Skip to main content
Log in

The Functional Role of β Subunits in Oligomeric P-Type ATPases

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Na,K-ATPase and gastric and nongastric H,K-ATPases are the only P-type ATPases of higher organisms that are oligomeric and are associated with a β subunit, which is obligatory for expression and function of enzymes. Topogenesis studies suggest that β subunits have a fundamental and unique role in K+-transporting P-type ATPases in that they facilitate the correct membrane integration and packing of the catalytic α subunit of these P-type ATPases, which is necessary for their resistance to cellular degradation, their acquisition of functional properties, and their routing to the cell surface. In addition to this chaperone function, β subunits also participate in the determination of intrinsic transport properties of Na,K- and H,K-ATPases. Increasing experimental evidence suggests that β assembly is a highly ordered, β isoform-specific process, which is mediated by multiple interaction sites that contribute in a coordinate, multistep process to the structural and functional maturation of Na,K- and H,K-ATPases.

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.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  • Abriel, H., Hasler, U., Geering, K., and Horisberger, J. D. (1999). Biochim. Biophys. Acta 1418, 85-96.

    PubMed  Google Scholar 

  • Ackermann, U., and Geering, K. (1990). FEBS Lett. 269, 105-108.

    PubMed  Google Scholar 

  • Ackermann, U., and Geering, K. (1992). J. Biol. Chem. 267, 12911-12915.

    PubMed  Google Scholar 

  • Altendorf, K., and Epstein, W. (1994). Cell. Physiol. Biochem. 4, 160-168.

    Google Scholar 

  • Asano, S., Kimura, T., Ueno, S., Kawamura, M., and Takeguchi, N. (1999). J. Biol. Chem. 274, 22257-22265.

    PubMed  Google Scholar 

  • Asano, S., Kawada, K., Kimura, T., Grishin, A. V., Caplan, M. J., and Takeguchi, N. (2000). J. Biol. Chem. 275, 8324-8330.

    PubMed  Google Scholar 

  • Axelsen, K. B., and Palmgren, M. G. (1998). J. Mol. Evol. 46, 84-101.

    PubMed  Google Scholar 

  • Bamberg, K., and Sachs, G. (1994). J. Biol. Chem. 269, 16909-16919.

    PubMed  Google Scholar 

  • Bayle, D., Weeks, D., and Sachs, G. (1995). J. Biol. Chem. 270, 25678-25684.

    PubMed  Google Scholar 

  • Bayle, D., Wangler, S., Weitzenegger, T., Steinhilber, W., Volz, J., Przybylski, M., Schafer, K. P., Sachs, G., and Melchers, K. (1998). J. Bacteriol. 180, 317-329.

    PubMed  Google Scholar 

  • Beggah, A. T., Béguin, P., Jaunin, P., Peitsch, M. C., and Geering, K. (1993). Biochemistry 32, 14117-14124.

    PubMed  Google Scholar 

  • Beggah, A., Mathews, P., Béguin, P., and Geering, K. (1996). J. Biol. Chem. 271, 20895-20902.

    PubMed  Google Scholar 

  • Beggah, A. T., Jaunin, P., and Geering, K. (1997). J. Biol. Chem. 272, 10318-10326.

    PubMed  Google Scholar 

  • Beggah, A. T., Béguin, P., Bamberg, K., Sachs, G., and Geering, K. (1999). J. Biol. Chem. 274, 8217-8223.

    PubMed  Google Scholar 

  • Béguin, P., Hasler, U., Beggah, A., Horisberger, J. D., and Geering, K. (1998). J. Biol. Chem. 273, 24921-24931.

    PubMed  Google Scholar 

  • Béguin, P., Hasler, U., Staub, O., and Geering, K. (2000). Mol. Biol. Cell 11, 1657-1672.

    PubMed  Google Scholar 

  • Blanco, G., and Mercer, R.W. (1998). Amer. J. Physiol. 275, F633-F650.

    PubMed  Google Scholar 

  • Blobel, G. (1980). Proc. Natl. Acad. Sci. USA 77, 1496-1500.

    PubMed  Google Scholar 

  • Brosig, B., and Langosch, D. (1998). Protein Sci. 7, 1052-1056.

    PubMed  Google Scholar 

  • Burrow, C. R., Devuyst, O., Li, X., Gatti, L., and Wilson, P. D. (1999). Amer. J. Physiol. 277, F391-F403.

