Skip to main content

Advertisement

Log in

Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The matrix metalloproteinases (MMPs) are a family of proteases capable of degrading various components of the extracellular matrix (ECM). Among them, the membrane type MMP–1 (MT1–MMP) has been shown to participate in the activation of MMP gelatinase A (GelA), suggesting that they may function together in development and pathogenesis. Here, we have investigated the spatiotemporal expression profiles of Xenopus laevis MT1–MMP and GelA genes during thyroid-hormone-dependent metamorphosis. We have focused our studies on two organs: (1) the intestine, which undergoes first the degeneration of the tadpole epithelium through apoptosis and then the development of adult epithelium and other tissues, and (2) the tail, which completely resorbs through programmed cell death. We show that both MT1–MMP and GelA are upregulated in the intestine and tail when both organs undergo metamorphosis. Within the organs, MT1–MMP and GelA are coexpressed in the connective tissues during both natural and thyroid-hormone-induced metamorphosis. In addition, MT1–MMP (but not GelA) is also expressed in the longitudinal muscle cells of the metamorphosing intestine. These results suggest that MT1–MMP and GelA function together in the ECM degradation or remodeling associated with metamorphosis and that MT1–MMP has additional GelA–independent roles in the development of adult longitudinal muscle in the intestine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alexander CM, Werb Z (1991) Extracellular matrix degradation. In: ED Hay (ed) Cell biology of extracellular matrix. Plenum, New York, pp 255–302

    Google Scholar 

  • Bai S, Thummel R, Godwin AR, Nagase H, Itoh Y, Li L, Evans R, McDermott J, Seiki M, Sarras MP Jr (2005) Matrix metalloproteinase expression and function during fin regeneration in zebrafish: analysis of MT1–MMP, MMP2 and TIMP2. Matrix Biol 24:247–260

    Article  PubMed  CAS  Google Scholar 

  • Barrett JA, Rawloings ND, Woessner JF (1998) Handbook of proteolytic enzymes. Academic Press, New York

    Google Scholar 

  • Berry DL, Rose CS, Remo BF, Brown DD (1998a) The expression pattern of thyroid hormone response genes in remodeling tadpole tissues defines distinct growth and resorption gene expression programs. Dev Biol 203:24–35

    Article  PubMed  CAS  Google Scholar 

  • Berry DL, Schwartzman RA, Brown DD (1998b) The expression pattern of thyroid hormone response genes in the tadpole tail identifies multiple resorption programs. Dev Biol 203:12–23

    Article  PubMed  CAS  Google Scholar 

  • Birkedal-Hansen H, Moore WG, Bodden MK, Windsor LJ, Birkedal-Hansen B, DeCarlo A, Engler JA (1993) Matrix metalloproteinases: a review. Crit Rev Oral Biol Med 4:197–250

    PubMed  CAS  Google Scholar 

  • Bjorn SF, Hastrup N, Lund LR, Dano K, Larsen JF, Pyke C (1997) Co-ordinated expression of MMP–2 and its putative activator, MT1–MMP, in human placentation. Mol Hum Reprod 3:713–723

    Article  PubMed  CAS  Google Scholar 

  • Cao J, Kozarekar P, Pavlaki M, Chiarelli C, Bahou WF, Zucker S (2004) Distinct roles for the catalytic and hemopexin domains of membrane type 1–matrix metalloproteinase in substrate degradation and cell migration. J Biol Chem 279:14129–14139

    Article  PubMed  CAS  Google Scholar 

  • d’Ortho MP, Will H, Atkinson S, Butler G, Messent A, Gavrilovic J, Smith B, Timpl R, Zardi L, Murphy G (1997) Membrane–type matrix metalloproteinases 1 and 2 exhibit broad-spectrum proteolytic capacities comparable to many matrix metalloproteinases. Eur J Biochem 250:751–757

    Article  PubMed  CAS  Google Scholar 

  • Damjanovski S, Ishizuya-Oka A, Shi YB (1999) Spatial and temporal regulation of collagenases–3, –4, and stromelysin–3 implicates distinct functions in apoptosis and tissue remodeling during frog metamorphosis. Cell Res 9:91–105

    Article  PubMed  CAS  Google Scholar 

  • Dodd MHI, Dodd JM (1976) The biology of metamorphosis. In: Lofts B (ed) Physiology of amphibia, vol 3. Academic Press, New York, pp 467–599

