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Cell-cell and cell-ECM interactions in epithelial apoptosis and cell renewal during frog intestinal development

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Abstract

Amphibian intestinal remodeling during metamorphosis is a developmental system that is entirely controlled by thyroid hormone. It transforms a simple tubular organ into a complex multiply folded frog intestine similar to that in higher vertebrates. This process involves the degeneration of the larval epithelium through programmed cell death (apoptosis) and concurrent proliferation and differentiation of adult cell types. Earlier morphological and cellular studies have provided strong evidence implicating the importance of cell-cell and cell-ECM (extracellular matrix) interactions in this process. The recent molecular characterization of the genes that are regulated by thyroid hormone has begun to reveal some molecular clues underlying such interactions. In particular, theXenopus putative morphogen hedgehog appears to be involved in regulating/mediating cell-cell interactions during adult epithelial proliferation, differentiation, and/or intestinal morphogenesis. On the other hand, several matrix metalloproteinases (MMPs) may be involved in remodeling the ECM. Of special interest is stromelysin-3, whose spatial and temporal expression profile during intestinal metamorphosis implicates a role in ECM remodeling, which in turn facilitates cell fate determination, i.e., apoptosis vs proliferation and differentiation. Understanding the mechanisms of action for those extracellular molecules will present a future challenge in developmental research.

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References

  1. Glass, G. B. J. (1968)Introduction to Gastrointestinal Physiology, Prentice-Hall, Englewood Cliffs, NJ.

    Google Scholar 

  2. Segal, G. H. and Petras, R. E. (1992) Small intestine, inHistology for Pathologists (Sternberg, S.S., ed.) Raven, New York. pp. 547–571.

    Google Scholar 

  3. Louvard, D., Kedinger, M. and Hauri, H. P. (1992) The differenitating intestinal epithelial cell: Establishment and maintenance of functions through interactions between cellular structures.Ann. Rev. Cell. Biol. 8, 157–195.

    PubMed  CAS  Google Scholar 

  4. Simon-Assmann, P. and Kedinger, M. (1993) Heterotypic cellular cooperation in gut morphogenesis and differentiation.Sem. Cell Biol. 4, 221–230.

    Article  CAS  Google Scholar 

  5. Traber, P. G. (1994) Differentiation of intestinal epithelial cells: lessons from the study of intestine-specific gene expression.J. Lab. Clin. Med. 123, 467–477.

    PubMed  CAS  Google Scholar 

  6. Simon, T. C. and Gordon, J. J. (1995) Intestinal epithelial cell differentiation: new insights from mice, flies and nematodes.Opin. Genet. Dev. 5, 577–586.

    Article  CAS  Google Scholar 

  7. Potten, C. S. and Loeffler, M. (1990) Stem cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt.Development 110, 1001–1020.

    PubMed  CAS  Google Scholar 

  8. Hermiston, M. L. and Gordon, J. I. (1993) Use of transgenic mice to characterize the multipotent intestinal stem cell and to analyze regulation of gene expression in various epithelial cell lineages as a function of their position along the cephalocaudal and crypt-to-villus (or crypt-to-surface epithelial cuff) axes of the gut.Sem. Develop. Biol. 4, 275–291.

    Article  CAS  Google Scholar 

  9. Dauca, M. and Hourdry, J. (1985) Transformations in the intestinal epithelium during anuran metamorphosis, inMetamorphosis (Balls, M. and Bownes, M., eds.), Clarendon, Oxford, UK, pp. 36–58.

    Google Scholar 

  10. Shi, Y.-B. and Ishizuya-Oka, A. (1996) Biphasic intestinal development in amphibians: Embryogensis and remodeling during metamorphosis.Current Topics Dev. Biol. 32, 205–235.

    Article  CAS  Google Scholar 

  11. 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.

    PubMed  CAS  Google Scholar 

  12. Nieuwkoop, P. D. and Faber, J. (1956)Normal Table of Xenopus laevis. North Holland Publishing, Amsterdam.

    Google Scholar 

  13. Ishizuya-Oka, A. and Shimozawa, A. (1987) Development of the connective tissue in the digestive tract of the larval and metamorphosing Xenopus laevis.Ant. Anz. Jena 164, 81–93.

