Xenopus oocytes can secrete bacterial β-lactamase

Abstract

Most secretory proteins are synthesized as precursor polypeptides carrying N-terminal, Hydrophobie sequences which, by means of a signal recognition particle (SRP)1,3, trigger the membrane transfer of the polypeptide and are subsequently cleaved off. The signal sequences appear to be interchangeable between prokaryotes and eukaryotes4,5. In bacteria, secretion only involves the crossing of a membrane6, whereas in eukaryotes the secretory process can be separated into two distinct phases: translocation across the membrane of the rough endoplasmic retieulum and subsequent intraluminal transport by processes involving vesicle budding and fusion7. Since secretory proteins must be distinguished from other soluble proteins destined for various sites in the reticular system, it is conceivable that eukaryotic secretory proteins possess additional markers distinct from the signal peptide to guide the polypeptide after its transfer through the membrane. Proteins are secreted at different rates from a eukaryotic cell8,34, suggesting a role in intracellular transport for receptors with differing affinities for some topogenic features in secretory proteins. We have tested this possibility by introducing into the lumen of eukaryotic rough endoplasmic reticulum a prokaryotic protein which, by virtue of its origin, had not been adapted to the eukaryotic secretory pathway. We reasoned that secretion of the bacterial protein would indicate that after membrane transfer no topogenic signal(s) and corresponding recognition system(s) are required. We report here that this is indeed the case.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1

    Walter, P. & Blobel, G. J. Cell Biol. 91, 557–561 (1981).

  2. 2

    Walter, P. & Blobel, G. Nature 299, 691–698 (1982).

  3. 3

    Blobel, G. & Dobberstein, B. J. Cell Biol. 67, 852–862 (1975).

  4. 4

    Talmadge, K., Stahl, S. & Gilbert, W. Proc. natn. Acad. Sci. U.S.A. 77, 3369–3373 (1980).

  5. 5

    Müller, M., Ibrahimi, I., Chang, C. N., Walter, P. & Blobel, G. J. biol. Chem. 257, 11860–11863 (1982).

  6. 6

    Michaelis, S. & Beckwith, J. A. Rev. Microbiol. 36, 435–465 (1982).

  7. 7

    Palade, G. Science 189, 347–358 (1975).

  8. 8

    Strous, G. J. A. M. & Lodish, H. F. Cell 22, 709–717 (1980).

  9. 9

    Lane, C. D. Cell 24, 281–282 (1981).

  10. 10

    Huth, A., Rapoport, T. A. & Kääriäinen, L. EMBO J. 3, 767–771 (1984).

  11. 11

    Barnard, E. A., Miledi, R. & Sumikawa, K. Proc. R. Soc. B215, 241–246 (1982).

  12. 12

    Roberts, B. E. et al. Proc. natn. Acad. Sci. U.S.A. 72, 1922–1926 (1975).

  13. 13

    Contreras, R., Cheroutre, H. & Fiers, W. Nucleic Acids Res. 10, 6353–6362 (1982).

  14. 14

    Furuichi, Y., La Fiandra, A. & Shatkin, A. J. Nature 266, 235–239 (1977).

  15. 15

    Paterson, B. M. & Rosenberg, M. Nature 279, 692–696 (1979).

  16. 16

    Walter, P. & Blobel, G. Proc. natn. Acad. Sci. U.S.A. 77, 7112–7116 (1980).

  17. 17

    Roggenkamp, R., Kustermann-Kunn, B. & Hollenberg, C. P. Proc. natn. Acad. Sci. U.S.A. 78, 4466–4470 (1981).

  18. 18

    Lockard, R. E. & Lane, C. D. Nucleic Acids Res. 5, 3237–3247 (1978).

  19. 19

    Sykes, R. B. & Matthew, M. in Beta-Lactamases (eds Hamilton-Miller, J. M. T. & Smith, J. T.) 17–49 (Academic, New York, 1979).

  20. 20

    Eppig, J. J. Jr & Dumont, J. N. Devl Biol. 28, 531–536 (1972).

  21. 21

    Rapoport, T. A. Eur. J. Biochem. 115, 665–669 (1980).

  22. 22

    Colman, A. & Morser, J. Cell 17, 517–526 (1979).

  23. 23

    Hasilik, A. Trends biochem. Sci. 5, 237–240 (1980).

  24. 24

    Lane, C. D., Champion, J., Haiml, L. & Kreil, G. Eur. J. Biochem. 113, 273–281 (1981).

  25. 25

    Hurkman, W. J., Smith, L. D., Richter, J. & Larkins, B. A. J. Cell Biol. 89, 292–299 (1981).

  26. 26

    Walter, P., Ibrahimi, I. & Blobel, G. J. Cell Biol. 91, 545–550 (1981).

  27. 27

    Bolivar, F. et al. Gene 2, 95–113 (1977).

  28. 28

    Scheele, G. A. & Blackburn, P. Proc. natn. Acad. Sci. U.S.A. 76, 4898–4902 (1979).

  29. 29

    Pelham, H. R. B. & Jackson, R. J. Eur. J. Biochem. 67, 247–256 (1976).

  30. 30

    Gurdon, J. J. Embryol. exp. Morph. 20, 401–414 (1968).

  31. 31

    Soreq, H. & Miskin, R. FEBS Lett. 128, 305–310 (1981).

  32. 32

    Laemmli, U. K. Nature 277, 680–685 (1970).

  33. 33

    Bonner, W. M. & Laskey, R. A. Eur. J. Biochem. 46, 83–88 (1974).

  34. 34

    Lodish, H. F., Kong, N., Snider, M. & Strous, G. J. A. M. Nature 304, 80–83 (1983).

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wiedmann, M., Huth, A. & Rapoport, T. Xenopus oocytes can secrete bacterial β-lactamase. Nature 309, 637–639 (1984). https://doi.org/10.1038/309637a0

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.