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Volume 270, Number 5, Issue of February 3, 1995 pp. 2320-2326
©1995 by The American Society for Biochemistry and Molecular Biology, Inc.
Phosphorylation of Ribosomal Protein S6 Is Inhibitory for Autophagy in Isolated Rat Hepatocytes

(Received for publication, September 19, 1994; and in revised form, November 7, 1994)

Edward F. C. Blommaart ,  Joost J. F. P. Luiken ,  Pietjan J. E. Blommaart ,  George M. van Woerkom ,  Alfred J. Meijer

In rat hepatocytes, autophagy is known to be inhibited by amino acids. Insulin and cell swelling promote inhibition by amino acids. Each of the conditions leading to inhibition of autophagic proteolysis was found to be associated with phosphorylation of a 31-kDa protein that we identified as ribosomal protein S6. A combination of leucine, tyrosine, and phenylalanine, which efficiently inhibits autophagic proteolysis, was particularly effective in stimulating S6 phosphorylation. The relationship between the percentage inhibition of proteolysis and the degree of S6 phosphorylation was linear. Thus, inhibition of autophagy and phosphorylation of S6 are under the control of the same signal transduction pathway. Stimulation of S6 phosphorylation by the presence of amino acids was due to activation of S6 kinase and not to inhibition of S6 phosphatase.

The inhibition by amino acids of both autophagic proteolysis and autophagic sequestration of electro-injected cytosolic [^14C]sucrose was partially prevented by rapamycin, a compound known to inhibit activation of p70 S6 kinase. In addition, rapamycin partially inhibited the rate of protein synthesis.

We conclude that the fluxes through the autophagic and protein synthetic pathways are regulated in an opposite manner by the degree to which S6 is phosphorylated. Possible mechanisms by which S6 phosphorylation can cause inhibition of autophagy are discussed.