    CAS  Google Scholar 

  14. Marshall, J. A. and Dixon, K. E. (1978) Cell specialization in the epithelium of the small intestine of feeding Xenopus laevis.J. Anat. 126, 133–144.

    PubMed  CAS  Google Scholar 

  15. McAvoy, J. W. and Dixon, K. E. (1977) Cell proliferation and renewal in the small intestinal epithelium of metamorphosing and adult Xenopus laevis.J. Exp. Zool. 202, 129–138.

    Article  Google Scholar 

  16. Ishizuya-Oka, A. and Shimozawa, A. (1992) Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivo and in vitro.J. Morphol. 213, 185–195.

    Article  PubMed  CAS  Google Scholar 

  17. Marshall, J. A. and Dixon, K. E. (1978) Cell proliferation in the intestinal epithelium of Xenopus laevis tadpoles.J. Exp. Zool. 203, 31–40.

    Article  Google Scholar 

  18. McAvoy, J. W. and Dixon, K. E. (1978) Cell specialization in the small intestinal epithelium of adult Xenopus laevis: functional aspects.J. Anat. 125, 237–245.

    PubMed  CAS  Google Scholar 

  19. Gilbert, L. I., Tata, J. R. and Atkinson, B. G. (1996).Metamorphosis: Post-Embryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. Academic, New York.

    Google Scholar 

  20. Smith-Gill, S. J. and Carver, V. (1981) Biochemical characterization of organ differentiation and maturation, inMetamorphosis: A Problem in Developmental Biology (Gilber, L. I. and Friedan, E., eds.), Plenum, New York, pp. 491–544.

    Google Scholar 

  21. Ishizuya-Oka, A. and Shimozawa A. (1991) Induction of metamorphosis by thyroid hormone in anuran small intestine cultured organotypically in vitro.In Vitro Cell. Dev. Biol. 27A, 853–857.

    Article  PubMed  CAS  Google Scholar 

  22. Ishizuya-Oka, A. and Shimozawa, A. (1992) Connective tissue is involved in adult epithelial development of the small intestine during anuran metamorphosis in vitro.Roux’s Arch. Dev. Biol. 201, 322–329.

    Article  Google Scholar 

  23. Tata, J. R., Kawahara, A., and Baker B. S. (1991) Prolactin inhibits both thyroid hormone-induced morphogenesis and cell death in cultured amphibian larval tissues.Dev. Biol. 146, 72–80.

    Article  PubMed  CAS  Google Scholar 

  24. Mangelsdorf D. J., Thummel, C., Beato, M., Herrlich, P., Schutz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., and Evans, R. M. (1995) The nuclear receptor superfamily: the second decade.Cell 83, 835–839.

    Article  PubMed  CAS  Google Scholar 

  25. Shi, Y-B., Wong, J., and Puzianowska-Kuznicka, M. (1996) Thyroid hormone receptors: Mechanisms of transcriptional regulation and roles during frog development.J. Biomed. Sci. 3, 307–318.

    Article  PubMed  CAS  Google Scholar 

  26. Tsai, M.-J. and O’Malley, B. W. (1994) Molecular mechanisms of action of steroid/thyroid receptor superfamily members.Ann. Rev. Biochem. 63, 451–486.

    Article  PubMed  CAS  Google Scholar 

  27. Yen, P. M. and Chin, W. W. (1994) New advances in understanding the molecular mechanisms of thyroid hormone action.Trends Endocrinol. Metab. 5, 65–72.

    Article  CAS  PubMed  Google Scholar 

  28. Sap, J., Munoz, A., Damm, K., Goldberg, Y., Ghysdael, J., Leutz, A., Berg, H., and Vennstrom, B. (1986) The C-erb-A protein is a high affinity receptor for thyroid hormone.Nature 324, 635–640.

    Article  PubMed  CAS  Google Scholar 

  29. Weinberger, C., Thompson, C. C., Ong, E. S., Lebo, R., Gruol, D. J., and Evans, R. M. (1986) The c-erb-A gene encodes a thyroid hormone receptor.Nature 324, 641–646.

