Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 May;11(5):1815–1823. doi: 10.1002/j.1460-2075.1992.tb05233.x

HOM/HOX homeobox genes are present in hydra (Chlorohydra viridissima) and are differentially expressed during regeneration.

M Schummer 1, I Scheurlen 1, C Schaller 1, B Galliot 1
PMCID: PMC556639  PMID: 1374713

Abstract

Hydra, a diblastic animal consisting of two cell layers, ectoderm and endoderm, is one of the most ancient animals displaying an anteroposterior axis with a head and a foot developing from an uncommitted gastric region. As such, hydra is an interesting model for studying the presence and function of homeobox genes in a phylogenetically old organism. By screening a Chlorohydra viridissima cDNA library with a 'guessmer' oligonucleotide, we have cloned several such cnidarian homeobox-containing genes (cnox genes). Two of these, cnox1 and cnox2, display labial and Deformed type homeodomains respectively and could represent two ancestral genes of the HOM/HOX complexes; cnox3 exhibits some similarity to the BarH1 and the distal-less type homeodomains and a fourth gene is highly related to the msh/Hox7 type of homeodomain. We used quantitative PCR to study levels of expression of these genes along the body axis and during head regeneration. In all cases, the expression in heads was stronger than that in the gastric region. cnox1 transcripts dramatically peaked within the first hours of head regeneration, whereas cnox2 and cnox3 reached their maximal levels 1 and 2 days after cutting respectively. This differential expression of homeobox genes at various stages of regeneration suggests that they play specific roles in regenerative processes.

