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Thyroid hormone-dependent expression of bullfrog tadpole collagenase gene

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Abstract

Collagenase has been suggested to play a pivotal role in tissue remodeling during anuran metamorphosis. RNA blot analysis and nuclear run-on assay showed that collagenase genes of caudal cells of tadpoles of the bullfrog, Rana catesbeiana, are up-regulated by thyroid hormone after only 24 h. The gene for collagenase was cloned from genome DNA of the bullfrog and its structure, including the 5′-upstream region with-1 kbp, was determined. The gene contained 4 exons with sequences of the enzyme active centre in exon 2. Cis-acting regulatory sequences were recognized in the 5′-upstream region as AP-1 and Sp1, which had also been found in the mammalian collagenase gene. A special sequence was noticed near −870 bp, 5′-AG-GTAAGAACAGGATA-3′, that satisfies a general criterion for the identification of the thyroid hormone responsive element (TRE) proposed by Umesono et al. (1991) and is homologous to the element reported in genes of thyroid-hormone responsive proteins such as thyroid hormone receptor (TR) β, growth hormone, malic enzyme and myosin heavy chain. Results of the gel mobility shift assay supported the idea that the sequence functions as a TRE. The supershift procedure demonstrated that the complex formed in the gel mobility shift assay contains TR. The present study revealed the uniqueness of bullfrog collagenase as a metamorphosis-associated enzyme, because, to our knowledge, known mammalian collagenase genes do not contain THE in their transcription regulatory regions.

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Abbreviations

TH :

thyroid hormone

T 3 :

3,3′,5-triido-l-thyronine

TR :

thyroid hormone receptor

TRE :

thyroid hormone responsive element

MMP :

matrix metalloproteinase

SDS :

sodium dodecyl sulphate

SSC :

sodium-sodium citrate buffe

References

  • Angel P, Baumann I, Stein B, Delius H, Rahmsdorf HJ, Herrlich P (1987) 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5′-flanking region. Mol Cell Biol 7:2256–2266

    Google Scholar 

  • Cawston TE, Tyler JA (1979) Purification of pig synovial collagenase to high specific activity. Biochem J 183:647–656

    Google Scholar 

  • Collier IE, Smith J, Kronberger A, Bauer EA, Wilhelm SM, Eisen AZ, Goldberg GI (1988) The structure of the human skin fibroblast collagenase gene. J Biol Chem 263:10711–10713

    Google Scholar 

  • Demay MB, Kiernan MS, Delucca HF, Kronengerg HM (1992) Sequences in the human parathyroid hormone gene that bind the 1,25-dihydroxyvitamin D3 receptor and mediate transcriptional repression in response to 1,25-dihydroxyvitamin D3. Proc Natl Acad Sci USA 89:8097–8101

    Google Scholar 

  • Evans RM (1988) Steroid and thyroid hormone receptors as transcriptional regulators of development and physiology. Science 240:889–895

    Google Scholar 

  • Falcone M, Miyamoto T, Fierro-Renoy F, Macchia E, Degroot LJ (1992) Antipeptide polyclonal antibodies specifically recognize each human thyroid hormonereceptor isoform. Endcrinology 131:2419–2429

    Google Scholar 

  • Fini ME, Plucinska IM, Mayer AS, Gross RH, Brinckerhoff CE (1987) A gene for rabbit synovial cell collagenase: member for a family of metal] oproteinases that degrade the connective tissue matrix. Biochemistry 26:6156–6165

    Google Scholar 

  • Flink IL, Morkin E (1990) Interaction of thyroid hormone receptors with strong and weak cis-acting elements in the human amyosin heavy chain gene promoter. J Biol Chem 265:11233–11237

    Google Scholar 

  • Freije JMP, Díez-Itza I, Balbín M, Sánchez LM, Blascco R, Tolivia J, López-Otín C (1994) Molecular cloning and expression of collagenase-3, a novel human matrix metalloproteinase produced by breast carcinomas. J Biol Chem 269:16766–16773

    Google Scholar 

  • Fried MG, Crothers DM (1981) Nucleic Acids Res 9:6505–6510

    Google Scholar 

  • Garner MM, Revzin A (1981) A gel electrophoresis method for quantifying the binding of proteins to specific DNA regions: application to components of the Escherishia coli lactose operon regulatory system. Nucleic Acids Res 9:3047–3060

    Google Scholar 

  • Goldberg GI, Wilhelm SM, Kronberger A, Bauer EA, Grant GA, Eisen AZ (1986) Human fibroblast collagenase. Complete primary structure and homology to an oncogene transformation-induced rat protein. J Biol Chem 261:6600–6605

    Google Scholar 

  • Graubert T, Johnston J, Berliner N (1993) Cloning and expression of the cDNA encoding mouse neutrophil gelatinase: demonstration of coordinate secondary granule protein gene expression during terminal neutrophil maturation. Blood 82:3192–3197

    Google Scholar 

  • Greenberg ME, Ziff EB (1984) Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature 311:433–438

    Google Scholar 

  • Gross J, Lapiere CM (1962) Collagenolytic activity in amphibian tissues: a tissue culture assay. Proc Natl Acad Sci USA 48: 1014–1022

    Google Scholar 

  • Groudine M, Peretz M, Weintraub H (1981) Transcriptional regulation of hemoglobin switching in chicken embryos. Mol Cell Biol 1:281–288

    Google Scholar 

  • Gutman A, Wasylyk B (1990) The collagenase gene promoter contains a TPA and oncogene-responsive unit encompassing the PEA3 and AP-1 binding sites. EMBO J 9:2241–2246

    Google Scholar 

  • Hasty KA, Pourmotabbed TF, Goldberg GI, Thompson JP, Spinella DG, Stevens RM, Mainardi CL (1990) The collagen substrate specificity of human neutrophil collagenase. J Biol Chem 265:11421–11424