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T. C. Vary, L. S. Jefferson, and S. R. Kimball
Amino acid-induced stimulation of translation initiation in rat skeletal muscle
Am J Physiol Endocrinol Metab, December 1, 1999; 277(6): E1077 - E1086.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
P. Lipton
Ischemic Cell Death in Brain Neurons
Physiol Rev, October 1, 1999; 79(4): 1431 - 1568.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
S. O. Marx and A. R. Marks
Cell Cycle Progression and Proliferation Despite 4BP-1 Dephosphorylation
Mol. Cell. Biol., September 1, 1999; 19(9): 6041 - 6047.
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 J. Biol. Chem.Home page
T. Ueno, K. Ishidoh, R. Mineki, I. Tanida, K. Murayama, M. Kadowaki, and E. Kominami
Autolysosomal Membrane-associated Betaine Homocysteine Methyltransferase. LIMITED DEGRADATION FRAGMENT OF A SEQUESTERED CYTOSOLIC ENZYME MONITORING AUTOPHAGY
J. Biol. Chem., May 21, 1999; 274(21): 15222 - 15229.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. R. Kimball, L. M. Shantz, R. L. Horetsky, and L. S. Jefferson
Leucine Regulates Translation of Specific mRNAs in L6 Myoblasts through mTOR-mediated Changes in Availability of eIF4E and Phosphorylation of Ribosomal Protein S6
J. Biol. Chem., April 23, 1999; 274(17): 11647 - 11652.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Shigemitsu, Y. Tsujishita, K. Hara, M. Nanahoshi, J. Avruch, and K. Yonezawa
Regulation of Translational Effectors by Amino Acid and Mammalian Target of Rapamycin Signaling Pathways. POSSIBLE INVOLVEMENT OF AUTOPHAGY IN CULTURED HEPATOMA CELLS
J. Biol. Chem., January 8, 1999; 274(2): 1058 - 1065.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Y. Iiboshi, P. J. Papst, H. Kawasome, H. Hosoi, R. T. Abraham, P. J. Houghton, and N. Terada
Amino Acid-dependent Control of p70s6k. INVOLVEMENT OF tRNA AMINOACYLATION IN THE REGULATION
J. Biol. Chem., January 8, 1999; 274(2): 1092 - 1099.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. R. Kimball, R. L. Horetsky, and L. S. Jefferson
Implication of eIF2B Rather Than eIF4E in the Regulation of Global Protein Synthesis by Amino Acids in L6 Myoblasts
J. Biol. Chem., November 20, 1998; 273(47): 30945 - 30953.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
H. L. Fox, P. T. Pham, S. R. Kimball, L. S. Jefferson, and C. J. Lynch
Amino acid effects on translational repressor 4E-BP1 are mediated primarily by L-leucine in isolated adipocytes
Am J Physiol Cell Physiol, November 1, 1998; 275(5): C1232 - C1238.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. P. Feranchak, R. M. Roman, E. M. Schwiebert, and J. G. Fitz
Phosphatidylinositol 3-Kinase Contributes to Cell Volume Regulation through Effects on ATP Release
J. Biol. Chem., June 12, 1998; 273(24): 14906 - 14911.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. Hara, K. Yonezawa, Q.-P. Weng, M. T. Kozlowski, C. Belham, and J. Avruch
Amino Acid Sufficiency and mTOR Regulate p70 S6 Kinase and eIF-4E BP1 through a Common Effector Mechanism
J. Biol. Chem., June 5, 1998; 273(23): 14484 - 14494.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Noda and Y. Ohsumi
Tor, a Phosphatidylinositol Kinase Homologue, Controls Autophagy in Yeast
J. Biol. Chem., February 13, 1998; 273(7): 3963 - 3966.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
H. L. Fox, S. R. Kimball, L. S. Jefferson, and C. J. Lynch
Amino acids stimulate phosphorylation of p70S6k and organization of rat adipocytes into multicellular clusters
Am J Physiol Cell Physiol, January 1, 1998; 274(1): C206 - C213.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Ogier-Denis, A. Petiot, C. Bauvy, and P. Codogno
Control of the Expression and Activity of the Galpha -interacting Protein (GAIP) in Human Intestinal Cells
J. Biol. Chem., September 26, 1997; 272(39): 24599 - 24603.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Ogier-Denis, J.-J. Houri, C. Bauvy, and P. Codogno
Guanine Nucleotide Exchange on Heterotrimeric Gi3 Protein Controls Autophagic Sequestration in HT-29 Cells
J. Biol. Chem., November 8, 1996; 271(45): 28593 - 28600.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
U. Krause, M. H. Rider, and L. Hue
Protein Kinase Signaling Pathway Triggered by Cell Swelling and Involved in the Activation of Glycogen Synthase and Acetyl-CoA Carboxylase in Isolated Rat Hepatocytes
J. Biol. Chem., July 12, 1996; 271(28): 16668 - 16673.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Arico, A. Petiot, C. Bauvy, P. F. Dubbelhuis, A. J. Meijer, P. Codogno, and E. Ogier-Denis
The Tumor Suppressor PTEN Positively Regulates Macroautophagy by Inhibiting the Phosphatidylinositol 3-Kinase/Protein Kinase B Pathway
J. Biol. Chem., September 14, 2001; 276(38): 35243 - 35246.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Mordier, C. Deval, D. Bechet, A. Tassa, and M. Ferrara
Leucine Limitation Induces Autophagy and Activation of Lysosome-dependent Proteolysis in C2C12 Myotubes through a Mammalian Target of Rapamycin-independent Signaling Pathway
J. Biol. Chem., September 15, 2000; 275(38): 29900 - 29906.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
E. Ogier-Denis, S. Pattingre, J. El Benna, and P. Codogno
Erk1/2-dependent Phosphorylation of Galpha -interacting Protein Stimulates Its GTPase Accelerating Activity and Autophagy in Human Colon Cancer Cells
J. Biol. Chem., December 8, 2000; 275(50): 39090 - 39095.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
J. Rohde, J. Heitman, and M. E. Cardenas
The TOR Kinases Link Nutrient Sensing to Cell Growth
J. Biol. Chem., March 23, 2001; 276(13): 9583 - 9586.
[Abstract] [Full Text] [PDF]


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