Full text

PDF
1815

Images in this article

1819Image
on p.1819
1819Image
on p.1819
1820Image
on p.1820
1821Image
on p.1821

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akam M. Hox and HOM: homologous gene clusters in insects and vertebrates. Cell. 1989 May 5;57(3):347–349. doi: 10.1016/0092-8674(89)90909-4. [DOI] [PubMed] [Google Scholar]
  2. Blin N., Stafford D. W. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res. 1976 Sep;3(9):2303–2308. doi: 10.1093/nar/3.9.2303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bodmer R., Jan L. Y., Jan Y. N. A new homeobox-containing gene, msh-2, is transiently expressed early during mesoderm formation of Drosophila. Development. 1990 Nov;110(3):661–669. doi: 10.1242/dev.110.3.661. [DOI] [PubMed] [Google Scholar]
  4. Bogarad L. D., Utset M. F., Awgulewitsch A., Miki T., Hart C. P., Ruddle F. H. The developmental expression pattern of a new murine homeo box gene: Hox-2.5. Dev Biol. 1989 Jun;133(2):537–549. doi: 10.1016/0012-1606(89)90056-0. [DOI] [PubMed] [Google Scholar]
  5. Boncinelli E., Simeone A., Acampora D., Mavilio F. HOX gene activation by retinoic acid. Trends Genet. 1991 Oct;7(10):329–334. doi: 10.1016/0168-9525(91)90423-n. [DOI] [PubMed] [Google Scholar]
  6. Bosch T. C., Unger T. F., Fisher D. A., Steele R. E. Structure and expression of STK, a src-related gene in the simple metazoan Hydra attenuata. Mol Cell Biol. 1989 Oct;9(10):4141–4151. doi: 10.1128/mcb.9.10.4141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bürglin T. R., Finney M., Coulson A., Ruvkun G. Caenorhabditis elegans has scores of homoeobox-containing genes. Nature. 1989 Sep 21;341(6239):239–243. doi: 10.1038/341239a0. [DOI] [PubMed] [Google Scholar]
  8. Bürglin T. R., Ruvkun G., Coulson A., Hawkins N. C., McGhee J. D., Schaller D., Wittmann C., Müller F., Waterston R. H. Nematode homeobox cluster. Nature. 1991 Jun 27;351(6329):703–703. doi: 10.1038/351703a0. [DOI] [PubMed] [Google Scholar]
  9. Chelly J., Montarras D., Pinset C., Berwald-Netter Y., Kaplan J. C., Kahn A. Quantitative estimation of minor mRNAs by cDNA-polymerase chain reaction. Application to dystrophin mRNA in cultured myogenic and brain cells. Eur J Biochem. 1990 Feb 14;187(3):691–698. doi: 10.1111/j.1432-1033.1990.tb15355.x. [DOI] [PubMed] [Google Scholar]
  10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
  11. Cohen S. M., Brönner G., Küttner F., Jürgens G., Jäckle H. Distal-less encodes a homoeodomain protein required for limb development in Drosophila. Nature. 1989 Mar 30;338(6214):432–434. doi: 10.1038/338432a0. [DOI] [PubMed] [Google Scholar]
  12. Dolecki G. J., Wannakrairoj S., Lum R., Wang G., Riley H. D., Carlos R., Wang A., Humphreys T. Stage-specific expression of a homeo box-containing gene in the non-segmented sea urchin embryo. EMBO J. 1986 May;5(5):925–930. doi: 10.1002/j.1460-2075.1986.tb04305.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Dollé P., Duboule D. Two gene members of the murine HOX-5 complex show regional and cell-type specific expression in developing limbs and gonads. EMBO J. 1989 May;8(5):1507–1515. doi: 10.1002/j.1460-2075.1989.tb03535.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Duboule D., Dollé P. The structural and functional organization of the murine HOX gene family resembles that of Drosophila homeotic genes. EMBO J. 1989 May;8(5):1497–1505. doi: 10.1002/j.1460-2075.1989.tb03534.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fainsod A., Greunbaum Y. A chicken homeo box gene with developmentally regulated expression. FEBS Lett. 1989 Jul 3;250(2):381–385. doi: 10.1016/0014-5793(89)80760-4. [DOI] [PubMed] [Google Scholar]
  16. Featherstone M. S., Baron A., Gaunt S. J., Mattei M. G., Duboule D. Hox-5.1 defines a homeobox-containing gene locus on mouse chromosome 2. Proc Natl Acad Sci U S A. 1988 Jul;85(13):4760–4764. doi: 10.1073/pnas.85.13.4760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fisher D. A., Bode H. R. Nucleotide sequence of an actin-encoding gene from Hydra attenuata: structural characteristics and evolutionary implications. Gene. 1989 Dec 7;84(1):55–64. doi: 10.1016/0378-1119(89)90139-x. [DOI] [PubMed] [Google Scholar]
  18. Frohman M. A., Boyle M., Martin G. R. Isolation of the mouse Hox-2.9 gene; analysis of embryonic expression suggests that positional information along the anterior-posterior axis is specified by mesoderm. Development. 1990 Oct;110(2):589–607. doi: 10.1242/dev.110.2.589. [DOI] [PubMed] [Google Scholar]