    Article  PubMed  CAS  Google Scholar 

  30. Shi, Y.-B. (1994) Molecular biology of amphibian metamorphosis: A new approach to an old problem.Trends Endocrinol. Metab. 5, 14–20.

    Article  CAS  PubMed  Google Scholar 

  31. Tata, J. R. (1993) Gene expression during metamorphosis: An ideal model for post-embryonic development.BioEssays 15, 239–248.

    Article  PubMed  CAS  Google Scholar 

  32. Mamajiwalla, S. N., Fath, K. R., and Burgess, D. R. (1992) Development of the chicken intestinal epithelium.Current Topics Dev. Biol. 26, 123–143.

    CAS  Google Scholar 

  33. Haffen, K., Lacroix, B., Kedinger, M., and Simon-Assmann, P. M. (1983) Inductive properties of fibroblastic cell cultures derived from rat intestinal mucosa on epithelial differentiation.Differentiation 23, 226–233.

    Article  PubMed  CAS  Google Scholar 

  34. Ishizuya-Oka, A. and Mizuno, T. (1984) Intestinal cytodifferentiation in vitro of chick stomach endoderm induced by the duodenal mesenchyme.J. Embryol. Exp. Morph. 82, 163–176.

    PubMed  CAS  Google Scholar 

  35. Ishizuya-Oka, A. and Mizuno, T. (1985) Chronological analysis of the intestinalization of chick stomach endoderm induced in vitro by duodenal mesenchyme.Roux’s Arch. Dev. Biol. 194, 301–305.

    Google Scholar 

  36. Kedinger, M., Simon-Assmann, P., Alexandre, E., and Haffen, K. (1987) Improtance of a fibrablastic support for in vitro differentiation of intestinal endodermal cells and for their response to glucocorticoids.Cell Differ.20, 171–182.

    Article  PubMed  CAS  Google Scholar 

  37. Stallmach, A., Hahn, U., Merker, H. J., Hahn, E. G., and Riecken, E. O. (1989) Differentiation of rat intestinal epithelial cells is induced by organotypic mesenchymal cells in vitro.Gut 30, 959–970.

    Article  PubMed  CAS  Google Scholar 

  38. Ishizuya-Oka, A. and Shimozawa, A. (1987) Ultrastructural changes in the intestinal connective tissue of Xenopus laevis during metamorphosis.J. Morphol. 193, 13–22.

    Article  PubMed  CAS  Google Scholar 

  39. Hay, E. D. (1991)Cell Biology of Extracellular Matrix, 2nd ed. Plenum, New York.

    Google Scholar 

  40. Timpl, R. and Brown, J. C. (1996) Supramolecular assembly of basement membranes.BioEssays 18, 123–132.

    Article  PubMed  CAS  Google Scholar 

  41. Ruoslahti, E. and Reed, J. C. (1994) Anchorage dependence, integrins, and apoptosis.Cell 77, 477–478.

    Article  PubMed  CAS  Google Scholar 

  42. Schmidt, J. W., Piepenhagen, P. A., and Nelson, W. J. (1993) Modulation of epithelial morphogenesis and cell fate by cell-to-cell signals and regulated cell adhesion.Sem. Cell Biol. 4, 161–173.

    Article  CAS  Google Scholar 

  43. Simon-Assmann, P., Duclos, B., Orian-Rousseau, V., Arnold, C., Mathelin, C., Engvali, E., and Kedinger, M. (1994) Differential expression of laminin isoforms and α6-β4 integrin subunits in the developing human and mouse intestine.Dev. Dynamics 201, 71–85.

    CAS  Google Scholar 

  44. Simo, P., Simon-Assmann, P., Bouzigos, F., Leberquier, C., Kedinger, M., Ekblom, P., and Sorokin, L. (1991) Changes in the expression of laminin during intestinal development.Development 112, 477–487.

    PubMed  CAS  Google Scholar 

  45. Bouziges, F., Simo, P., and Kedinger, M. (1991) Changes in glycosaminoglycan expression in the rat developing intestine.Cell Biol. Int. Rep. 152, 97–106.

    Article  Google Scholar 

  46. Altmann, G. G. and Quaroni, A. (1990) Behavior of fetal intestinal organ culture explanted onto a collagen substratum.Development 110, 5353–5370.

