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and Noninvolvement of Diacylglycerol-Sensitive PKCs in Insulin-Stimulated Glucose Transport in L6 Myotubes1
J. A. Haley Veterans Hospital and the Departments of Internal Medicine and Biochemistry/Molecular Biology (G.B., M.L.S., L.G., R.V.F.), University of South Florida College of Medicine, Tampa, Florida 33612; and Centro de Biologia Molecular "Severo Ochoa" (J.M.), Universidad Autonoma, Canto Blanco, 28049 Madrid, Spain
Address all correspondence and requests for reprints to: Robert V. Farese, M.D., Research Service (VAR 151), J. A. Haley Veterans Hospital, 13000 Bruce Downs Boulevard, Tampa, Florida 33612.
We examined the question of whether insulin activates protein kinase C
(PKC)-
in L6 myotubes, and the dependence of this activation on
phosphatidylinositol (PI) 3-kinase. We also evaluated a number of
issues that are relevant to the question of whether diacylglycerol
(DAG)-dependent PKCs or DAG-insensitive PKCs, such as PKC-, are more
likely to play a role in insulin-stimulated glucose transport in L6
myotubes and other insulin-sensitive cell types. We found that insulin
increased the enzyme activity of immunoprecipitable PKC- in L6
myotubes, and this effect was blocked by PI 3-kinase inhibitors,
wortmannin and LY294002; this suggested that PKC- operates
downstream of PI 3-kinase during insulin action. We also found that
treatment of L6 myotubes with 5 µM tetradecanoyl
phorbol-13-acetate (TPA) for 24 h led to 80–100% losses of all
DAG-dependent PKCs (
, ß1, ß2, 
, 
)
and TPA-stimulated glucose transport (2-deoxyglucose uptake); in
contrast, there was full retention of PKC-, as well as
insulin-stimulated glucose transport and translocation of GLUT4 and
GLUT1 to the plasma membrane. Unlike what has been reported in BC3H-1
myocytes, TPA treatment did not elicit increases in PKCß2 messenger
RNA or protein in L6 myotubes, and selective retention of this PKC
isoform could not explain the retention of insulin effects on glucose
transport after prolonged TPA treatment. Of further interest, TPA
acutely activated membrane-associated PI 3-kinase in L6 myotubes, and
acute effects of TPA on glucose transport were inhibited, not only by
the PKC inhibitor, LY379196, but also by both wortmannin and LY294002;
this suggested that DAG-sensitive PKCs activate glucose transport
through cross-talk with phosphatidylinositol (PI) 3-kinase, rather than
directly through PKC. Also, the cell-permeable, myristoylated PKC-
pseudosubstrate inhibited insulin-stimulated glucose transport both in
non-down-regulated and PKC-depleted (TPA-treated) L6 myotubes; thus,
the PKC- pseudosubstrate appeared to inhibit a protein kinase that
is required for insulin-stimulated glucose transport but is distinct
from DAG-sensitive PKCs. In keeping with the latter dissociation of
DAG-sensitive PKCs and insulin-stimulated glucose transport, LY379196,
which inhibits PKC-ß (preferentially) and other DAG-sensitive PKCs at
relatively low concentrations, inhibited insulin-stimulated glucose
transport only at much higher concentrations, not only in L6 myotubes,
but also in rat adipocytes, BC3H-1 myocytes, 3T3/L1 adipocytes and rat
soleus muscles. Finally, stable and transient expression of a
kinase-inactive PKC- inhibited basal and insulin-stimulated glucose
transport in L6 myotubes. Collectively, our findings suggest that,
whereas PKC- is a reasonable candidate to participate in insulin
stimulation of glucose transport, DAG-sensitive PKCs are unlikely
participants.
