedilol Heart Failure Study Group. , 1996, The New England journal of medicine.

[60]  D. Srivastava,et al.  Molecular Pathways Controlling Heart Development , 1996, Science.

[61]  H. E. Young,et al.  A population of cells isolated from rat heart capable of differentiating into several mesodermal phenotypes. , 1996, The Journal of surgical research.

[62]  H. E. Young,et al.  Effect of rat mesenchymal stem cells on development of abdominal adhesions after surgery. , 1996, The Journal of surgical research.

[63]  H. Arnold,et al.  Chick NKx-2.3 represents a novel family member of vertebrate homologues to the Drosophila homeo☐ gene tinman: differential expression of cNKx-2.3 and cNKx-2.5 during heart and gut development , 1996, Mechanisms of Development.

[64]  Y. Jiang,et al.  The Xenopus GATA-4/5/6 genes are associated with cardiac specification and can regulate cardiac-specific transcription during embryogenesis. , 1996, Developmental biology.

[65]  L. Leinwand,et al.  Cardiomyopathy in transgenic myf5 mice. , 1996, Circulation research.

[66]  C. Eisenberg,et al.  Establishment of the mesodermal cell line QCE-6. A model system for cardiac cell differentiation. , 1996, Circulation research.

[67]  K. Shiota,et al.  Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[68]  R. Hruban,et al.  Arterial delivery of genetically labelled skeletal myoblasts to the murine heart: long-term survival and phenotypic modification of implanted myoblasts. , 1996, Cell transplantation.

[69]  B. Wold,et al.  Evidence for Developmentally Programmed Transdifferentiation in Mouse Esophageal Muscle , 1995, Science.

[70]  H. Blau,et al.  Muscle-mediated gene therapy. , 1995, The New England journal of medicine.

[71]  A. Caplan,et al.  Myogenic cells derived from rat bone marrow mesenchymal stem cells exposed to 5‐azacytidine , 1995, Muscle & nerve.

[72]  A. Caplan,et al.  Myogenic Expression of Mesenchymal Stem Cells within Myotubes of mdx Mice in Vitro and in Vivo. , 1995, Tissue engineering.

[73]  Kuo-Fen Lee,et al.  Requirement for neuregulin receptor erbB2 in neural and cardiac development , 1995, Nature.

[74]  Rüdiger Klein,et al.  Aberrant neural and cardiac development in mice lacking the ErbB4 neuregulin receptor , 1995, Nature.

[75]  D. Smith,et al.  Myoblast transplantation in the porcine model: a potential technique for myocardial repair. , 1995, The Journal of thoracic and cardiovascular surgery.

[76]  N. Papalopulu,et al.  tinman, a Drosophila homeobox gene required for heart and visceral mesoderm specification, may be represented by a family of genes in vertebrates: XNkx-2.3, a second vertebrate homologue of tinman. , 1995, Development.

[77]  B. Spiegelman,et al.  Transdifferentiation of myoblasts by the adipogenic transcription factors PPAR gamma and C/EBP alpha. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[78]  D. Zipes,et al.  Stable fetal cardiomyocyte grafts in the hearts of dystrophic mice and dogs. , 1995, The Journal of clinical investigation.

[79]  A J Harris,et al.  Myogenic conversion of mammalian fibroblasts induced by differentiating muscle cells. , 1995, Journal of cell science.

[80]  A. Fulton,et al.  Transdifferentiation of chicken embryonic cells into muscle cells by the 3' untranslated region of muscle tropomyosin. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[81]  R. C. Chiu,et al.  Cellular cardiomyoplasty: myocardial regeneration with satellite cell implantation. , 1995, The Annals of thoracic surgery.

[82]  Ruili Li,et al.  Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. , 1995, Genes & development.

[83]  O. Bagasra,et al.  Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[84]  H. Halperin,et al.  Reverse remodeling from cardiomyoplasty in human heart failure. External constraint versus active assist. , 1995, Circulation.

[85]  A. Wechsler,et al.  Transcriptional regulation of phospholamban gene and translational regulation of SERCA2 gene produces coordinate expression of these two sarcoplasmic reticulum proteins during skeletal muscle phenotype switching , 1995, The Journal of Biological Chemistry.

[86]  F. Lund-Johansen,et al.  The "common stem cell" hypothesis reevaluated: human fetal bone marrow contains separate populations of hematopoietic and stromal progenitors. , 1995, Blood.

[87]  L. Kirshenbaum,et al.  Adenovirus E1A Represses Cardiac Gene Transcription and Reactivates DNA Synthesis in Ventricular Myocytes, via Alternative Pocket Protein- and p300-binding Domains (*) , 1995, The Journal of Biological Chemistry.

[88]  G. Koh,et al.  Potential Approaches for Myocardial Regeneration a , 1995, Annals of the New York Academy of Sciences.

[89]  J. Smith,et al.  Mesenchymal stem cells reside within the connective tissues of many organs , 1995, Developmental dynamics : an official publication of the American Association of Anatomists.

[90]  C. Eisenberg,et al.  QCE-6: a clonal cell line with cardiac myogenic and endothelial cell potentials. , 1995, Developmental biology.

[91]  R. Kao,et al.  Myocardial regeneration. Transplanting satellite cells into damaged myocardium. , 1995, Texas Heart Institute journal.

[92]  G. Koh,et al.  Targeted expression of transforming growth factor-beta 1 in intracardiac grafts promotes vascular endothelial cell DNA synthesis. , 1995, The Journal of clinical investigation.

[93]  B. Nadal-Ginard,et al.  Activation of the myogenic lineage by MEF2A, a factor that induces and cooperates with MyoD. , 1994, Science.

[94]  S. Bruder,et al.  Mesenchymal stem cells in bone development, bone repair, and skeletal regenaration therapy , 1994 .

[95]  Philippe Soriano,et al.  Transcriptional enhancer factor 1 disruption by a retroviral gene trap leads to heart defects and embryonic lethality in mice. , 1994, Genes & development.

[96]  W. Gu,et al.  Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. , 1994, Science.

[97]  K. Chien,et al.  Heterokaryons of cardiac myocytes and fibroblasts reveal the lack of dominance of the cardiac muscle phenotype , 1994, Molecular and cellular biology.

[98]  J. Brockes.  New approaches to amphibian limb regeneration. , 1994, Trends in genetics : TIG.

[99]  G. Koh,et al.  Formation of nascent intercalated disks between grafted fetal cardiomyocytes and host myocardium. , 1994, Science.

[100]  M. Soonpaa,et al.  Assessment of cardiomyocyte DNA synthesis during hypertrophy in adult mice. , 1994, The American journal of physiology.

[101]  M. Arbonés,et al.  Gene targeting in normal somatic cells: inactivation of the interferon–γ receptor in myoblasts , 1994, Nature Genetics.

[102]  G. Gross,et al.  Expression of human bone morphogenetic proteins-2 or -4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. , 1993, DNA and cell biology.

[103]  L Hartley,et al.  Authors' correction: Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants , 1993 .

[104]  L Hartley,et al.  Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. , 1993, Development.

[105]  G. Koh,et al.  Differentiation and long-term survival of C2C12 myoblast grafts in heart. , 1993, The Journal of clinical investigation.

[106]  T. N. James,et al.  Electron microscopic demonstration of intercellular junctions between subendocardial smooth muscle and myocardium in the sheep heart. , 1993, American heart journal.

[107]  M. Frasch,et al.  tinman and bagpipe: two homeo box genes that determine cell fates in the dorsal mesoderm of Drosophila. , 1993, Genes & development.

[108]  G. Koh,et al.  Long-term survival of AT-1 cardiomyocyte grafts in syngeneic myocardium. , 1993, The American journal of physiology.

[109]  Jon A. Wolff,et al.  Long-term correction of rat model of Parkinson's disease by gene therapy , 1993, Nature.

[110]  C. Naus,et al.  Expression of gap junctions in cultured rat L6 cells during myogenesis. , 1993, Developmental biology.

[111]  J C Stanley,et al.  Adhesion and incorporation of lacZ-transduced endothelial cells into the intact capillary wall in the rat. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[112]  A. Neumeyer,et al.  Arterial delivery of myoblasts to skeletal muscle , 1992, Neurology.

[113]  V. Stewart,et al.  Embryonic lethality in mice homozygous for a targeted disruption of the N-myc gene. , 1992, Genes & development.

[114]  E. Ralston,et al.  Restricted distribution of mRNA produced from a single nucleus in hybrid myotubes , 1992, The Journal of cell biology.

[115]  R. C. Chiu,et al.  Cell Transplantation for Myocardial Repair: An Experimental Approach , 1992, Cell transplantation.

[116]  B. Wold,et al.  Skeletal muscle phenotypes initiated by ectopic MyoD in transgenic mouse heart. , 1992, Development.

[117]  J. Leiden,et al.  Systemic delivery of recombinant proteins by genetically modified myoblasts. , 1991, Science.

[118]  H. Blau,et al.  Systemic delivery of human growth hormone by injection of genetically engineered myoblasts. , 1991, Science.

[119]  E. Marbán,et al.  L-type calcium channels, potassium channels, and novel nonspecific cation channels in a clonal muscle cell line derived from embryonic rat ventricle. , 1991, Circulation research.

[120]  W. Claycomb,et al.  Morphological characterization of cardiomyocytes isolated from a transplantable cardiac tumor derived from transgenic mouse atria (AT-1 cells). , 1991, Circulation research.

[121]  K. Verbanac,et al.  The veto mechanism in transplant tolerance , 1991 .

[122]  A. Caplan.  Mesenchymal stem cells , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[123]  F. Tristani,et al.  A comparison of enalapril with hydralazine-isosorbide dinitrate in the treatment of chronic congestive heart failure. , 1991, The New England journal of medicine.

[124]  W. Claycomb,et al.  Proliferation in vivo and in culture of differentiated adult atrial cardiomyocytes from transgenic mice. , 1990, The American journal of physiology.

[125]  Manoel Luis Costa,et al.  MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[126]  K. Campbell,et al.  Ca‐ATPase isozyme expression in sarcoplasmic reticulum is altered by chronic stimulation of skeletal muscle , 1990, FEBS letters.

[127]  K. Beam,et al.  Restoration of normal function in genetically defective myotubes by spontaneous fusion with fibroblasts , 1989, Nature.

[128]  C. Brandl,et al.  Slow/cardiac sarcoplasmic reticulum Ca2+-ATPase and phospholamban mRNAs are expressed in chronically stimulated rabbit fast-twitch muscle. , 1989, European journal of biochemistry.

[129]  S. Tapscott,et al.  5-bromo-2'-deoxyuridine blocks myogenesis by extinguishing expression of MyoD1. , 1989, Science.

[130]  S. Tapscott,et al.  Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[131]  E. Ralston,et al.  Transfer of a protein encoded by a single nucleus to nearby nuclei in multinucleated myotubes. , 1989, Science.

[132]  D. Paul,et al.  Antisera directed against connexin43 peptides react with a 43-kD protein localized to gap junctions in myocardium and other tissues , 1989, The Journal of cell biology.

[133]  R. Palmiter,et al.  Heart and bone tumors in transgenic mice. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[134]  L. Field,et al.  Atrial natriuretic factor-SV40 T antigen transgenes produce tumors and cardiac arrhythmias in mice. , 1988, Science.

[135]  L. Weiss.  Biomechanical destruction of cancer cells in the heart: a rate regulator for hematogenous metastasis. , 1988, Invasion & metastasis.

[136]  H. Weintraub,et al.  Expression of a single transfected cDNA converts fibroblasts to myoblasts , 1987, Cell.

[137]  J. Brockes.  The nerve dependence of amphibian limb regeneration. , 1987, The Journal of experimental biology.

[138]  S. Gottlieb,et al.  Role of neurohormonal mechanisms in determining survival in patients with severe chronic heart failure. , 1987, Circulation.

[139]  S Salmons,et al.  Skeletal muscle as the potential power source for a cardiovascular pump: assessment in vivo. , 1987, Science.

[140]  Harold Weintraub,et al.  Transfection of a DNA locus that mediates the conversion of 10T1 2 fibroblasts to myoblasts , 1986, Cell.

[141]  M. Grounds,et al.  Cell proliferation in denervated skeletal muscle: does it provide a pool of potential circulating myoblasts? , 1986, Bibliotheca anatomica.

[142]  D. Dimitrov,et al.  The hemodynamic destruction of intravascular cancer cells in relation to myocardial metastasis. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[143]  H. Blau,et al.  Isolation and characterization of human muscle cells. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[144]  F. Jolesz,et al.  Development, innervation, and activity-pattern induced changes in skeletal muscle. , 1981, Annual review of physiology.

[145]  Peter A. Jones,et al.  Cellular differentiation, cytidine analogs and DNA methylation , 1980, Cell.

[146]  Peter A. Jones,et al.  Multiple new phenotypes induced in 10T 1 2 and 3T3 cells treated with 5-azacytidine , 1979, Cell.

[147]  D. Bader,et al.  Autoradiographic and electron microscopic studies of minced cardiac muscle regeneration in the adult newt, notophthalmus viridescens. , 1979, The Journal of experimental zoology.

[148]  D. Yaffe,et al.  Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle , 1977, Nature.

[149]  N. Gilula,et al.  Cell-to-cell communication and myogenesis , 1977, The Journal of cell biology.

[150]  S. Chacko,et al.  The effect of 5-bromodeoxyuridine (BrdU) on cardiac muscle differentiation. , 1974, Developmental biology.

[151]  J. Oberpriller,et al.  Response of the adult newt ventricle to injury. , 1974, The Journal of experimental zoology.

[152]  J. Rash,et al.  Freeze-cleave demonstration of gap junctions between skeletal myogenic cells in vivo. , 1974, Developmental biology.

[153]  J. Rash,et al.  Ultrastructural and electrophysiological correlates of cell coupling and cytoplasmic fusion during myogenesis in vitro. , 1973, Developmental biology.

[154]  H. Weintraub,et al.  Identification of a developmental program using bromodeoxyuridine. , 1972, Journal of molecular biology.

[155]  H. Holtzer,et al.  INHIBITION OF MYOBLAST FUSION AFTER ONE ROUND OF DNA SYNTHESIS IN 5-BROMODEOXYURIDINE , 1970, The Journal of cell biology.

[156]  K. Okazaki,et al.  5-Bromodeoxyuridine: Effect on Myogenesis in vitro , 1964, Science.

[157]  A. Mauro.  SATELLITE CELL OF SKELETAL MUSCLE FIBERS , 1961, The Journal of biophysical and biochemical cytology.

[158]  M. E. Rawles.  The Heart-Forming Areas of the Early Chick Blastoderm , 1943, Physiological Zoology.