    Google Scholar 

  47. Simon-Assmann, P., Bouziges, F., Arnold, C., Haffen, K., and Kedinger, M. (1988) Epithelial-mesenchymal interactions in the production of the basement membrane components in the gut.Development 102 339–347.

    PubMed  CAS  Google Scholar 

  48. Kedinger M., Bouziges, F., Simon-Assmann, P., and Haffen, K. (1989) Influence of cell interactions on intestinal brush border enzyme expression, inHighlights Modern Biochem. vol. 2 (Kotyk, A., Skoda, J., Paces, V., and Kostka, V., eds.), VSP International, Zeist, pp. 1103–1112.

    Google Scholar 

  49. Simo, P., Simon-Assmann, P., Arnold, C., and Kedinger, M. (1992) Mesenchyme-mediated effect of dexamethasone on laminin in cocultures of embryonic gut epithelial cells and mesenchymederived cells.J. Cell. Sci. 101, 161–171.

    PubMed  CAS  Google Scholar 

  50. Murata, E. and Merker, H. J. (1991) Morphologic changes of the basal lamina in the small intestine of Xenopus laevis during metamorphosis.Acta Anat. 140, 60–69.

    PubMed  CAS  Google Scholar 

  51. Shi, Y.-B. and Brown, D. D. (1993) The earliest changes in gene expression in tadpole intestine induced by thyroid hormone.J. Biol. Chem. 268, 20,312–20,317.

    CAS  Google Scholar 

  52. Brown, D. D., Wang, Z., Furlow, J. D., Kanamori, A., Schwartzman, R. A., Rmo, B. F., and Pinder, A. (1996) The thyroid hormone-induced tail resorption program duringXenopus laevis metamorphosis.Proc. Natl. Acad. Sci. USA 93, 1924–1929.

    Article  PubMed  CAS  Google Scholar 

  53. Stolow, M. A. and Shi, Y.-B. (1995) Xenopus sonic hedgehog as a potential morphogen during embryogenesis and thyroid hormone-dependent metamorphosis.Nucleic Acids Res.23, 2555–2562.

    Article  PubMed  CAS  Google Scholar 

  54. Lee, J. J., von Kessler, D. P., Parks, S., and Beachy, P. A. (1992) Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog.Cell,71, 33–50.

    Article  PubMed  CAS  Google Scholar 

  55. Perrimon, N. (1995) Hedgehog and beyond.Cell 80, 517–520

    Article  PubMed  CAS  Google Scholar 

  56. Bumcrot, D. A. and McMahon, A. P. (1996)Current Biol. Sonic Signals Somites 5, 612–614.

    Article  Google Scholar 

  57. Ekker, S. C., McGrew, L. L., Lai, C.-J., Lee, J. J., von Kessler, D. P., Moon, R. T., and Beachy, P. A. (1995) Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis.Development 121, 2337–2347.

    PubMed  CAS  Google Scholar 

  58. Bitgood, M. J. and McMahon, A. P. (1995) Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo.Develop. Biol. 172, 126–138.

    Article  PubMed  CAS  Google Scholar 

  59. Capovilla, M., Brandt, M., and Botas, J. (1994) Direct regulation of decapentaglegic by ultrabithorax and its role in Drosophila midgut morphogenesis.Cell 76, 461–475.

    Article  PubMed  CAS  Google Scholar 

  60. Roberts, D. J., Johnson, R. L., Burke, A. C., Nelson, C. E., Morgan, B. A., and Tabin, C. (1995) Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut.Development 121, 3163–3174.

    PubMed  CAS  Google Scholar 

  61. Alexander, C. M. and Werb, Z. (1991) Extracellular matrix degradation, inCell Biology of Extracellular Matrix, 2nd ed. (Hay, E. D., ed.), Plenum, New York, pp. 255–302.

    Google Scholar 

  62. Birkedal-Hansen, H., Moore, W. G. I., Bodden, M. K., Windsor, L. J., Birkedal-Hansen, B., DeCarlo, A., and Engler, J. A. (1993) Matrix metalloproteinases: a review.Crit. Rev. Oral Biol. Med. 4(2), 197–250.