    PubMed  Google Scholar 

  • Caplan, M. J., Palade, G. E., and Jamieson, J. D. (1986). J. Biol. Chem. 261, 2860-2865.

    PubMed  Google Scholar 

  • Caplan, M. J., Forbush, B., Palade, G. E., and Jamieson, J. D. (1990). J. Biol. Chem. 265, 3528-3534.

    PubMed  Google Scholar 

  • Chen, P. X., Mathews, P. M., Good, P. J., Rossier, B. C., and Geering, K. (1998). Amer. J. Physiol. 44, C139-C145.

    Google Scholar 

  • Chow, D. C., and Forte, J. G. (1993). Amer. J. Physiol. 265, C1562-C1570.

    PubMed  Google Scholar 

  • Chow, D. C., and Forte, J. G. (1995). I. Exp. Biol. 198, 1-17.

    Google Scholar 

  • Chow, D. C., Browning, C. M., and Forte, J. G. (1992). Amer. J. Physiol. 263, C39-C46.

    PubMed  Google Scholar 

  • Codina, J., Kone, B. C., Delmasmata, J. T., and Dubose, T. D. (1996). J. Biol. Chem. 271, 29759-29763.

    PubMed  Google Scholar 

  • Codina, J., Delmas-Mata, J. T., and DuBose, T. J. (1998). J. Biol. Chem. 273, 7894-7899.

    PubMed  Google Scholar 

  • Colonna, T. E., Huynh, L., and Fambrough, D. M. (1997). J. Biol. Chem. 272, 12366-12372.

    PubMed  Google Scholar 

  • Cougnon, M., Planelles, G., Crowson, M. S., Shull, G. E., Rossier, B. C., and Jaisser, F. (1996). J. Biol. Chem. 271, 7277-7280.

    PubMed  Google Scholar 

  • Cougnon, M., Bouyer, P., Planelles, G., and Jaisser, F. (1998). Proc. Natl. Acad. Sci. USA 95, 6516-6520.

    PubMed  Google Scholar 

  • Cougnon, M., Bouyer, P., Jaisser, F., Edelman, A., and Planelles, G. (1999). Amer. J. Physiol. 277, C280-C287.

    PubMed  Google Scholar 

  • Courtois-Coutry, N., Roush, D., Rajendran, V., McCarthy, J. B., Geibel, J., Kashgarian, M., and Caplan, M. J. (1997). Cell 90, 501-551.

    PubMed  Google Scholar 

  • Crambert, G., Hasler, U., Beggah, A. T., Yu, C., Modyanov, N. N., Horisberger, J. D., Lelievre, L., and Geering, K. (2000). J. Biol. Chem. 275, 1976-1986.

    PubMed  Google Scholar 

  • Dalbey, R. E., Chen, M., Jiang, F., and Samuelson, J. C. (2000). Curr. Opinion Cell Biol. 12, 435-442.

    PubMed  Google Scholar 

  • Donnet, C., Arystarkhova, E., and Sweadner, K. J. (2001). J. Biol. Chem. 276, 7357-7365.

    PubMed  Google Scholar 

  • Eakle, K. A., Kim, K. S., Kabalin, M. A., and Farley, R. A. (1992). Proc. Natl. Acad. Sci. USA 89, 2834-2838.

    PubMed  Google Scholar 

  • Eakle, K. A., Kabalin, M. A., Wang, S. G., and Farley, R. A. (1994). J. Biol. Chem. 269, 6550-6557.

    PubMed  Google Scholar 

  • Eakle, K. A., Lyu, R. M., and Farley, R. A. (1995). J. Biol. Chem. 270, 13937-13947.

    PubMed  Google Scholar 

  • Ellgaard, L., Molinari, M., and Helenius, A. (1999). Science 286, 1882-1888.

    PubMed  Google Scholar 

  • Engelman, D. M., and Steitz T. A. (1981). Cell 23, 411-422.

    PubMed  Google Scholar 

  • Fink, A. L. (1999). Physiol. Rev. 79, 425-449.

    PubMed  Google Scholar 

  • Gatto, C., Wang, A. X., and Kaplan, J. H. (1998). J. Biol. Chem. 273, 10578-10585.

    PubMed  Google Scholar 

  • Geering, K. (1988). Progr. Clin. Biol. Res. 268 B, 19-33.

    Google Scholar 

  • Geering, K. (1998). Advan. Mol. Cell Biol. 23B, 275-309.

    Google Scholar 

  • Geering, K. (2000). J. Membr. Biol. 174, 181-190.

