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Originally published In Press as doi:10.1074/jbc.M103917200 on June 11, 2001

J. Biol. Chem., Vol. 276, Issue 35, 33027-33035, August 31, 2001
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Mechanisms of pH Regulation in the Regulated Secretory Pathway*

Minnie M. WuDagger §, Michael Grabe||, Stephen Adams**, Roger Y. Tsien**, Hsiao-Ping H. MooreDagger , and Terry E. MachenDagger Dagger Dagger

From the Dagger  Department of Molecular and Cell Biology, University of California, Berkeley, California 94720-3200, the  Department of Physics, University of California, Berkeley, California 94720-3112, and the ** Department of Pharmacology and Howard Hughes Medical Institute, University of California, San Diego, La Jolla, California 92093-0647

A precise pH gradient between organelles of the regulated secretory pathway is required for sorting and processing of prohormones. We studied pH regulation in live endocrine cells by targeting biotin-based pH indicators to cellular organelles expressing avidin-chimera proteins. In AtT-20 cells, we found that steady-state pH decreased from the endoplasmic reticulum (ER) (pHER = 7.4 ± 0.2, mean ± S.D.) to Golgi (pHG = 6.2 ± 0.4) to mature secretory granules (MSGs) (pHMSG = 5.5 ± 0.4). Golgi and MSGs required active H+ v-ATPases for acidification. ER, Golgi, and MSG steady-state pH values were also dependent upon the different H+ leak rates across each membrane. However, neither steady-state pHMSG nor rates of passive H+ leak were affected by Cl--free solutions or valinomycin, indicating that MSG membrane potential was small and not a determinant of pHMSG. Therefore, our data do not support earlier suggestions that organelle acidification is primarily regulated by Cl- conductances. Measurements of H+ leak rates, buffer capacities, and estimates of surface areas and volumes of these organelles were applied to a mathematical model to determine the H+ permeability (PH+) of each organelle membrane. We found that PH+ decreased progressively from ER to Golgi to MSGs, and proper acidification of Golgi and MSGs required gradual decreases in PH+ and successive increases in the active H+ pump density.

* This work was supported in part by National Institutes of Health Grants DK51799 (to T. E. M.) and R24RR14891 (to H.-P. H. M.) and National Science Foundation Grant MCB-9983342 (to H.-P. H. M. and T. E. M.).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ Supported by National Institutes of Health training grants.

|| Supported by National Science Foundation Grant DMS9220719.

Dagger Dagger To whom correspondence should be addressed: 231 Life Sciences Addition, University of California, Berkeley, CA 94720-3200. Tel.: 510-642-2983; Fax: 510-643-6791; E-mail: machen@socrates.berkeley.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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