    Google Scholar 

  • Fu L, Ishizuya-Oka A, Buchholz DR, Amano T, Matsuda H, Shi YB (2005) A causative role of stromelysin–3 in extracellular matrix remodeling and epithelial apoptosis during intestinal metamorphosis in Xenopus laevis. J Biol Chem 280:27856–27865

    Article  PubMed  CAS  Google Scholar 

  • Harrison M, Abu-Elmagd M, Grocott T, Yates C, Gavrilovic J, Wheeler GN (2004) Matrix metalloproteinase genes in Xenopus development. Dev Dyn 231:214–220

    Article  PubMed  CAS  Google Scholar 

  • Ishizuya-Oka A, Ueda S (1996) Apoptosis and cell proliferation in the Xenopus small intestine during metamorphosis. Cell Tiss Res 286:467–476

    Article  CAS  Google Scholar 

  • Ishizuya-Oka A, Li Q, Amano T, Damjanovski S, Ueda S, Shi YB (2000) Requirement for matrix metalloproteinase stromelysin–3 in cell migration and apoptosis during tissue remodeling in Xenopus laevis. J Cell Biol 150:1177–1188

    Article  PubMed  CAS  Google Scholar 

  • Jenkins GM, Crow MT, Bilato C, Gluzband Y, Ryu WS, Li Z, Stetler-Stevenson W, Nater C, Froehlich JP, Lakatta EG, Cheng L (1998) Increased expression of membrane-type matrix metalloproteinase and preferential localization of matrix metalloproteinase–2 to the neointima of balloon-injured rat carotid arteries. Circulation 97:82–90

    PubMed  CAS  Google Scholar 

  • Jung JC, Leco KJ, Edwards DR, Fini ME (2002) Matrix metalloproteinases mediate the dismantling of mesenchymal structures in the tadpole tail during thyroid hormone-induced tail resorption. Dev Dyn 223:402–413

    Article  PubMed  CAS  Google Scholar 

  • Kikuyama S, Kawamura K, Tanaka S, Yamamoto K (1993) Aspects of amphibian metamorphosis: hormonal control. Int Rev Cytol 145:105–148

    PubMed  CAS  Google Scholar 

  • Kleiner DE Jr, Stetler-Stevenson WG (1993) Structural biochemistry and activation of matrix metalloproteases. Curr Opin Cell Biol 5:891–897

    Article  PubMed  CAS  Google Scholar 

  • Matsuda H, Yokoyama H, Endo T, Tamura K, Ide H (2001) An epidermal signal regulates Lmx–1 expression and dorsal–ventral pattern during Xenopus limb regeneration. Dev Biol 229:351–362

    Article  PubMed  CAS  Google Scholar 

  • McCawley LJ, Matrisian LM (2001) Matrix metalloproteinases: they’re not just for matrix anymore! Curr Opin Cell Biol 13:534–540

    Article  PubMed  CAS  Google Scholar 

  • Mott JD, Werb Z (2004) Regulation of matrix biology by matrix metalloproteinases. Curr Opin Cell Biol 16:558–564

    Article  PubMed  CAS  Google Scholar 

  • Murphy G, Stanton H, Cowell S, Butler G, Knauper V, Atkinson S, Gavrilovic J (1999) Mechanisms for pro matrix metalloproteinase activation. Apmis 107:38–44

    Article  PubMed  CAS  Google Scholar 

  • Nagase H (1998) Cell surface activation of progelatinase A (proMMP–2) and cell migration. Cell Res 8:179–186

    PubMed  CAS  Google Scholar 

  • Nagase H, Suzuki K, Morodomi T, Enghild JJ, Salvesen G (1992) Activation mechanisms of the precursors of matrix metalloproteinases 1, 2 and 3. Matrix Suppl 1:237–244

    PubMed  CAS  Google Scholar 

  • Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). Garland, New York

    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

    PubMed  CAS  Google Scholar 

  • Overall CM (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 22:51–86

    Article  PubMed  CAS  Google Scholar 

  • Parks WC, Mecham RP (1998) Matrix metalloproteinases. Academic Press, New York

    Google Scholar 

  • Patterton D, Hayes WP, Shi YB (1995) Transcriptional activation of the matrix metalloproteinase gene stromelysin–3 coincides with thyroid hormone-induced cell death during frog metamorphosis. Dev Biol 167:252–262

    Article  PubMed  CAS  Google Scholar 

  • Pei D (1999) Leukolysin/MMP25/MT6–MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res 9:291–303