    PubMed  Google Scholar 

  • Geering, K., Meyers, D. I., Paccolat, M. P., Kraehenbuhl, J. P., and Rossier, B. C. (1985). J. Biol. Chem. 260, 5154-5160.

    PubMed  Google Scholar 

  • Geering, K., Kraehenbuhl, J.-P., and Rossier, B. C. (1987). J. Cell Biol. 105, 2613-2619.

    PubMed  Google Scholar 

  • Geering, K., Theulaz, I., Verrey, F., Häuptle, M. T., and Rossier, B. C. (1989). Amer. J. Physiol. 257, C851-C858.

    PubMed  Google Scholar 

  • Geering, K., Jaunin, P., Jaisser, F., Merillat, A. M., Horisberger, J. D., Mathews, P. M., Lemas, V., Fambrough, D. M., and Rossier, B. C. (1993). Amer. J. Physiol. 265, C1169-C1174.

    PubMed  Google Scholar 

  • Geering, K., Jaunin, P., Beggah, A., and Jaisser, F. (1994). In Molecular Mechanisms of H + Transport (Hirst, Barry H., ed.), Springer-Verlag, Berlin, pp. 63-69.

    Google Scholar 

  • Geering, K., Beggah, A., Good, P., Girardet, S., Roy, S., Schaer, D., and Jaunin, P. (1996). J. Cell Biol. 133, 1193-1204.

    PubMed  Google Scholar 

  • Geering, K., Crambert, G., Yu, C., Korneenko, T. V., Pestov, N. B., and Modyanov, N. N. (2000). Biochemistry 39, 12688-12698.

    PubMed  Google Scholar 

  • Gottardi, C. J., and Caplan, M. J. (1993). J. Biol. Chem. 268, 14342-14347.

    PubMed  Google Scholar 

  • Grishin, A. V., and Caplan, M. J. (1998). J. Biol. Chem. 273, 27772-2778.

    PubMed  Google Scholar 

  • Grishin, A. V., Bevensee, M. O., Modyanov, N. N., Rajendran,V., Boron, W. F., and Caplan, M. J. (1996). Amer. J. Physiol. 40, F539-F551.

    Google Scholar 

  • Hamrick, M., Renaud, K. J., and Fambrough, D. M. (1993). J. Biol. Chem. 268, 24367-24373.

    PubMed  Google Scholar 

  • Hasler, U., Wang, X., Crambert, G., Beguin, P., Jaisser, F., Horisberger, J. D., and Geering, K. (1998). J. Biol. Chem. 273, 30826-30835.

    PubMed  Google Scholar 

  • Hasler, U., Greasley, P. J., von Heijne, H. G., and Geering, K. (2000). J. Biol. Chem. 275, 29011-29022.

    PubMed  Google Scholar 

  • Hasler, U., Crambert, G., Horisberger, J.-D., and Geering, K. (2001). J. Biol. Chem. 276, 16356-16364.

    PubMed  Google Scholar 

  • Heinrich, S. U., Mothes, W., Brunner, J., and Rapoport, T. A. (2000). Cell 102, 233-244.

    PubMed  Google Scholar 

  • Hirsch, C., and Ploegh, H. L. (2000). Trends Cell Biol. 10, 268-272.

    PubMed  Google Scholar 

  • Horisberger, J. D., Jaunin, P., Reuben, M. A., Lasater, L. S., Chow, D. C., Forte, J. G., Sachs, G., Rossier, B. C., and Geering K. (1991). J. Biol. Chem. 266, 19131-19134.

    PubMed  Google Scholar 

  • Ivanov, A., Zhao, H., and Modyanov, N. N. (2000). Biochemistry 39, 9778-9785.

    PubMed  Google Scholar 

  • Jaisser, F., Jaunin, P., Geering, K., Rossier, B. C., and Horisberger, J. D. (1994). J. Gen. Physiol. 103, 605-623.

    PubMed  Google Scholar 

  • James, P. F., Grupp, I. L., Grupp, G., Woo, A. L., Askew, G. R., Croyle, M. L., Walsh, R. A., and Lingrel, J. B. (1999). Mol. Cell 3, 555-563.

    PubMed  Google Scholar 

  • Jaunin, P., Horisberger, J. D., Richter, K., Good, P. J., Rossier, B. C., and Geering, K. (1992). J. Biol. Chem. 267, 577-585.

