Expression of Cnox-2, a HOM/HOX homeobox gene in hydra, is correlated with axial pattern formation.

Cnox-2 is a HOM/HOX homeobox gene that we have identified in the simple metazoan Hydra vulgaris (Cnidaria: Hydrozoa). Cnox-2 is most closely related to anterior members of the Antennapedia gene complex from Drosophila, with the greatest similarity to Deformed. The Cnox-2 protein is expressed in the epithelial cells of adult hydra polyps in a region-specific pattern along the body axis, at a low level in the head and at a high level in the body column and the foot. The expression pattern of Cnox-2 is consistent with a role in axial pattern formation. Alteration of hydra axial patterning by treatment with diacylglycerol (DAG) results in an increase of head activation down the body column and in a coordinate reduction of Cnox-2 expression in epithelial cells in 'head-like' regions. These results suggest that Cnox-2 expression is negatively regulated by a signaling pathway acting through protein kinase C (PKC), and that the varying levels of expression of Cnox-2 along the body axis have the potential to result in differential gene expression which is important for hydra pattern formation.

[1]  H. Macwilliams.  Hydra transplantation phenomena and the mechanism of Hydra head regeneration. II. Properties of the head activation. , 1983, Developmental biology.

[2]  T Sugiyama,et al.  Genetic analysis of developmental mechanisms in hydra. XII. Analysis of chimaeric hydra produced from a normal and a slow-budding strain (L4). , 1984, Journal of embryology and experimental morphology.

[3]  A. Feinberg,et al.  A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. , 1983, Analytical biochemistry.

[4]  H. Bode,et al.  Nucleotide sequence of an actin-encoding gene from Hydra attenuata: structural characteristics and evolutionary implications. , 1989, Gene.

[5]  L. Björck,et al.  Purification and some properties of streptococcal protein G, a novel IgG-binding reagent. , 1984, Journal of immunology.

[6]  M. Scott,et al.  The structure and function of the homeodomain. , 1989, Biochimica et biophysica acta.

[7]  W. Gehring,et al.  Quox-1, a quail homeobox gene expressed in the embryonic central nervous system, including the forebrain. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[8]  P. Lemotte,et al.  The homeotic gene Sex Combs Reduced of Drosophila: gene structure and embryonic expression. , 1989, The EMBO journal.

[9]  P. Gruss,et al.  Primary structure and nuclear localization of a murine homeodomain protein. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[10]  T. Sugiyama,et al.  Genetic analysis of developmental mechanisms in hydra: XIV. Identification of the cell lineages responsible for the altered developmental gradients in a mutant strain, reg-16 , 1986 .

[11]  T. Bosch,et al.  Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata. , 1989, Molecular and cellular biology.

[12]  M. Vigneron,et al.  The mouse Hox-1.4 gene: primary structure, evidence for promoter activity and expression during development. , 1989, Development.

[13]  P. Holland,et al.  Expression of homeo box genes during mouse development: a review. , 1988, Genes & development.

[14]  R. Krumlauf,et al.  Characterization of a murine homeo box gene, Hox-2.6, related to the Drosophila Deformed gene. , 1988, Genes & development.

[15]  W. Gehring,et al.  Structural organization and sequence of the homeotic gene Antennapedia of Drosophila melanogaster. , 1986, The EMBO journal.

[16]  W. Müller.  Diacylglycerol-induced multihead formation in Hydra , 1989 .

[17]  G. Ruvkun,et al.  Nematode homeobox cluster , 1991, Nature.

[18]  C. Kenyon,et al.  Activation of a C. elegans Antennapedia homologue in migrating cells controls their direction of migration , 1992, Nature.

[19]  R. Krumlauf,et al.  Developmental and spatial patterns of expression of the mouse homeobox gene, Hox 2.1. , 1987, Development.

[20]  T. Fujisawa,et al.  Genetic analysis of developmental mechanisms in Hydra. II. Isolation and characterization of an interstitial cell-deficient strain. , 1978, Journal of cell science.

[21]  C. Tyler-Smith,et al.  Structure of repeated sequences in the centromeric region of the human Y chromosome. , 1987, Development.

