Expression of the helix‐loop‐helix gene Id3 during murine embryonic development

The family of dominant‐negative helix‐loop‐helix (dnHLH) transcriptional modulators consists of four mammalian genes known to date: Id1, Id2, Id3 (Id3 was formerly designated HLH462 or HEIR1 or HLH1R21), and Id4. We have performed a detailed study of Id3 expression in mouse embryos in order to gain insight into the possible developmental control functions of this gene and to compare its expression to that of other mammalian dnHLH genes. Employing RNA in situ hybridization on sectioned mouse embryos of gestational stages E9.5–17.5 and neonatal head, we generally detected a high abundance of transcripts at early stages that gradually declined at most sites toward E15.5. Expression of Id3 in embryos was detected in brain, spinal cord, olfactory system, branchial arches, limbs, sclerotome, endocardiac cushions, the outer lining of the gut, lung, retina, the collecting system of the kidney, and in tooth anlagen. Although the abundance of mRNA decreased toward later stages in most tissues, it remained high in teeth and kidney. This expression pattern suggests that Id3 functions both in undifferentiated tissues and in organs which are in the process of differentiation. When compared to the expression of other dnHLH genes, it becomes obvious that the pattern of Id3 mainly coincides with that of Id1. This may reflect a partial redundancy in gene function. Furthermore, previous experiments suggested a mutually exclusive expression of the proto‐oncogene N‐myc an Id3. The results of the present study confirm these data. ©1995 Wiley‐Liss, Inc.

[1]  R. Pepperkok,et al.  Regulation of G1 progression by E2A and Id helix‐loop‐helix proteins. , 1994, The EMBO journal.

[2]  F. Sablitzky,et al.  The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. , 1994, Nucleic acids research.

[3]  R. Benezra,et al.  The loop region of the helix-loop-helix protein Id1 is critical for its dominant negative activity , 1993, Molecular and cellular biology.

[4]  C. Emerson Embryonic signals for skeletal myogenesis: arriving at the beginning. , 1993, Current opinion in cell biology.

[5]  David J. Anderson,et al.  Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons , 1993, Cell.

[6]  P. Gruss,et al.  Neuronal expression of regulatory helix-loop-helix factor Id2 gene in mouse. , 1993, Developmental biology.

[7]  S. Evans,et al.  Expression of the helix-loop-helix factor Id during mouse embryonic development. , 1993, Developmental biology.

[8]  M. Santibanez-Koref,et al.  An immediate early human gene encodes an Id-like helix-loop-helix protein and is regulated by protein kinase C activation in diverse cell types. , 1993, Oncogene.

[9]  E. Olson,et al.  Helix-loop-helix proteins as regulators of muscle-specific transcription. , 1993, The Journal of biological chemistry.

[10]  K. Chada,et al.  The gene for the helix-loop-helix protein, Id, is specifically expressed in neural precursors. , 1992, Developmental biology.

[11]  H. Weintraub,et al.  Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. , 1992, Genes & development.

[12]  A. Aguzzi,et al.  Mutually exclusive expression of a helix‐loop‐helix gene and N‐myc in human neuroblastomas and in normal development. , 1992, The EMBO journal.

[13]  R. Benezra,et al.  Id expression during mouse development: A role in morphogenesis , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[14]  A. Aguzzi,et al.  Dominant and Recessive Molecular Changes in Neuroblastomas , 1992, Brain pathology.

[15]  R. Benezra,et al.  Inhibition of myeloid differentiation by the helix-loop-helix protein Id. , 1992, Science.

[16]  R. Kingston,et al.  HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors , 1992, Molecular and cellular biology.

[17]  M. Israel,et al.  A human Id-like helix-loop-helix protein expressed during early development. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[18]  D. Baltimore,et al.  Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins , 1991, Molecular and cellular biology.

[19]  T. Saito,et al.  Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. , 1991, Genes & development.

[20]  N. Copeland,et al.  An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  R. Stein,et al.  Pancreatic beta-cell-type-specific transcription of the insulin gene is mediated by basic helix-loop-helix DNA-binding proteins , 1991, Molecular and cellular biology.

[22]  P. Gerlinger,et al.  The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. , 1991, Developmental biology.

[23]  David J. Anderson,et al.  Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors , 1990, Nature.

[24]  W. Rutter,et al.  Pan: a transcriptional regulator that binds chymotrypsin, insulin, and AP-4 enhancer motifs. , 1990, Genes & development.

[25]  E. Wagner,et al.  Sympathetic hyperplasia and neuroblastomas in transgenic mice expressing polyoma middle T antigen. , 1990, The New biologist.

[26]  Harold Weintraub,et al.  The protein Id: A negative regulator of helix-loop-helix DNA binding proteins , 1990, Cell.

[27]  A. Aronheim,et al.  A cDNA from a mouse pancreatic beta cell encoding a putative transcription factor of the insulin gene. , 1990, Nucleic acids research.

[28]  T. Kadesch,et al.  Two distinct transcription factors that bind the immunoglobulin enhancer microE5/kappa 2 motif. , 1990, Science.

[29]  Y. Jan,et al.  Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence , 1989, Cell.

[30]  David Baltimore,et al.  A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins , 1989, Cell.

[31]  B. Jacq,et al.  Hox‐7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. , 1989, The EMBO journal.

[32]  F. Alt,et al.  N-myc proto-oncogene expression during organogenesis in the developing mouse as revealed by in situ hybridization , 1988, The Journal of cell biology.

[33]  A. Lumsden Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. , 1988, Development.

[34]  D. Noden Interactions and fates of avian craniofacial mesenchyme. , 1988, Development.

[35]  R. Keynes,et al.  Mechanisms of vertebrate segmentation. , 1988, Development.

[36]  F. Alt,et al.  Structure and expression of the murine N-myc gene. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[37]  A J Verbout,et al.  The development of the vertebral column. , 1985, Advances in anatomy, embryology, and cell biology.

[38]  G. Church,et al.  B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. , 1985, Science.

[39]  T. Kadesch,et al.  Consequences of heteromeric interactions among helix-loop-helix proteins. , 1993, Cell growth & differentiation : the molecular biology journal of the American Association for Cancer Research.

[40]  T. Kadesch Helix-loop-helix proteins in the regulation of immunoglobulin gene transcription. , 1992, Immunology today.

[41]  J. Bard,et al.  The development of the mouse kidney--embryogenesis writ small. , 1992, Current opinion in genetics & development.

[42]  Y. Jan,et al.  Genetic and molecular bases of neurogenesis in Drosophila melanogaster. , 1991, Annual review of neuroscience.

[43]  M. Justice,et al.  A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. , 1989, Genes & development.

[44]  R. Rugh,et al.  The mouse; its reproduction and development , 1968 .