Enhancement of secretion of human procollagen I in mouse HSP47- expressing insect cells

Journal of Biochemistry

Volumn 126, Issue 6, 1999, Pages 1118-1126

  Tomita, Masahiro ^a,b,c   Yoshizato, Katsutoshi ^b,c   Nagata, Kazuhiro ^d   Kitajima, Takashi ^a  

^a TERUMO CORPORATION   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

Baculovirus expression system; Collagen secretion; HSP47; Recombinant collagen; Type I procollagen

Indexed keywords

COMPLEMENTARY DNA; HEAT SHOCK PROTEIN 47; PROCOLLAGEN; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; AUTORADIOGRAPHY; CONTROLLED STUDY; IMMUNOPRECIPITATION; LEPIDOPTERA; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN SECRETION;

ANIMALIA; INSECTA; LEPIDOPTERA; MAMMALIA; UNIDENTIFIED BACULOVIRUS;

EID: 0033376076     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a022557     Document Type: Article

References (50)

1. Kielty, C.M., Hopkinson, I., and Grant, M.E. (1993) Collagen: The collagen family: Structure, assembly, and organization in the extracellular matrix in Connective Tissue and Its Heritable Disorders: Molecular, Genetic and Medical Aspects (Royce, P.M. and Steinmann, B., eds.) pp. 103-147, Wiley-Liss, New York
2. Prockop, D.J. and Kivirikko, K.I. (1995) Collagens: Molecular biology, disease, and potentials for therapy. Annu. Rev. Biochem. 64, 403-434
3. Prockop, D.J., Berg, R.A., Kivirikko, K.I., and Uitto, J. (1976) Intracellular steps in the biosynthesis of collagen in Biochemistry of Collagen (Ramachandran, G.N. and Reddi, A.H., eds.) pp. 163-273, Plenum Press, New York
4. Kao, W.W.-Y., Prockop, D.J., and Berg, R.A. (1979) Kinetics for the secretion of nonhelical procollagen by freshly isolated tendon cells. J. Biol. Chem. 254, 2234-2243
5. Jimenez, S.A. and Yankowski, R. (1978) Role of molecular conformation on secretion of chick tendon procollagen. J. Biol. Chem. 253, 1420-1426
6. Nakai, A., Satoh, M., Hirayoshi, K., and Nagata, K. (1992) Involvement of the stress protein HSP47 in procollagen processing in the endoplasmic reticulum. J. Cell Biol. 117, 903-914
7. Smith, T., Ferreira, L.R., Hebert, C., Norris, K., and Sauk, J. (1995) Hsp47 and cyclophilin B traverse the endoplasmic reticulum with procollagen into pre-Golgi intermediate vesicles. J. Biol Chem. 270, 18323-18328
8. Natsume, T., Koide, T., Yokota, S., Hirayoshi, K., and Nagata, K. (1994) Interactions between collagen-binding stress protein HSP47 and collagen. J. Biol. Chem. 269, 31224-31228
9. Nagata, K., Saga, S., and Yamada, K.M. (1986) A major collagen binding protein of chick embryo fibroblasts is a novel heat shock protein. J. Cell Biol. 103, 223-229
10. Nagata, K. (1996) Hsp47: a collagen-specific molecular chaperone. Trends Biochem. Sci. 21, 23-26
11. Nakai, A., Hirayoshi, K., and Nagata, K. (1990) Transformation of BALB/3T3 cells by simian virus 40 causes a decreased synthesis of a collagen-binding heat-shock protein (hsp47). J. Biol. Chem. 265, 992-999
12. Satoh, M., Hirayoshi, K., Yokota, S., Hosokawa, N., and Nagata, K. (1996) Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen. J. Cell Biol. 133, 469-483
13. Nagata, K. and Hosokawa, N. (1996) Regulation and function of collagen-specific molecular chaperone, HSP47. Cell Struct. Funct. 21, 425-430
14. Tomita, M., Kitajima, T., and Yoshizato, K. (1997) Formation of recombinant human procollagen I heterotrimers in a baculovirus expression system. J. Biochem. 121, 1061-1069
15. Tomita, M., Ohkura, N., Ito, M., Royce, P.M., and Kitajima, T. (1995) Biosynthesis of recombinant human pro-α1(III) chains in a baculovirus expression system: production of disulphide-bonded and non-disulphide-bonded species containing full-length triple helices. Biochem. J. 312, 847-853