  19. Galliot B., Dollé P., Vigneron M., Featherstone M. S., Baron A., Duboule D. The mouse Hox-1.4 gene: primary structure, evidence for promoter activity and expression during development. Development. 1989 Oct;107(2):343–359. doi: 10.1242/dev.107.2.343. [DOI] [PubMed] [Google Scholar]
  20. Garcia-Fernàndez J., Baguñ J., Saló E. Planarian homeobox genes: cloning, sequence analysis, and expression. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7338–7342. doi: 10.1073/pnas.88.16.7338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Gehring W. J., Müller M., Affolter M., Percival-Smith A., Billeter M., Qian Y. Q., Otting G., Wüthrich K. The structure of the homeodomain and its functional implications. Trends Genet. 1990 Oct;6(10):323–329. doi: 10.1016/0168-9525(90)90253-3. [DOI] [PubMed] [Google Scholar]
  22. Gough N. M. Rapid and quantitative preparation of cytoplasmic RNA from small numbers of cells. Anal Biochem. 1988 Aug 15;173(1):93–95. doi: 10.1016/0003-2697(88)90164-9. [DOI] [PubMed] [Google Scholar]
  23. Graham A., Papalopulu N., Krumlauf R. The murine and Drosophila homeobox gene complexes have common features of organization and expression. Cell. 1989 May 5;57(3):367–378. doi: 10.1016/0092-8674(89)90912-4. [DOI] [PubMed] [Google Scholar]
  24. Hill R. E., Jones P. F., Rees A. R., Sime C. M., Justice M. J., Copeland N. G., Jenkins N. A., Graham E., Davidson D. R. A new family of mouse homeo box-containing genes: molecular structure, chromosomal location, and developmental expression of Hox-7.1. Genes Dev. 1989 Jan;3(1):26–37. doi: 10.1101/gad.3.1.26. [DOI] [PubMed] [Google Scholar]
  25. Holland P. W. Cloning and evolutionary analysis of msh-like homeobox genes from mouse, zebrafish and ascidian. Gene. 1991 Feb 15;98(2):253–257. doi: 10.1016/0378-1119(91)90182-b. [DOI] [PubMed] [Google Scholar]
  26. Kaufman T. C., Lewis R., Wakimoto B. Cytogenetic Analysis of Chromosome 3 in DROSOPHILA MELANOGASTER: The Homoeotic Gene Complex in Polytene Chromosome Interval 84a-B. Genetics. 1980 Jan;94(1):115–133. doi: 10.1093/genetics/94.1.115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Keppel E., Schaller H. C. A 33 kDa protein with sequence homology to the 'laminin binding protein' is associated with the cytoskeleton in hydra and in mammalian cells. J Cell Sci. 1991 Dec;100(Pt 4):789–797. doi: 10.1242/jcs.100.4.789. [DOI] [PubMed] [Google Scholar]
  28. Kim Y., Nirenberg M. Drosophila NK-homeobox genes. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7716–7720. doi: 10.1073/pnas.86.20.7716. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kojima T., Ishimaru S., Higashijima S., Takayama E., Akimaru H., Sone M., Emori Y., Saigo K. Identification of a different-type homeobox gene, BarH1, possibly causing Bar (B) and Om(1D) mutations in Drosophila. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4343–4347. doi: 10.1073/pnas.88.10.4343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lathe R. Synthetic oligonucleotide probes deduced from amino acid sequence data. Theoretical and practical considerations. J Mol Biol. 1985 May 5;183(1):1–12. doi: 10.1016/0022-2836(85)90276-1. [DOI] [PubMed] [Google Scholar]
  31. Lewis E. B. A gene complex controlling segmentation in Drosophila. Nature. 1978 Dec 7;276(5688):565–570. doi: 10.1038/276565a0. [DOI] [PubMed] [Google Scholar]
  32. Lufkin T., Dierich A., LeMeur M., Mark M., Chambon P. Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell. 1991 Sep 20;66(6):1105–1119. doi: 10.1016/0092-8674(91)90034-v. [DOI] [PubMed] [Google Scholar]
  33. Mavilio F., Simeone A., Giampaolo A., Faiella A., Zappavigna V., Acampora D., Poiana G., Russo G., Peschle C., Boncinelli E. Differential and stage-related expression in embryonic tissues of a new human homoeobox gene. Nature. 1986 Dec 18;324(6098):664–668. doi: 10.1038/324664a0. [DOI] [PubMed] [Google Scholar]
  34. McGinnis W. Homeo box sequences of the Antennapedia class are conserved only in higher animal genomes. Cold Spring Harb Symp Quant Biol. 1985;50:263–270. doi: 10.1101/sqb.1985.050.01.033. [DOI] [PubMed] [Google Scholar]
  35. Monaghan A. P., Davidson D. R., Sime C., Graham E., Baldock R., Bhattacharya S. S., Hill R. E. The Msh-like homeobox genes define domains in the developing vertebrate eye. Development. 1991 Aug;112(4):1053–1061. doi: 10.1242/dev.112.4.1053. [DOI] [PubMed] [Google Scholar]
  36. Murtha M. T., Leckman J. F., Ruddle F. H. Detection of homeobox genes in development and evolution. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10711–10715. doi: 10.1073/pnas.88.23.10711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Park H. D., Ortmeyer A. B., Blankenbaker D. P. Cell division during regeneration in Hydra. Nature. 1970 Aug 8;227(5258):617–619. doi: 10.1038/227617a0. [DOI] [PubMed] [Google Scholar]