    PubMed  CAS  Google Scholar 

  63. Matrisian, L. M. (1992) The matrix-degrading metalloproteinases.Bioessays 14, 455–463.

    Article  PubMed  CAS  Google Scholar 

  64. Sang, Q. A. and Douglas, D. A. (1996) Computational sequence analysis of matrix metalloproteinases.J. Protein Chem. 15, 137–160.

    Article  PubMed  CAS  Google Scholar 

  65. Pei, D. and Weiss, S. J. (1995) Furin-dependent intracellular activation of the human stromelysin-3 zymogen.Nature 375, 244–247.

    Article  PubMed  CAS  Google Scholar 

  66. Stetler-Stevenson, W. G., Aznavoorian, S., and Liotta, L. A. (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis.Annu. Rev. Cell Biol. 9, 541–573.

    Article  PubMed  CAS  Google Scholar 

  67. Tryggvason, K., Hoyhtya, M., and Salo, T. (1987) Proteolytic degradation of extracellular matrix in tumor invasion.Biochim. Biophys. Acta 907, 191–217.

    PubMed  CAS  Google Scholar 

  68. Talhouk, R. S., Bissell, M. J., and Werb, Z. (1992) Coordinated expression of extracellular matrix-degrading proteinases and their inhibitors regulates mammary epithelial function during involution.J. Cell Biol. 118, 1271–1282.

    Article  PubMed  CAS  Google Scholar 

  69. Matrisian, L. M. and Hogan, B. L. M. (1990) Growth factor-regulated proteases and extracellular matrix remodeling during mammalian development.Current Topics in Dev. Biol. 24, 219–259.

    CAS  Google Scholar 

  70. Gross, J. (1966) How tadpoles lose their tails.J. Invest. Dermatol. 47, 274–277.

    Article  PubMed  CAS  Google Scholar 

  71. Oofusa, K., Yomori, S., and 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 

  72. Patterton, D., Hayes, W. P., and Shi, Y.-B. (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 

  73. Wang, Z. and Brown, D. D. (1993) Thyroid hormone-induced gene expression program for amphibian tail resorption.J. Biol. Chem. 268, 16,270–16,278.

    CAS  Google Scholar 

  74. Ishizuya-Oka, A., Ueda, S., and Shi, Y.-B. (1996) Transient expression of stromelysin-3 mRNA in the amphibian small intestine during metamorphosis.Cell Tissue Res. 283, 325–329.

    Article  PubMed  CAS  Google Scholar 

  75. Shi, Y.-B. and Hayes, W. P. (1994) Thyroid hormone-dependent regulation of the intestinal fatty acid-binding protein gene during amphibian metamorphosis.Dev. Biol. 161, 48–58.

    Article  PubMed  Google Scholar 

  76. Stolow, M. A., Bauzon, D. D., Li, J., Sedgwick, T., Liang, V. C.-T., Sang, Q. A., and Shi, Y.-B. (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 

  77. Lund, L. R., Romer, J., Thomasset, N., Solberg, H., Pyke, C., Bissell, M. J., Dono, K., and Werb, Z. (1996) Two distinct phases of apoptosis in mammary gland involution: proteinase-independent and-dependent pathways.Development 122, 181–193.

    PubMed  CAS  Google Scholar 

  78. Boudreau, N., Sympson, C. J., Werb, Z., and Bissell, M. J. (1995) Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix.Science 267, 891–893.

    Article  PubMed  CAS  Google Scholar 

  79. Roskelley, C. D., Srebrow, A., and Bissell, M. J. (1995) A hierarchy of ECM-mediated signalling regulates tissue-specific gene expression.Current Opin. Cell Biol. 7, 736–747.

    Article  CAS  Google Scholar 

  80. Bates, R. C., Buret, A., van Helden, D. F., Horton, M. A., and Burns, G. F. (1994) Apoptosis induced by inhibition of intercellular contact.J. Cell Biol. 125, 403–415.

    Article  PubMed  CAS  Google Scholar 

  81. Brooks, P. C., Montgomery, A. M. P., Rosenfeld, M., Reisfeld, R. A., Hu, T., Klier, G., and Cheresh, D. A. (1994) Integrin avβ3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels.Cell 79, 1157–1164.