    PubMed  Google Scholar 

  • Jaunin, P., Jaisser, F., Beggah, A. T., Takeyasu, K., Mangeat, P., Rossier, B. C., Horisberger, J. D., and Geering, K. (1993). J. Cell Biol. 123, 1751-1759.

    PubMed  Google Scholar 

  • Karlish, S. J. D., Goldshleger, R., and Stein, W. D. (1990). Proc. Natl. Acad. Sci. USA 87, 4566-4570.

    PubMed  Google Scholar 

  • Kawakami, K., and Nagano, K. (1988). J. Biochem. 103, 54-60.

    PubMed  Google Scholar 

  • Kawamura, M., and Nagano, K. (1984). Biochem. Biophys. Acta 774, 188-192.

    PubMed  Google Scholar 

  • Kirley, T. L. (1989). J. Biol. Chem. 264, 7185-7192.

    PubMed  Google Scholar 

  • Klaassen, C. H. W., Fransen, J. A. M., Swarts, H. G. P., and Depont, J. (1997). Biochem. J. 321, 419-424.

    PubMed  Google Scholar 

  • Koenderink, J. B., Swarts, H. G., Hermsen, H. P., and De Pont, J. J. (1999). J. Biol. Chem. 274, 11604-11610.

    PubMed  Google Scholar 

  • Kraut, J. A., Hiura, J., Shin, J. M., Smolka, A., Sachs, G., and Scott, D. (1998). Kidney Int. 53, 958-962.

    PubMed  Google Scholar 

  • Lemas, M. V., Yu, H-Y., Takeyasu, K., Kone, B., and Fambrough, D. M. (1994a). J. Biol. Chem. 269, 18651-18655.

    PubMed  Google Scholar 

  • Lemas, M. V., Hamrick, M., Takeyasu, K., and Fambrough, D. M. (1994b). J. Biol. Chem. 269, 8255-8259.

    PubMed  Google Scholar 

  • Lin, J., and Addison, R. (1995a). J. Biol. Chem. 270, 6935-6941.

    PubMed  Google Scholar 

  • Lin, J. L., and Addison, R. (1995b). J. Biol. Chem. 270, 6942-6948.

    PubMed  Google Scholar 

  • Lutsenko, S., and Kaplan, J. H. (1993). Biochemistry 32, 6737-6743.

    PubMed  Google Scholar 

  • Lutsenko, S., and Kaplan, J. H. (1994). J. Biol. Chem. 269, 4555-4564.

    PubMed  Google Scholar 

  • Lutsenko, S., and Kaplan, J. H. (1995). Biochemistry 34, 15607-15613.

    PubMed  Google Scholar 

  • Magyar, J. P., Bartsch, U., Wang, Z. Q., Howells, N., Aguzzi, A., Wagner, E. F., and Schachner, M. (1994). J. Cell Biol. 127, 835-845.

    PubMed  Google Scholar 

  • Melchers, K., Weitzenegger, T., Buhmann, A., Steinhilber, W., Sachs, G., and Schafer, K. P. (1996). J. Biol. Chem. 271, 446-457.

    PubMed  Google Scholar 

  • Melle-Milovanovic, D., Milovanovic, M., Nagpal, S., Sachs, G., and Shin, J. M. (1998). J. Biol. Chem. 273, 11075-11081.

    PubMed  Google Scholar 

  • Modyanov, N. N., Mathews, P. M., Grishin, A. V., Beguin, P., Beggah, A. T., Rossier, B. C., Horisberger, J. D., and Geering, K. (1995). Amer. J. Physiol. 38, C992-C997.

    Google Scholar 

  • Nilsson, I. M., and von Heijne, H. G. (1993). J. Biol. Chem. 268, 5798-5801.

    PubMed  Google Scholar 

  • Noguchi, S., Mishina, M., Kawamura, M., and Numa, S. (1987). FEBS Lett. 225, 27-32.

    PubMed  Google Scholar 

  • Noguchi, S., Higashi, K., and Kawamura, M. (1990). Biochim. Biophys. Acta 1023, 247-253.

    PubMed  Google Scholar 

  • Noguchi, S., Maeda, M., Futai, M., and Kawamura, M. (1992). Biochem. Biophys. Res. Commun. 182, 659-666.

    PubMed  Google Scholar 

  • Noguchi, S., Mutoh, Y., and Kawamura, M. (1994). FEBS Lett. 341, 233-238.

    PubMed  Google Scholar 

  • Okamoto, C. T., Chow, D. C., and Forte, A. J. (2000). Amer. J. Physiol. 278, C727-C738.

