Proprotein-processing endoprotease furin controls the growth and differentiation of gastric surface mucous cells

Journal of Clinical Investigation

Volumn 99, Issue 8, 1997, Pages 1842-1851

  Konda, Yoshitaka ^a   Yokota, Hiromi ^a   Kayo, Tsuyoshi ^a   Horiuchi, Tadashi ^b   Sugiyama, Norifumi ^b   Tanaka, Shigeyasu ^a   Takata, Kuniaki ^a   Takeuchi, Toshiyuki ^a  

^a GUNMA UNIVERSITY   (Japan)

^b DAIICHI SANKYO CO   (Japan)

Author keywords

cell growth; furin; gastric surface mucous cells; perodic acid Schiff positive materials; transforming growth factor

Indexed keywords

FURIN; PROTEIN PRECURSOR; PROTEINASE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN PROCESSING; SECRETORY GRANULE; STEM CELL; STOMACH MUCUS;

EID: 0030910371     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119351     Document Type: Article

References (53)

1. Karam, S.M., and C.P. Leblond. 1993. Dynamics of epithelial cells in the corpus of the mouse stomach. I. Identification of proliferative cell types and pinpointing of the stem cell. Anat. Rec. 236:259-279.
2. Karam, S.M., and C.P. Leblond. 1993. Dynamics of epithelial cells in the corpus of the mouse stomach. II. Outward migration of pit cells. Anat. Rec. 236: 280-296.
3. Boland, C.R., E.R. Kraus, J.M. Scheiman, C. Black, G.D. Deshmukh, and W.O. Dobbins III. 1990. Characterization of mucous cell synthetic functions in a new primary canine gastric mucous cell culture system. Am. J. Physiol. 258:G774-G787.
4. Goddard, P.J., Y.-C.J. Kao, and L.M. Lichtenberger. 1990. Luminal surface hydrophobicity of canine gastric mucosa is dependent on a surface mucous gel. Gastroenterology. 98:361-370.
5. Soll, A.H., D.A. Amirian, L.P. Thomas, T.J. Reedy, and J.D. Elashoff. 1984. Gatrin receptors on isolated canine parietal cells. J. Clin. Invest. 73:1434-1447.
6. Johnson, L.R. 1988. Regulation of gastrointestinal mucosal growth. Physiol. Rev. 68:456-502.
7. Allen, A., G. Flemstrom, A. Garner, and E. Kivilaakso. 1993. Gastroduodenal mucosal protection. Physiol. Rev. 73:823-857.
8. Kelly, S.M., and J.O. Hunter. 1990. Epidermal growth factor stimulates synthesis and secretion of mucus glycoproteins in human gastric mucosa. Clin. Sci. 79:425-427.
9. Beauchamp, R.D., J.A. Barnard, C.M. McCutchen, J.A. Cherner, and M. Renewal. 1989. Localization of transforming growth factor α and its receptor in gastric mucosal cells. J. Clin. Invest. 84:1017-1023.
10. Chen, M.C., A.T. Lee, and A.M. Soll. 1991. Mitogenic response of canine fundic epithelial cells in short-term culture to transfoming growth factor α and insulinlike growth factor I. J. Clin. Invest. 87:1716-1723.
11. Murayama, Y., J. Miyagawa, S. Higashiyama, S. Kondo, M. Yabu, K. Isozaki, Y. Kayanoki, S. Kanayama, Y. Shinomura, N. Taniguchi, and Y. Matsuzawa. 1995. Localization of heparin-binding epidermal growth factor-like growth factor in human gastric mucosa. Gastroenterology. 109:1051-1059.
12. Takahashi, M., S. Ota, T. Shimada, E. Hamada, T. Kawabe, T. Okudaira, M. Matsumura, N. Kaneko, A. Terano, T. Nakamura, and M. Omata. 1995. Hepatocyte growth factor is the most potent endogenous stimulant of rabbit gastric epithelial cell proliferation and migration in primary culture. J. Clin. Invest. 95:1994-2003.
13. Nasim, M.M., D.M. Thomas, M.R. Alison, and M.I. Filipe. 1992. Transforming growth factor α expression in normal gastric mucosa, intestinal metaplasia, dysplasia and gastric carcinoma-an immunohistochemical study. Histopathology (Oxf.). 20:339-343.
14. Thomas, D.M., M.M. Nasim, W.J. Gullick, and M.R. Alison. 1992. Immunoreactivity of transforming growth factor alpha in the normal adult gastrointestinal tract. Gut. 33:628-631.
15. Dempsey, P.J., J.R. Goldenring, C.J. Soroka, I.M. Modlin, R.W. McClure, C.D. Lind, D.A. Ahlquist, M.R. Pittelkow, D.C. Lee, E.P. Sandgren, et al. 1992. Possible role of transforming growth factor α in the pathogenesis of Ménétrier's disease: supportive evidence from humans and transgenic mice. Gastroenterology. 103:1950-1963.