    Article  PubMed  CAS  Google Scholar 

  • Pei D, Weiss SJ (1995) Furin-dependent intracellular activation of the human stromelysin–3 zymogen. Nature 375:244–247

    Article  PubMed  CAS  Google Scholar 

  • Ricke WA, Smith GW, Reynolds LP, Redmer DA, Smith MF (2002) Matrix metalloproteinase (2, 9, and 14) expression, localization, and activity in ovine corpora lutea throughout the estrous cycle. Biol Reprod 66:1083–1094

    Article  PubMed  CAS  Google Scholar 

  • Sang QA, Douglas DA (1996) Computational sequence analysis of matrix metalloproteinases. J Protein Chem 15:137–160

    Article  PubMed  CAS  Google Scholar 

  • Seiki M (1999) Membrane–type matrix metalloproteinases. Apmis 107:137–143

    PubMed  CAS  Google Scholar 

  • Shi Y-B (1999) Amphibian metamorphosis: from morphology to molecular biology. Wiley, New York

    Google Scholar 

  • Shi YB, Ishizuya-Oka A (1996) Biphasic intestinal development in amphibians: embryogenesis and remodeling during metamorphosis. Curr Top Dev Biol 32:205–235

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Shi YB, Fu L, Hsia SC, Tomita A, Buchholz D (2001) Thyroid hormone regulation of apoptotic tissue remodeling during anuran metamorphosis. Cell Res 11:245–252

    Article  PubMed  CAS  Google Scholar 

  • Stawowy P, Meyborg H, Stibenz D, Stawowy NB, Roser M, Thanabalasingam U, Veinot JP, Chretien M, Seidah NG, Fleck E, Graf K (2005) Furin-like proprotein convertases are central regulators of the membrane type matrix metalloproteinase–pro–matrix metalloproteinase–2 proteolytic cascade in atherosclerosis. Circulation 111:2820–2827

    Article  PubMed  CAS  Google Scholar 

  • Sternlicht MD, Werb Z (2001) How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 17:463–516

    Article  PubMed  CAS  Google Scholar 

  • Stolow MA, Bauzon DD, Li J, Sedgwick T, Liang VC, Sang QA, Shi YB (1996) Identification and characterization of a novel collagenase in Xenopus laevis: possible roles during frog development. Mol Biol Cell 7:1471–1483

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Uria JA, Werb Z (1998) Matrix metalloproteinases and their expression in mammary gland. Cell Res 8:187–194

    PubMed  CAS  Google Scholar 

  • Van Wart HE, Birkedal-Hansen H (1990) The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc Natl Acad Sci USA 87:5578–5582

    Article  PubMed  Google Scholar 

  • Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92:827–839

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Brown DD (1993) Thyroid hormone-induced gene expression program for amphibian tail resorption. J Biol Chem 268:16270–16278

    PubMed  CAS  Google Scholar 

  • Woessner JF Jr (1991) Matrix metalloproteinases and their inhibitors in connective tissue remodeling. FASEB J 5:2145–2154

    PubMed  CAS  Google Scholar 

  • Yoshida N, Urase K, Takahashi J, Ishii Y, Yasugi S (1996) Mucus-associated antigen in epithelial cells of the chicken digestive tract: developmental change in expression and implications for morphogenesis-function relationship. Dev Growth Differ 38:185–192

    Article  CAS  Google Scholar 

  • Zhou Z, Apte SS, Soininen R, Cao R, Baaklini GY, Rauser RW, Wang J, Cao Y, Tryggvason K (2000) Impaired endochondral ossification and angiogenesis in mice deficient in membrane-type matrix metalloproteinase I. Proc Natl Acad Sci USA 97:4052–4057

    Article  PubMed  CAS  Google Scholar 

  • Zucker S, Pei D, Cao J, Lopez-Otin C (2003) Membrane type–matrix metalloproteinases (MT–MMP). Curr Top Dev Biol 54:1–74

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yun-Bo Shi.

Additional information

This research was supported by the Intramural Research Program of the National Institute of Child Health and Human Development, NIH. T. Hasebe and H. Matsuda were supported in part by JSPS (NIH) fellowships.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hasebe, T., Hartman, R., Matsuda, H. et al. Spatial and temporal expression profiles suggest the involvement of gelatinase A and membrane type 1 matrix metalloproteinase in amphibian metamorphosis. Cell Tissue Res 324, 105–116 (2006). https://doi.org/10.1007/s00441-005-0099-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-005-0099-7

Keywords

Navigation