Abstract
Homeobox (HBox) genes are well-known to be involved in development and differentiation. To ascertain a role of HBox genes in the process of liver regeneration, we identified HBox genes expressed at various times after partial hepatectomy in rats (at 0 hr, 1 hr, 2 days, and 4 days) by using reverse transcription-polymerase chain reaction (RT-PCR), cloning, and sequencing techniques. By the competitive RT-PCR method using generic primers, expression levels of HBox genes in regenerating livers were estimated at as low as only 0.4–2% of that in 14-day embryonic liver; however, we identified multiple HBox genes at different stages. Comparing sets of HBox genes identified at different stages, we could find two candidates of stage specifically expressed HBox genes (one rat caudal-related gene,RCdx-3, stimulated at 1 hr, and one rat Hox gene,RHoxB5, repressed after hepatectomy) and continuous expression of five Hox genes (RHoxA1, A4, A5, B2, andB3) before and after hepatectomy. These HBox genes are considered to correlate with the process of liver regeneration.
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Acampora, D., D'Esposito, M., Faiella, A., Pannese, M., Migliaccio, E., Morelli, F., Stornaiuolo, A., Nigro, V., Simeone, A., and Boncinelli, E. (1989). The human HOX gene family.Nucl. Acids Res. 1710385.
Baron, A., Featherstone, M. S., Hill, R. E., Hall, A., Galliot, B., and Duboule, D. (1987).Hox-1.6: A mouse homeo-box-containing gene member of the Hox-1 complex.EMBO J. 62977.
Breier, G., Dressler, G. R., and Gruss, P. (1988). Primary structure and developmental expression pattern ofHox 3.1, a member of the murineHox 3 homeobox gene cluster.EMBO J. 71329.
Duboule, D., Baron, A., Mahl, P., and Galliot, B. (1986). A new homeobox is present in overlapping cosmid clones which define the mouse HOX-1 locus.EMBO J. 51973.
Duprey, P., Chowdhury, K., Dressler, G. R., Balling, R., Simon, D., Guenet, J.-L., and Gruss, P. (1988). A mouse gene homologous to theDrosophila gene caudal is expressed in epithelial cells from the embryonic intestine.Genes Dev. 21647.
Falzon, M., and Chung, S. Y. (1988). The expression of rat homeobox-containing genes is developmentally regulated and tissue specific.Development 103601.
Falzon, M., Sanderson, N., and Chung, S. Y. (1987). Cloning and expression of rat homeo-box-containing sequences.Gene 5423.
Frain, M., Swart, G., Monaci, P., Nicosia, A., Stampfli, S., Frank, R., and Cortese, R. (1989). The liver-specific transcription factor LF-B1 contains a highly diverged homeobox DNA binding domain.Cell 59145.
Freund, J.-N., Boukamel, R., and Benazzouz, A. (1992). Gradient expression ofCdx along the rat intestine throughout postnatal development.FEBS Lett. 314163.
Gamer, L. W., and Wright, C. V. E. (1993). MurineCdx-4 bears striking similarities to theDrosophila caudal gene in its homeodomain sequence and early expression pattern.Mech. Dev. 4371.
German, M. S., Wang, J., Chadwick, R. B., and Rutter, W. J. (1992). Synergistic activation of the insulin gene by a LIM-homeo domain protein and a basic helix-loop-helix protein: building a functional insulin minienhancer complex.Genes Dev. 62165.
Graham, A., Papalopulu, N., Lorimer, J., McVey, J. H., Tuddenham, E. G. D., and Krumlauf, R. (1988). Characterization of a murine homeo box gene,Hox-2.6, related to theDrosophila Deformed gene.Genes Dev. 21424.
Guazzi, S., Price, M., Felice, M. D., Damante, G., Mattei, M.-G., and Di Lauro, R. (1990). Thyroid nuclear factor 1 (TTF-1) contains a homeodomain and displays a novel DNA binding specificity.EMBO J. 93631.
Hart, C. P., Fainsod, A., and Ruddle, F. H. (1987). Sequence analysis of the murineHox-2.2, -2.3, and-2.4 homeo boxes; Evolutionary and structural comparisons.Genomics 1182.
Higgins, G. M., and Anderson, R. M. (1931). Experimental pathology of the liver. I. Restoration of the liver 3 of the white rat following partial surgical removal.Arch. 3 Pathol. 12186.
Jackson, I. J., Schofield, P., and Hogan, B. (1985). A mouse homeo box gene is expressed during embryogenesis and in adult kidney.Nature 317745.