    Article  PubMed  CAS  Google Scholar 

  82. Montgomery, A. M. P., Reisfeld, R. A., and Cheresh, D. A. (1994) Integrin αvβ3 rescues melanoma cells from apoptosis in three dimensional dermal collagen.Proc. Natl. Acad. Sci. USA 91, 8856–8860.

    Article  PubMed  CAS  Google Scholar 

  83. Brown, K. E. and Yamada, K. M. (1995) The role of integrins during vertebrate development.Sem. Dev. Biol. 6, 69–77.

    Article  CAS  Google Scholar 

  84. Damsky, C. H. and Werb, Z. (1992) Signal transduction by integrin receptors for extracellular matrix: cooperative processing of extracellular information.Current Biol. 4, 772–781.

    Article  CAS  Google Scholar 

  85. Werb, Z., Tremble, P. M., Behrendtsen, O., Crowley, E., and Damsky, C. (1989) Signal transduction through the fibronectin receptor induces collagenase and stromelysin gene expression.J. Cell Biol. 109, 877–889.

    Article  PubMed  CAS  Google Scholar 

  86. Roskelley, C. D., Desprez, P. Y., and Bissell, M. J. (1994) Extracellular matrix-dependent tissue-specific gene expression in mammary epithelial cells requires both physical and biochemical signal transduction.Proc. Natl. Acad. Sci. USA 91, 12,378–12,382.

    Article  CAS  Google Scholar 

  87. Alcedo, J., Ayzenzon, M., Von Ohlen, T., Noll, M., and Hooper, J. E. (1996) The Drosophila smoothened gene encodes a seven-pass membrane protein, a putative receptor for the hedgehog signal.Cell 86, 221–232.

    Article  PubMed  CAS  Google Scholar 

  88. Marigo, V., Davey, R. A., Zuo, Y., Cunningham, J. M., and Tabin, C. J. (1996) Biochemical evidence that patched is the hedgehog receptor.Nature 384, 176–179.

    Article  PubMed  CAS  Google Scholar 

  89. Stone, D. M., Hynes, M., Armanini, M., Swanson, T. A., Ku, O., Johnson, R. L., Scott, M. P., Pennica, D., Goddard, A., Phillips, H., Noll, M., Hooper, J. E., de Sauvage, F., and Rosenthal, A. (1996) The tumor-suppressor gene patched encodes a candidate receptor for sonic hedgehog.Nature 384, 129–134.

    Article  PubMed  CAS  Google Scholar 

  90. Van den Heuvel, M. and Ingham, P. W. (1996) Smoothened encodes a receptor-like serpentine protein required for hedgehog signaling.Nature 382, 547–551.

    Article  PubMed  Google Scholar 

  91. Lee, J. J., Ekker, S. C., von Kessler, D. P., Porter, J. A., Sun, B. I., and Beachy, P. A. (1994) Autoproteolysis in hedgehog protein biogenesis.Science 266, 1528–1537.

    Article  PubMed  CAS  Google Scholar 

  92. Tanaka Hall, T. M., Porter, J. A., Beachy, P. A., and Leahy, D. J. (1995) A potential catalytic site revealed by the 1.7-Å crystal structure of the amino-terminal signalling domain of sonic hedgehog.Nature 378, 212–216.

    Article  Google Scholar 

  93. Basset, P., Bellocq, J. P., Wolf, C., Stoll, I., Hutin, P., Limacher, J. M., Podhajcer, O. L., Chenard, M. P., Rio, M. C., and Chambon, P. (1990) A novel metalloproteinase gene specifically expressed in stromal cells of breast carcinomas.Nature 348, 699–704.

    Article  PubMed  CAS  Google Scholar 

  94. Pei, D., Majmudar, G., and Weiss, S. J. (1994) Hydrolytic inactivation of a breast carcinoma cell-derived serpin by human stromelysin-3.J. Biol. Chem. 269, 25,849–25,855.

    CAS  Google Scholar 

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Shi, YB. Cell-cell and cell-ECM interactions in epithelial apoptosis and cell renewal during frog intestinal development. Cell Biochem Biophys 27, 179–202 (1997). https://doi.org/10.1007/BF02738109

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