[22]  H. Bode,et al.  Plasticity in the nervous system of adult hydra. I. The position-dependent expression of FMRFamide-like immunoreactivity. , 1986, Developmental biology.

[23]  B. Maden,et al.  Nucleotide sequence of Xenopus laevis 18S ribosomal RNA inferred from gene sequence , 1981, Nature.

[24]  R. D. Campbell.  Tissue dynamics of steady state growth in Hydra littoralis. II. Patterns of tissue movement , 1967, Journal of morphology.

[25]  C. Kenyon,et al.  A cluster of Antennapedia-class homeobox genes in a nonsegmented animal. , 1991, Science.

[26]  F. Studier,et al.  Use of T7 RNA polymerase to direct expression of cloned genes. , 1990, Methods in enzymology.

[27]  J. Engel,et al.  Mini-collagens in hydra nematocytes , 1991, The Journal of cell biology.

[28]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[29]  C. Tabin,et al.  Embryonic expression and nuclear localization of Xenopus homeobox (Xhox) gene products. , 1986, The EMBO journal.

[30]  D. Hartl,et al.  27 – AMPLIFICATION OF FLANKING SEQUENCES BY INVERSE PCR , 1989 .

[31]  G. Blobel,et al.  Immunoprecipitation of proteins from cell-free translations. , 1983, Methods in enzymology.

[32]  H. Bode,et al.  Both the epithelial cells and the nerve cells are involved in the head inhibition properties in Hydra attenuata. , 1982, Developmental biology.

[33]  C. Jenkin,et al.  Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-sepharose. , 1978, Immunochemistry.

[34]  O K Wilby,et al.  Experimental studies on axial polarity in hydra. , 1970, Journal of embryology and experimental morphology.

[35]  B. Schierwater,et al.  Homeoboxes in cnidarians. , 1991, The Journal of experimental zoology.

[36]  F. Palmer-Hill,et al.  Expression of a homeo domain protein in noncontact-inhibited cultured cells and postmitotic neurons. , 1987, Genes & development.

[37]  R. Harland,et al.  Posterior expression of a homeobox gene in early Xenopus embryos. , 1987, Development.

[38]  R. W. Davis,et al.  Rapid DNA isolations for enzymatic and hybridization analysis. , 1980, Methods in enzymology.

[39]  L. Björck,et al.  A physicochemical study of protein G, a molecule with unique immunoglobulin G-binding properties. , 1986, The Journal of biological chemistry.

[40]  M. Schummer,et al.  HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration. , 1992, The EMBO journal.

[41]  W. McGinnis,et al.  Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development , 1987, The EMBO journal.

[42]  M. Akam.  Hox and HOM: Homologous gene clusters in insects and vertebrates , 1989, Cell.

[43]  H. Schaller,et al.  A 33 kDa protein with sequence homology to the 'laminin binding protein' is associated with the cytoskeleton in hydra and in mammalian cells. , 1991, Journal of cell science.

[44]  R. D. Campbell,et al.  Tissue dynamics of steady state growth in Hydra littoralis. I. Patterns of cell division. , 1967, Developmental biology.

[45]  F. Ruddle,et al.  Detection of homeobox genes in development and evolution. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Gruss,et al.  Murine developmental control genes. , 1990, Science.

[47]  S. Bryant,et al.  Pattern Formation: A Primer in Developmental Biology , 1984 .

[48]  T. Kaufman,et al.  Structural complexity and evolutionary conservation of the Drosophila homeotic gene proboscipedia. , 1992, The EMBO journal.

[49]  H. Bode,et al.  Development of the two-part pattern during regeneration of the head in hydra. , 1988, Development.

[50]  H. Lehrach,et al.  Coding sequence and expression of the homeobox gene Hox 1.3. , 1988, Development.

[51]  William McGinnis,et al.  Homeobox genes and axial patterning , 1992, Cell.

[52]  J. Takano,et al.  Genetic analysis of developmental mechanisms in hydra. VIII. Head-activation and head-inhibition potentials of a slow-budding strain (L4). , 1983, Journal of embryology and experimental morphology.

[53]  R. Gourse,et al.  Sequence analysis of 28S ribosomal DNA from the amphibian Xenopus laevis. , 1983, Nucleic acids research.