    Google Scholar 

  • Or, E., Goldshleger, R., and Karlish, S. J. (1999). J. Biol. Chem. 274, 2802-2809.

    PubMed  Google Scholar 

  • Reinhardt, J., Grishin, A. V., Oberleithner, H., and Caplan, M. J. (2000). Amer. J. Physiol. 279, F417-F425.

    Google Scholar 

  • Renaud, K. J., Inman, E. M., and Fambrough, D. M. (1991). J. Biol. Chem. 266, 20491-20497.

    PubMed  Google Scholar 

  • Sangan, P., Kolla, S. S., Rajendran, V. M., Kashgarian, M., and Binder, H. J. (1999). Amer. J. Physiol. 276, C350-C360.

    PubMed  Google Scholar 

  • Sangan, P., Thevananther, S., Sangan, S., Rajendran, V. M., and Binder, H. J. (2000). Amer. J. Physiol. 278, C182-C189.

    Google Scholar 

  • Schmalzing, G., Kroner, S., Schachner, M., and Gloor, S. (1992). J. Biol. Chem. 267, 20212-20216.

    PubMed  Google Scholar 

  • Schmalzing, G., Ruhl, K., and Gloor, S. M. (1997). Proc. Natl. Acad. Sci. USA 94, 1136-1141.

    PubMed  Google Scholar 

  • Schneider, H., and Scheiner-Bobis, G. (1997). J. Biol.Chem. 272, 16158-16165.

    PubMed  Google Scholar 

  • Sen Gupta, S., DeWitt N. D., Allen K. E., and Slayman C. W. (1998). J. Biol. Chem. 273, 34328-34334.

    PubMed  Google Scholar 

  • Shainskaya, A., and Karlish, S. J. D. (1996). J. Biol. Chem. 271, 10309-10316.

    PubMed  Google Scholar 

  • Shainskaya, A., Schneeberger, A., Apell, H. J., and Karlish, S. J. (2000). J. Biol. Chem. 275, 2019-2028.

    PubMed  Google Scholar 

  • Shimon, M. B., Goldshleger, R., and karlish, S. J. (1998). J. Biol. Chem. 273, 34190-34195.

    PubMed  Google Scholar 

  • Takeda, K., Noguchi, S., Sugino, A., and Kawamura, M. (1988). FEBS Lett. 238, 201-204.

    PubMed  Google Scholar 

  • Tamkun, M. M., and Fambrough, D. M. (1986). J. Biol. Chem. 261, 1009-1019.

    PubMed  Google Scholar 

  • Toyoshima, C., Nakasako, M., Nomura, H., and Ogawa, H. (2000). Nature (London) 405, 647-655.

    Google Scholar 

  • Tran, C. M., and Farley, R. A. (1999). Biophys. J. 77, 258-266.

    PubMed  Google Scholar 

  • Tyagarajan, K., Chow, D. C., Smolka, A., and Forte, J. G. (1995). Biochim. Biophys. Acta 1236, 105-113.

    PubMed  Google Scholar 

  • Ueno, S., Kusaba, M., Takeda, K., Maeda, M., Futai, M., Izumi, F., and Kawamura, M. (1995). J. Biochem. 117, 591-596.

    PubMed  Google Scholar 

  • Ueno, S., Takeda, K., Izumi, F., Futai, M., Schwarz,W., and Kawamura, M. (1997). Biochim. Biophys. Acta 1330, 217-224.

    PubMed  Google Scholar 

  • Wang, S. G., and Farley, R. A. (1998). J. Biol. Chem. 273, 29400-29405.

    PubMed  Google Scholar 

  • Wang, S. G., Eakle, K. A., Levenson, R., and Farley, R. A. (1997). Amer. J. Physiol. 41, C923-C930.

    Google Scholar 

  • Xie, Y. H., and Morimoto, T. (1995). J. Biol. Chem. 270, 11985-11991.

    PubMed  Google Scholar 

  • Zamofing, D., Rossier, B. C., and Geering, K. (1988). J. Membr. Biol. 104, 69-79.

    PubMed  Google Scholar 

  • Zamofing, D., Rossier, B. C., and Geering, K. (1989). Amer. J. Physiol. 256, C958-C966.

    PubMed  Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Geering, K. The Functional Role of β Subunits in Oligomeric P-Type ATPases. J Bioenerg Biomembr 33, 425–438 (2001). https://doi.org/10.1023/A:1010623724749

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010623724749

Navigation