Kongsuwan, K., Webb, E., Housiaux, P., and Adams, J. M. (1988). Expression of multiple homeobox genes within diverse mammalian haematopoietic lineages.EMBO J. 72131.
Krumlauf, R. (1994). Hox genes in vertebrate development.Cell 78191.
Lawrence, P. A., and Morata, G. (1994). Homeobox genes: Their function in Drosophila segmentation and pattern formation.Cell 78181.
Lonai, P., Arman, E., Czosnek, H., Ruddle, F. H., and Blatt, C. (1987). New murine homeoboxes: structure, chromosomal assignment, and differential expression in adult erythropoiesis.DNA 6409.
McGinnis, W., Levine, M. S., Hafen, E., Kuroiwa, A., and Gehring, W. J. (1984). A conserved DNA sequence in homeotic genes of theDrosophila Antennapedia andBithorax complexes.Nature 308428.
Michalopoulos, G. K. (1990). Liver regeneration: molecular mechanisms of growth control.FASEB J. 4176.
Nudel, U., Zakut, R., Shani, M., Neuman, S., Levy, Z., and Yaffe, D. (1983). The nucleotide sequence of rat cytoplasmic β-actin gene.Nucl. Acids Res. 111759.
Odenwald, W. F., Taylor, C. F., Palmer-Hill, F. J., Friedrich, V., Jr., Tani, M., and Lazzarini, R. A. (1987). Expression of a homeo domain protein in noncontact-inhibited cultured cells and postmitotic neurons.Genes Dev. 1482.
Petropoulos, C., Andrews, G., Tamaoki, T., and Fausto, N. (1983). α-Fetoprotein and alubumin mRNA levels in liver regeneration and carcinogenesis.J. Biol. Chem. 2584901.
Poietz, B. J., Ehrlich, G. D., Byrne, B. C., Abbot, M., Kwok, S., and Sninsky, J. (1989). Use of polymerase chain reaction in detection, quantification, and characterization of human retroviruses. In Ehrlich, H. A., Gibbs, R., and Kazazian, H. H., Jr. (eds.),Polymerase Chain Reaction Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, p. 159.
Rubin, M. R., King, W., Toth, L. E., Sawczuk, I. S., Levine, M. S., D'Eustachio, P., and Nguyen-Huu, M. C. (1987). MurineHox-1.7 homeo-box gene: Cloning, chromosomal location, and expression.Mol. Cell. Biol. 73836.
Rubock, M. J., Larin, Z., Cook, M., Papalopulu, N., Krumlauf, R., and Lehrach, H. (1990). A yeast artificial chromosome containing the mouse homeobox clusterHox-2.Proc. Natl. Acad. Sci. USA 874751.
Saiki, R. K., Gelfand, D. H., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1988). Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.Science 239487.
Sakoyama, Y., Mizuta, I., Ogasawara, N., and Yoshikawa, H. (1994). Cloning of rat homeobox genes.Biochem. Genet. 32351.
Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989).Molecular Cloning: A Laboratory Manual Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Sanger, F., Nicklen, S., and Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors.Proc. Natl. Acad. Sci. USA 745463.
Schughart, K., Pravtcheva, D., Newman, M. S., Hunihan, L. W., Jiang, Z., and Ruddle, F. H. (1989). Isolation and regional localization of the murine homeobox-containing geneHox-3.3 to mouse chromosome region 15E.Genomics 576.
Scott, M. P. (1992). Vertebrate homeobox gene nomenclature.Cell 71551.
Scott, M. P., and Weiner, A. J. (1984). Structural relationships among genes that control development: Sequence homology between theAntennapedia, Ultrabithorax andfushitarazu loci of Drosophila.Proc. Natl. Acad. Sci. USA 814115.
Shen, W.-F., Largman, C., Lowney, P., Corral, J. C., Detmer, K., Hauser, C. A., Simonitch, T. A., Hack, F. M., and Lawrence, H. J. (1989). Lineage-restricted expression of homeobox-containing genes in human hematopoietic cell lines.Proc. Natl. Acad. Sci. USA 868536.
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Mizuta, I., Ogasawara, N., Yoshikawa, H. et al. Identification of homeobox genes expressed during the process of rat liver regeneration after partial hepatectomy. Biochem Genet 34, 1–15 (1996). https://doi.org/10.1007/BF02396236
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DOI: https://doi.org/10.1007/BF02396236