16. Chen, M.C., A.T. Lee, W.E. Karnes, D. Avedian, M. Martin, J.M. Sorvillo, and A.H. Soll. 1993. Paracrine control of gastric epithelial cell growth in culture by transforming growth factor-α. Am. J. Physiol. 264:G390-G396.
17. Sottili, M., C. Sternini, N.C. Brecha, E. Lezoche, and J.H. Walsh. 1992. Transforming growth factor α receptor binding sites in the canine gastrointestinal tract. Gastroenterology. 103:1427-1436.
18. Rutten, M.J., P.J. Dempsey, C.A. Luttropp, M.A. Hawkey, B.C. Sheppard, R.A. Crass, C.W. Deveney, and R.J. Coffey. 1996. Identification of an EGF/TGF-α receptor in primary cultures of guinea pig gastric mucous epithelial cells. Am. J. Physiol. 270:G604-G612.
19. Terano, A., K.J. Ivey, J. Stachura, S. Sekhon, H. Hosojima, W.N. McKenzie, W.J. Krause, and J.H. Wyche. 1982. Cell culture of rat gastric fundic mucosa. Gastroenterology. 83:1280-1291.
20. 2. Gastroenterology. 84: 498-505.
21. Fukamachi, H., M. Ichinose, S. Ishihama, S. Tsukada, S. Yasugi, K. Shiokawa, C. Furihata, S. Yonezawa, and K. Miki. 1994. Fetal rat glandular stomach epithelial cells differentiate into surface mucous cells which express cathepsin E in the absence of mesenchymal cells in primary culture. Differentiation. 56:83-89.
22. Kayo, T., Y. Sawada, Y. Suzuki, M. Suda, S. Tanaka, Y. Konda, J. Miyazaki, and T. Takeuchi. 1996. Proprotein-processing endoprotease furin decreases regulated secretory pathway-specific proteins in the pancreatic β cell line MIN6. J. Biol. Chem. 271:10731-10737.
23. Frederiken, K., P.S. Jat, N. Valtz, D. Levy, and R. McKay. 1988. Immortalization of precursor cells from the mammalian CNS. Neuron. 1:439-448.
24. Jat, P.S., M.D. Noble, P. Ataliotis, Y. Tanaka, N. Yannoutsos, L. Larsen, and D. Kioussis. 1991. Direct derivation of conditonally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. USA. 88: 5096-5100.
25. Sugiyama, N., Y. Tabuchi, T. Horiuchi, M. Obinata, and M. Furusawa. 1993. Establishment of gastric surface mucous cell lines from transgenic mice harboring temperature-sensitive simian virus 40 large T-antigen gene. Exp. Cell Res. 209:382-387.
26. Tabuchi, Y., N. Sugiyama, T. Horiuchi, K. Furuhama, and M. Furusawa. 1996. Biological characterization of gastric surface mucous cell line GSM06 from transgenic mice harboring temperature-sensitive simian virus 40 large T-antigen gene. Digestion. 57:141-148.
27. Dohi, T., M. Nakasuji, K. Nakanishi, E. Yausgi, Y. Yuyama, N. Sugiyama, Y. Tabuchi, T. Horiuchi, and M. Oshima. 1996. Biochemical bases in differentiation of a mouse cell line GSN06 to gastric surface cells. Biochim. Biophys. Acta. 1289:71-78.
28. Bresnahan, P.A., R. Leduc, L. Thomas, J. Thorner, H.L. Gibson, A.J. Brake, P.J. Barr, and G. Thomas. 1990. Human fur gene encodes a yeast KEX2-like endoprotease that cleaves Pro-β-NGF in vivo. J. Cell Biol. 111:2851-2859.
29. Seidah, N.G., and M. Chrétien. 1992. Proprotein and prohormone convertases of the subtilisin family. Recent developments and future perspectives. Trends Endocrinol. Metab. 3:133-140.
30. Hatta, K., A. Nose, A. Nagafuchi, and M. Takcichi. 1988. Cloning and expression of cDNA encoding a neural calcium-dependent cell adhesion molecule: its identity in the cadherin gene family. J. Cell Biol. 106:873-881.
31. Marchand, P., J. Tang, G.D. Johnson, and J.S. Bond. 1995. COOH-terminal proteolytic processing of secreted and membrane forms of the α subunit of the metalloprotease meprin A. Requirement of the I domain for processing in the endoplasmic reticulum. J. Biol. Chem. 270:5449-5456.
32. Pei, D., and S.J. Weiss. 1995. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature (Lond.). 375:244-247.
33. Sato, H., T. Takino, Y. Okada, J. Cao, A. Shinagawa, E. Yamamoto, and M. Seiki. 1994. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature (Lond.). 370:61-65.