16. Lamberg, A., Helaakoski, T., Myllyharju, J., Peltonen, S., Notbohm, H., Pihlajaniemi, T., and Kivirikko, K.I. (1996) Characterization of human type III collagen expressed in a baculovirus system. J. Biol. Chem. 271, 11988-11995
17. Takechi, H., Hirayoshi, K., Nakai, A., Kudo, H., Saga, S., and Nagata, K. (1992) Molecular cloning of a mouse 47-kDa heatshock protein (HSP47), a collagen-binding stress protein, and its expression during the differentiation of F9 teratocarcinoma cells. Eur. J. Biochem. 206, 323-329
18. O'Reilly, D.R., Miller, L.K., and Luckow, V.A. (1992) Baculovirus Expression Vectors, W.H. Freeman, New York
19. Jarvis, D.L. and Summers, M.D. (1989) Glycosylation and secretion of human tissue plasminogen activator in recombinant baculovirus-infected insect cells. Mol. Cell. Biol. 9, 214-223
20. Leammli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
21. Hill-Perkins, M.S. and Possee, R.D. (1990) A baculovirus expression vector derived from the basic protein promoter of Autographa californica nuclear polyhedrosis virus. J. Gen. Virol. 71, 971-976
22. 14C]proto-collagen and its hydroxylation by prolylhydroxylase. Biochemistry 12, 3395-3401
23. Berg, R.A. and Prockop, D.J. (1973) The thermal transition of a non-hydroxylated form of collagen. Evidence for a role for hydroxyproline in stabilizing the triple-helix of collagen. Biochem. Biophys. Res. Commun. 52, 115-120
24. Jimenez, S., Harsch, M., and Rosenbloom, J. (1973) Hydroxyproline stabilizes the triple helix of chick tendon collagen. Biochem. Biophys. Res. Commun. 52, 106-114
25. Uitto, J., Dehm, P., and Prockop, D.J. (1972) Incorporation of cis-hydroxyproline into collagen by tendon cells. Failure of the intracellular collagen to assume a triple-helical conformation. Biochim. Biophys. Acta 278, 601-605
26. Lee, S.-T., Smith, B.D., and Greenspan, D.S. (1988) Construction of a full-length cDNA encoding human pro-α-2(I) collagen and its expression in pro-α2(I)-deficient W8 rat cells. J. Biol. Chem. 263, 13414-13418
27. Geddis, A.E. and Prockop, D.J. (1993) Expression of human COL1A1 gene in stably transfected HT1080 cells: The production of a thermostable homotrimer of type I collagen in a recombinant system. Matrix 13, 399-405
28. Nicholls, A.C., Osse, G., Schloon, H.G., Lenard, H.G., Deak, S., Myers, J.C., Prockop, D.J., Weigel, W.R.F., Fryer, P., and Pope, F.M. (1984) The clinical features of homozygous α2(I) collagen deficient osteogenesis imperfecta. J. Med. Genet. 21, 257-262
29. Deak, S.B., Nicholls, A., Pope, F.M., and Prockop, D.J. (1983) The molecular defect in a nonlethal variant of osteogenesis imperfecta. J. Biol. Chem. 258, 15192-15197
30. Deak, S.B., van der Rest, M., and Prockop, D.J. (1985) Altered helical structure of a homotrimer of α1(I)chains synthesized by fibroblasts from a variant of osteogenesis imperfecta. Collagen Rel. Res. 5, 305-313
31. Dickson, L.A., Pihlajaniemi, T., Deak, S., Pope, F.M., Nicholls, A., Prockop, D.J., and Myers, J.C. (1984) Nuclease S1 mapping of a homozygous mutation in the carboxyl-propeptide-coding region of the proa2(1) collagen gene in a patient with osteogenesis imperfecta. Proc. Natl. Acad. Sci. USA 81, 4524-4528
32. Schnieke, A., Dziadek, M., Bateman, J., Mascara, T., Harbers, K., Gelinas, R., and Jaenisch, R. (1987) Introduction of the human proα1(I) collagen gene into proα1(I)-deficient Mov-13 mouse cells leads to formation of functional mouse-human hybrid type I collagen. Proc. Natl. Acad. Sci. USA 84, 764-768