    Google Scholar 

  • Helbing C, Gergely G, Atkinson BG (1992) Sequential up-regulation of thyroid hormone β receptor, ornithine transcarbamylase, and carbamyl phosphate synthetase mRNAs in the liver of Rana catesbeiana tadpoles during spontaneous and thyroid hormone-induced metamorphosis. Dev. Genet 13:289–301

    Google Scholar 

  • Huang C-C, Abramson M (1975) Purification and characterization of collagenase from guinea pig skin. Biochim Biophys Acta 384:484–492

    Google Scholar 

  • Huhtala P, Tuuttila A, Chow LT, Lohi J, Keski-Oja J, Tryggvason (1991) Complete structure of the human gene for 92-kDa tyoe IV collagenase. J Biol Chem 266:16485–16490

    Google Scholar 

  • Kawahara A, Baker BS, Tata JR (1991) Developmental and regional expression of thyroid hormone receptor genes during Xenopus metamorphosis. Development 112:933–943

    Google Scholar 

  • Lapiere CM, Gross J (1963) Animal collagenase and collagen metabolism. In: Mechanisms of hard tissue destruction. American Association for the Advancement of Science, NY pp 663–694

    Google Scholar 

  • Muller D, Quantin B, Gesnel MC, Millon-Collard R, Abecassis J, Breathnach R (1988) The collagenase gene family in humans consists of at least four members. Biochem J 253:187–192

    Google Scholar 

  • Nagai Y, Lapiere CM, Gross J (1966) Tadpole collagenase. Preparation and purification. Biochemistry 5:3123–3130

    Google Scholar 

  • Nishikawa A, Yoshizato K (1985) Epidermal cells of the anuran tadpole tail: its isolation and characterization in vitro. Zool Sci 2:201–211

    Google Scholar 

  • Oofusa K, Yoshizato K (1991) Biochemical and immunological characterization of collagenase in tissues of metamorphosing bullfrog tadpoles. Dev Growth Differ 33:329–339

    Google Scholar 

  • Oofusa K, Yomori S, Yoshizato K (1994) Regionally and hormonally regulated expression of genes of collagen and collagenase in the anuran larval skin. Int J Dev Biol 38:345–350

    Google Scholar 

  • Patterson D, Hayes WP, Shi Y-B (1994) Transcriptional activation of the matrix metalloproteinase gene stromelysin-3 coincides with thyroid hormone-induced cell death during frog metamorphosis. Dev Biol in press

  • Petty KJ, Desvergne B, Mitsuhashi T, Nikodem VM (1990) Identification of a thyroid hormone responsive element in the malic enzyme gene. J Biol Chem 265:7395–7400

    Google Scholar 

  • Ranjan M, Wong M, Shi Y-B (1994) Transcriptional repression of Xenopus TRβ gene is mediated by a thyroid hormone response element located near the start site. J Biol Chem 269:24699–24705

    Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, NY

    Google Scholar 

  • Sap J, Magistris L, Stunnenberg H, Vennström B (1990) A major thyroid hormone responsive element in the third intron of the rat growth hormone gene. EMBO J 9:887–896

    Google Scholar 

  • Shi YB, Brown DD (1990) Developmental and thyroid hormone dependent regulation of pancreatic genes in Xenopus laevis. Gene Dev 4:1107–1113

    Google Scholar 

  • Shi Y-B, Liang VCT (1994) Cloning and characterization of the ribosomal protein L8 gene from Xenopus laevis. Biochim Biophys Acta 1217:227–228

    Google Scholar 

  • Tata JR (1993) Gene expression during metamorphosis: an ideal model for post-embryonic development. BioEssays 15:239–248

    Google Scholar 

  • Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–23

    Google Scholar 

  • Umesono K, Murakami KK, Thompson CC, Evans RM (1991) Direct repeats as selective response elements for the thyroid hormone, retinoic acid and vitamin D3 receptors. Cell 85:1255–1266

    Google Scholar 

  • Wang Z, Brown DD (1991) A gene expression screen. Proc Natl Acad Sci USA 88:11505–11509

    Google Scholar 

  • Whitham SE, Murphy G, Angel P, Rahmsdorf HJ, Smith B, Lyons A, Harris TJR, Reynolds JJ, Herrlich P, Docherty AJP (1986) Comparison of human stromelysin and collagenase by cloning and sequence analysis. Biochem J 240:913–916

    Google Scholar 

  • Wilhelm SM, Collier IE, Mariner BL, Eisen AZ, Grant GA, Goldberg GI (1989) SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J Biol Chem 264:17213–17221

    Google Scholar 

  • Yamamoto KR (1985) Steroid receptor regulated transcription of specific genes and gene networks. Ann Rev Genet 19:209–252

    Google Scholar 

  • Yaoita Y, Brown DD (1990) A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis. Gene Dev 4:1917–1924

    Google Scholar 

  • Yaoita Y, Shi YB, Brown DD (1990) Xenopus laevis a and b thyroid hormone receptors. Proc Natl Acad Sci USA 87:7090–7094

    Google Scholar 

  • Yoshizato K (1989) Biochemistry and cell biology of amphibian metamorphosis with a special emphasis on the mechanism of removal of larval organs. Int Rev Cytol 119:97–149

    Google Scholar 

  • Yoshizato K (1992) Death and transformation of larval cells during metamorphosis of anura. Dev Growth Differ 34:607–612

    Google Scholar 

Download references

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Oofusa, K., Yoshizato, K. Thyroid hormone-dependent expression of bullfrog tadpole collagenase gene. Roux's Arch Dev Biol 205, 243–251 (1996). https://doi.org/10.1007/BF00365802

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