34. Tsuda, T., K. Yoshida, T. Tsujino, H. Nakayama, G. Kajiyama, and E. Tahara. 1989. Coexpression of platelet-derived growth factor (PDGF) A-chain and PDGF receptor genes in human gastric carcinomas. Jpn. J. Cancer Res. 80: 813-817.
35. Dubois, C.M., M.-H. Laprise, M.F. Blanchette, L.E. Gentry, and R. Leduc. 1995. Processing of transforming growth factor β1 precursor by human furin convertase. J. Biol. Chem. 270:10618-10624.
36. Bravo, D.A., J.B. Gleason, R.I. Sanchez, R.A. Roth, and R.S. Fuller. 1994. Accurate and efficient cleavage of the human insulin proreceptor by the human proprotein-processing protease furin. J. Biol. Chem. 269:25830-25837.
37. Komada, M., K. Hatsuzawa, S. Shibamoto, F. Ito, K. Nakayama, and N. Kitamura. 1993. Proteolytic processing of the hepatocyte growth factor/scatter factor receptor by furin. FEBS Lett. 328:25-29.
38. Sharp, R., M.W. Babyatsky, H. Takagi, S. Tagerud, T.C. Wang, D.E. Bockman, S.J. Brand, and G. Merlino. 1995. Transforming growth factor α disrupts the normal program of cellular differentiation in the gastric mucosa of transgenic mice. Development (Camb.). 121:149-161.
39. Kayo, T., Y. Konda, S. Tanaka, K. Takata, A. Koizumi, and T. Takeuchi. 1996. Developmental expression of proprotein-processing endoprotease furin in rat pancreatic islets. Endocrinology. 137:5126-5134.
40. Wijsman, J.H., J.-H. van Dierendonck, R. Keijzer, C.J.H. van de Velde, and C.J. Cornelisse. 1992. Immunoreactivity of proliferating cell nuclear antigen compared with bromodeoxyuridine incorporation in normal and neoplastic rat tissue. J. Pathol. 168:75-83.
41. Clark, G. 1981. Periodic acid leucofuchsin method. In Staining Procedures. G. Clark, editor. Williams and Wilkins Book Co., Baltimore, MD. 200-201.
42. Ishiyama, M., M. Shiga, K. Sasamoto, M. Mizoguchi, and P.G. He. 1993. A new sulfonated tetrazolium salt that produces a highly water-solubule formazan dye. Chem. Pharm. Bull. (Tokyo). 41:1118-1122.
43. Hatsuzawa, K., M., Hosaka, T. Nakagawa, M. Nagase, A. Shoda, K. Murakami, and K. Nakayama. 1990. Structure and expression of mouse furin, a yeast Kex2-related protease. J. Biol. Chem. 265:22075-22078.
44. van der Krol, A.R., J.N.M. Mol, and A.R. Stuitje. 1988. Modulation of eukaryotic gene expression by complementary RNA or DNA sequences. Biotechniques. 6:958-976.
45. Helander, H.F. 1969. Ultrastructure and function of gastric parietal cells in the rat during development. Gatroenterology. 56:35-52.
46. Helander, H.F. 1969. Ultrastructure and function of gastric mucoid and zymogen cells in the rat during development. Gatroenterology. 56:53-70.
47. Johnson, L.R. 1985. Functional development of the stomach. Annu. Rev. Physiol. 47:199-215.
48. Waga, S., and B. Stillman. 1994. Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature (Lond.). 369: 207-212.
49. Pandiella, A., and J. Massague. 1991. Cleavage of the membrane precursor for transforming growth factor alpha is a regulated process. Proc. Natl. Acad. Sci. USA. 88:1726-1730.
50. Molloy, S.S., L. Thomas, J.K. VanSlyke, P.E. Stenberg, and G. Thomas. 1994. Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO (Eur. Mol. Biol. Organ.) J. 13:18-33.
51. Takahashi, S., T. Nakagawa, T. Banno, T. Watanabe, K. Murakami, and K. Nakayama. 1995. Localization of furin to the trans-Golgi network and recycling from the cell surface involves Ser and Tyr residues within the cytoplasmic domain. J. Biol. Chem. 270:28397-28401.
52. Derynck, R., A.B. Roberts, M.E. Winkler, E. Y. Chen, and D.V. Goeddel. 1984. Human transforming growth factor-α: precursor structure and expression in E. coli. Cell. 38:287-297.
53. Hormi, K., J.-P. Onolfo, L. Gres, V. Lebraud, and T. Lehy. 1995. Developmental expression of transfoming growth factor-α in the upper digestive tract and pancreas of the rat. Regul. Pept. 55:67-77.