33. Tkocz, C. and Kühn, K. (1969) The formation of triple-helical collagen molecules from α1 or α2 polypeptide chains. Eur. J. Biochem. 7, 454-462
34. Hsu, T.-A. and Betenbaugh, M.J. (1997) Coexpression of molecular chaperone BiP improves immunoglobulin solubility and IgG secretion from Trichoplusia ni insect cells. Biotechnol. Prog. 13, 96-104
35. Kellokumpu, S., Suokas, M., Risteli, L., and Myllylä, R. (1997) Protein disulfide isomerase and newly synthesized procollagen chains form higher-order structures in the lumen of the endoplasmic reticulum. J. Biol. Chem. 272, 2770-2777
36. Mizuno, M. and Singer, S.J. (1993) A soluble secretory protein is first concentrated in the endoplasmic reticulum before transfer to the Golgi apparatus. Proc. Natl. Acad. Sci. USA 90, 5732-5736
37. Balch, W.E., McCaffery, J.M., Plutner, H., and Farquhar, M.G. (1994) Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 76, 841-852
38. Bednarek, S.Y., Ravazzola, M., Hosobuchi, M., Amherdt, M., Perrelet, A., Schekman, R., and Orci, L. (1995) COPI- and COPII coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell 83, 1183-1196
39. Rothman, J.E. and Wieland, F.T. (1996) Protein sorting by transport vesicles. Science 272, 227-234
40. Semenza, J,C., Hardwick, K.G., Dean, N., and Pelham, H.R.B. (1990) ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61, 1349-1357
41. Tang, B.L., Wong, S.H., Qi, X.L., Low, S.H., and Hong, W. (1993) Molecular cloning, characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor. J. Cell Biol. 120, 325-338
42. Henderson, J., Macdonald, H., Lazarus, C.M., Napier, R.M., and Hawes, C.R. (1996) Protein retention in the endoplasmic reticulum of insect cells is not compromised by baculovirus infection. Cell Biol. Int. 20, 413-422
43. Vuori, K., Pihlajaniemi, T., Myllylä, R., and Kivirikko, K.I. (1992) Site-directed mutagenesis of human protein disulfide isomerase: effect on the assembly, activity and endoplasmic reticulum retention of human prolyl 4-hydroxylase in Spodoptera frugiperda insect cells. EMBO J. 11, 4213-4217
44. Lamandé, S.R., Chessler, S.D., Golub, S.B., Byers, P.H., Chan, D., Cole, W.G., Sillence, D.O., and Bateman, J.F. (1995) Endoplasmic reticulum-mediated quality control of type I collagen production by cells from osteogenesis imperfecta patients with mutations in the proα1(I) chain carboxyl-terminal propeptide which impair subunit assembly. J. Biol. Chem. 270, 8642-8649
45. Hosokawa, N., Hohenadl, C., Satoh, M., Kühn, K., and Nagata, K. (1998) HSP47, a collagen-specific molecular chaperone, delays the secretion of type III procollagen transfected in human embryonic kidney cell line 293: a possible role for HSP47 in collagen modification. J. Biochem. 124, 654-662
46. Berg, R.A., Schwartz, M.L., and Crystal, R.G. (1980) Regulation of the production of secretory proteins: intracellular degradation of newly synthesized "defective" collagen. Proc. Natl. Acad. Sci. USA 77, 4746-4750
47. Kopito, R.R. (1997) ER quality control: the cytoplasmic connection. Cell 88, 427-430
48. Gething, M.-J. and Sambrook, J. (1992) Protein folding in the cell. Nature 355, 33-45
49. Bergeron, J.J.M., Brenner, M.B., Thomas, D.Y., and Williams, D.B. (1994) Calnexin: a membrane-bound chaperone of the endoplasmic reticulum. Trends Biochem. Sci. 19, 124-128
50. Chessler, S.D. and Byers, P.H. (1993) BiP binds type I procollagen proα chains with mutations in the carboxyl-terminal propeptide synthesized by cells from patients with osteogenesis imperfecta. J. Biol. Chem. 268, 18226-18233