  38. Porteus M. H., Bulfone A., Ciaranello R. D., Rubenstein J. L. Isolation and characterization of a novel cDNA clone encoding a homeodomain that is developmentally regulated in the ventral forebrain. Neuron. 1991 Aug;7(2):221–229. doi: 10.1016/0896-6273(91)90260-7. [DOI] [PubMed] [Google Scholar]
  39. Price M., Lemaistre M., Pischetola M., Di Lauro R., Duboule D. A mouse gene related to Distal-less shows a restricted expression in the developing forebrain. Nature. 1991 Jun 27;351(6329):748–751. doi: 10.1038/351748a0. [DOI] [PubMed] [Google Scholar]
  40. Rangini Z., Frumkin A., Shani G., Guttmann M., Eyal-Giladi H., Gruenbaum Y., Fainsod A. The chicken homeo box genes CHox1 and CHox3: cloning, sequencing and expression during embryogenesis. Gene. 1989 Mar 15;76(1):61–74. doi: 10.1016/0378-1119(89)90008-5. [DOI] [PubMed] [Google Scholar]
  41. Robert B., Sassoon D., Jacq B., Gehring W., Buckingham M. Hox-7, a mouse homeobox gene with a novel pattern of expression during embryogenesis. EMBO J. 1989 Jan;8(1):91–100. doi: 10.1002/j.1460-2075.1989.tb03352.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Robinson M. O., Simon M. I. Determining transcript number using the polymerase chain reaction: Pgk-2, mP2, and PGK-2 transgene mRNA levels during spermatogenesis. Nucleic Acids Res. 1991 Apr 11;19(7):1557–1562. doi: 10.1093/nar/19.7.1557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sasaki H., Yokoyama E., Kuroiwa A. Specific DNA binding of the two chicken Deformed family homeodomain proteins, Chox-1.4 and Chox-a. Nucleic Acids Res. 1990 Apr 11;18(7):1739–1747. doi: 10.1093/nar/18.7.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Schaller D., Wittmann C., Spicher A., Müller F., Tobler H. Cloning and analysis of three new homeobox genes from the nematode Caenorhabditis elegans. Nucleic Acids Res. 1990 Apr 25;18(8):2033–2036. doi: 10.1093/nar/18.8.2033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Schaller H. C., Hoffmeister S. A., Dübel S. Role of the neuropeptide head activator for growth and development in hydra and mammals. Development. 1989;107 (Suppl):99–107. doi: 10.1242/dev.107.Supplement.99. [DOI] [PubMed] [Google Scholar]
  47. Schierwater B., Murtha M., Dick M., Ruddle F. H., Buss L. W. Homeoboxes in cnidarians. J Exp Zool. 1991 Dec;260(3):413–416. doi: 10.1002/jez.1402600316. [DOI] [PubMed] [Google Scholar]
  48. Scott M. P., Tamkun J. W., Hartzell G. W., 3rd The structure and function of the homeodomain. Biochim Biophys Acta. 1989 Jul 28;989(1):25–48. doi: 10.1016/0304-419x(89)90033-4. [DOI] [PubMed] [Google Scholar]
  49. Su M. W., Suzuki H. R., Solursh M., Ramirez F. Progressively restricted expression of a new homeobox-containing gene during Xenopus laevis embryogenesis. Development. 1991 Apr;111(4):1179–1187. doi: 10.1242/dev.111.4.1179. [DOI] [PubMed] [Google Scholar]
  50. Sundin O. H., Busse H. G., Rogers M. B., Gudas L. J., Eichele G. Region-specific expression in early chick and mouse embryos of Ghox-lab and Hox 1.6, vertebrate homeobox-containing genes related to Drosophila labial. Development. 1990 Jan;108(1):47–58. doi: 10.1242/dev.108.Supplement.47. [DOI] [PubMed] [Google Scholar]
  51. Suzuki H. R., Padanilam B. J., Vitale E., Ramirez F., Solursh M. Repeating developmental expression of G-Hox 7, a novel homeobox-containing gene in the chicken. Dev Biol. 1991 Nov;148(1):375–388. doi: 10.1016/0012-1606(91)90345-4. [DOI] [PubMed] [Google Scholar]
  52. Takahashi Y., Le Douarin N. cDNA cloning of a quail homeobox gene and its expression in neural crest-derived mesenchyme and lateral plate mesoderm. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7482–7486. doi: 10.1073/pnas.87.19.7482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wang G. V., Dolecki G. J., Carlos R., Humphreys T. Characterization and expression of two sea urchin homeobox gene sequences. Dev Genet. 1990;11(1):77–87. doi: 10.1002/dvg.1020110109. [DOI] [PubMed] [Google Scholar]
  54. Wolberger C., Vershon A. K., Liu B., Johnson A. D., Pabo C. O. Crystal structure of a MAT alpha 2 homeodomain-operator complex suggests a general model for homeodomain-DNA interactions. Cell. 1991 Nov 1;67(3):517–528. doi: 10.1016/0092-8674(91)90526-5. [DOI] [PubMed] [Google Scholar]
  55. Yokouchi Y., Ohsugi K., Sasaki H., Kuroiwa A. Chicken homeobox gene Msx-1: structure, expression in limb buds and effect of retinoic acid. Development. 1991 Oct;113(2):431–444. doi: 10.1242/dev.113.2.431. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES