Heart development in Drosophila and vertebrates: conservation of molecular mechanisms.

Vertebrate and insect (Drosophila) hearts look and function quite differently from each other. Nevertheless, during embryogenesis their mesodermal origin and initial assembly into a linear heart tube are comparable in many respects. In the past few years, numerous gene functions have been identified that are utilized by both vertebrates and Drosophila for the specification and differentiation of the heart progenitor cells. These studies have begun with the discovery of the homeobox gene tinman in Drosophila and its vertebrate counterparts. By now, there is also evidence that MEF2 transcription factors and TGF-beta signaling have cardiogenic functions in both these systems. Perhaps in a few years, the GATA and HAND transcription factors and Wnt signaling, which currently only have a demonstrated cardiogenic function in one of the systems, may also be part of this group. One of the pressing but still wide open questions is if the spectrum of targets for these transcription factors and signaling pathways is also conserved.

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

[2]  H. Yost Vertebrate left-right development , 1995, Cell.

[3]  Stephen S. Gisselbrecht,et al.  Dual functions of the heartless fibroblast growth factor receptor in development of the Drosophila embryonic mesoderm. , 1998, Developmental genetics.

[4]  S. Cohen,et al.  Specification of the wing by localized expression of wingless protein , 1996, Nature.

[5]  I. Komuro,et al.  Csx: a murine homeobox-containing gene specifically expressed in the developing heart. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Y. Saijoh,et al.  Left–right asymmetric expression of the TGFβ-family member lefty in mouse embryos , 1996, Nature.

[7]  M. Frasch,et al.  Regulation and function of tinman during dorsal mesoderm induction and heart specification in Drosophila. , 1998, Developmental genetics.

[8]  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.

[9]  Michael Bate,et al.  dpp induces mesodermal gene expression in Drosophila , 1994, Nature.

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

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

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

[13]  R A Schulz,et al.  Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila , 1995, Science.

[14]  C. Nüsslein-Volhard,et al.  The origin of pattern and polarity in the Drosophila embryo , 1992, Cell.

[15]  C. Mueller,et al.  GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. , 1994, The Journal of biological chemistry.

[16]  R. Krumlauf Hox genes in vertebrate development , 1994, Cell.

[17]  G. Eichele,et al.  Chicken Nkx-2.8: a novel homeobox gene expressed in early heart progenitor cells and pharyngeal pouch-2 and -3 endoderm. , 1997, Developmental biology.

[18]  M. Scott Intimations of a creature , 1994, Cell.

[19]  J. Emery,et al.  Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene. , 1994, Genes & development.

[20]  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.

[21]  H. Yost,et al.  Initiation of vertebrate left–right axis formation by maternal Vg1 , 1996, Nature.

[22]  A. Lassar,et al.  Induction of avian cardiac myogenesis by anterior endoderm. , 1995, Development.

[23]  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.

[24]  R. Harvey NK-2 homeobox genes and heart development. , 1996, Developmental biology.

[25]  R. Schulz,et al.  Regulation of muscle differentiation by the MEF2 family of MADS box transcription factors. , 1995, Developmental biology.

[26]  Y. Sasai,et al.  A common plan for dorsoventral patterning in Bilateria , 1996, Nature.

[27]  M. Fishman,et al.  Patterning the heart's left-right axis: from zebrafish to man. , 1998, Developmental genetics.

[28]  R A Schulz,et al.  D‐mef2 is a target for Tinman activation during Drosophila heart development , 1997, The EMBO journal.

[29]  E. Bier,et al.  Xenopus chordin and Drosophila short gastrulation genes encode homologous proteins functioning in dorsal-ventral axis formation , 1995, Cell.

[30]  M. Simon,et al.  Gotta have GATA , 1995, Nature Genetics.

[31]  R. Bodmer,et al.  Heart development in Drosophila requires the segment polarity gene wingless. , 1995, Developmental biology.

[32]  M. Nemer,et al.  Enhanced cardiogenesis in embryonic stem cells overexpressing the GATA-4 transcription factor. , 1997, Development.

[33]  D. Srivastava,et al.  Regulation of cardiac mesodermal and neural crest development by the bHLH transcription factor, dHAND , 1997, Nature Genetics.

[34]  A. Schier,et al.  A genetic screen for mutations affecting embryogenesis in zebrafish. , 1996, Development.

[35]  R. Bodmer,et al.  Heart development in Drosophila and its relationship to vertebrates. , 1995, Trends in cardiovascular medicine.

[36]  G. Lyons,et al.  Vertebrate homologs of tinman and bagpipe: roles of the homeobox genes in cardiovascular development. , 1998, Developmental genetics.

[37]  M. Levin Left‐right asymmetry in vertebrate embryogenesis , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

[38]  J. Cooke,et al.  Control of Vertebrate Left-Right Asymmetry by a Snail-Related Zinc Finger Gene , 1997, Science.

[39]  M. Nemer,et al.  Inhibition of transcription factor GATA-4 expression blocks in vitro cardiac muscle differentiation , 1995, Molecular and cellular biology.

[40]  R. Bodmer The gene tinman is required for specification of the heart and visceral muscles in Drosophila. , 1993, Development.

[41]  T. Evans,et al.  Regulation of Cardiac Gene Expression by GATA-4/5/6. , 1997, Trends in cardiovascular medicine.

[42]  D. Stainier,et al.  Screening mosaic F1 females for mutations affecting zebrafish heart induction and patterning. , 1998, Developmental genetics.

[43]  R. Bodmer,et al.  How many signals does it take? , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[44]  Y. Jan,et al.  A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. , 1990, Development.

[45]  Hanh T. Nguyen,et al.  Drosophila MEF2, a transcription factor that is essential for myogenesis. , 1995, Genes & development.

[46]  D. Wilson,et al.  Localization of transcription factor GATA-4 to regions of the mouse embryo involved in cardiac development. , 1994, Developmental biology.

[47]  R. Bodmer,et al.  Dual role for the zeste-white3/shaggy-encoded kinase in mesoderm and heart development of Drosophila. , 1998, Developmental genetics.

[48]  M. Fishman,et al.  Parsing the Heart: Genetic Modules for Organ Assembly , 1997, Cell.

[49]  C. Tabin,et al.  A molecular pathway determining left-right asymmetry in chick embryogenesis , 1995, Cell.

[50]  P. Krieg,et al.  tinman-related genes expressed during heart development in Xenopus. , 1998, Developmental genetics.

[51]  Y. Jiang,et al.  Common role for each of the cGATA-4/5/6 genes in the regulation of cardiac morphogenesis. , 1998, Developmental genetics.

[52]  D. Srivastava,et al.  A Subclass of bHLH Proteins Required for Cardiac Morphogenesis , 1995, Science.

[53]  M. Frasch,et al.  Induction of visceral and cardiac mesoderm by ectodermal Dpp in the early Drosophila embryo , 1995, Nature.

[54]  M. Frasch,et al.  Genetic Determination of Drosophila Heart Development , 1999 .

[55]  M. Fishman,et al.  The zebrafish as a model system to study cardiovascular development. , 1994, Trends in cardiovascular medicine.

[56]  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.

[57]  D A Kane,et al.  The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. , 1996, Development.

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

[59]  H. Robert Horvitz 6 Genetics of Cell Lineage , 1988 .

[60]  D. Supp,et al.  Conserved left–right asymmetry of nodal expression and alterations in murine situs inversus , 1996, Nature.

[61]  L Hartley,et al.  Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. , 1995, Genes & Development.

[62]  C. Biben,et al.  Homeodomain factor Nkx2-5 controls left/right asymmetric expression of bHLH gene eHand during murine heart development. , 1997, Genes & development.

[63]  C. Bucana,et al.  Control of mouse cardiac morphogenesis and myogenesis by transcription factor MEF2C. , 1997, Science.

[64]  D. Durocher,et al.  Combinatorial interactions regulating cardiac transcription. , 1998, Developmental genetics.

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

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

[67]  Y. Zou,et al.  CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. , 1997, Development.

[68]  J. Axelrod,et al.  The wingless signaling pathway is directly involved in Drosophila heart development. , 1996, Developmental biology.