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R. V. Farese Insulin-Sensitive Phospholipid Signaling Systems and Glucose Transport. Update II Experimental Biology and Medicine, April 1, 2001; 226(4): 283 - 295. [Abstract] [Full Text]
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G. Bandyopadhyay, Y. Kanoh, M. P. Sajan, M. L. Standaert, and R. V. Farese Effects of Adenoviral Gene Transfer of Wild-Type, Constitutively Active, and Kinase-Defective Protein Kinase C-{lambda} on Insulin-Stimulated Glucose Transport in L6 Myotubes Endocrinology, November 1, 2000; 141(11): 4120 - 4127. [Abstract] [Full Text] [PDF]
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P. Formisano, F. Oriente, F. Fiory, M. Caruso, C. Miele, M. A. Maitan, F. Andreozzi, G. Vigliotta, G. Condorelli, and F. Beguinot Insulin-Activated Protein Kinase Cbeta Bypasses Ras and Stimulates Mitogen-Activated Protein Kinase Activity and Cell Proliferation in Muscle Cells Mol. Cell. Biol., September 1, 2000; 20(17): 6323 - 6333. [Abstract] [Full Text]
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S.-F. Yan, J. Lu, Y. S. Zou, W. Kisiel, N. Mackman, M. Leitges, S. Steinberg, D. Pinsky, and D. Stern Protein Kinase C-beta and Oxygen Deprivation. A NOVEL Egr-1-DEPENDENT PATHWAY FOR FIBRIN DEPOSITION IN HYPOXEMIC VASCULATURE J. Biol. Chem., April 14, 2000; 275(16): 11921 - 11928. [Abstract] [Full Text] [PDF]
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L. Braiman, A. Alt, T. Kuroki, M. Ohba, A. Bak, T. Tennenbaum, and S. R. Sampson Protein Kinase C{delta} Mediates Insulin-Induced Glucose Transport in Primary Cultures of Rat Skeletal Muscle Mol. Endocrinol., December 1, 1999; 13(12): 2002 - 2012. [Abstract] [Full Text]
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L. M. NERI, A. M. MARTELLI, P. BORGATTI, M. L. COLAMUSSI, M. MARCHISIO, and S. CAPITANI Increase in nuclear phosphatidylinositol 3-kinase activity and phosphatidylinositol (3,4,5) trisphosphate synthesis precede PKC-{zeta} translocation to the nucleus of NGF-treated PC12 cells FASEB J, December 1, 1999; 13(15): 2299 - 2310. [Abstract] [Full Text]
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M. P. Sajan, M. L. Standaert, G. Bandyopadhyay, M. J. Quon, T. R. Burke Jr., and R. V. Farese Protein Kinase C-zeta and Phosphoinositide-dependent Protein Kinase-1 Are Required for Insulin-induced Activation of ERK in Rat Adipocytes J. Biol. Chem., October 22, 1999; 274(43): 30495 - 30500. [Abstract] [Full Text] [PDF]
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G. Bandyopadhyay, M. L. Standaert, M. P. Sajan, L. M. Karnitz, L. Cong, M. J. Quon, and R. V. Farese Dependence of Insulin-Stimulated Glucose Transporter 4 Translocation on 3-Phosphoinositide-Dependent Protein Kinase-1 and Its Target Threonine-410 in the Activation Loop of Protein Kinase C-{zeta} Mol. Endocrinol., October 1, 1999; 13(10): 1766 - 1772. [Abstract] [Full Text]
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M. L. Standaert, G. Bandyopadhyay, L. Galloway, J. Soto, Y. Ono, U. Kikkawa, R. V. Farese, and M. Leitges Effects of Knockout of the Protein Kinase C {beta} Gene on Glucose Transport and Glucose Homeostasis Endocrinology, October 1, 1999; 140(10): 4470 - 4477. [Abstract] [Full Text]
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L. Lavoie, C. J. Band, M. Kong, J. J. M. Bergeron, and B. I. Posner Regulation of Glycogen Synthase in Rat Hepatocytes. EVIDENCE FOR MULTIPLE SIGNALING PATHWAYS J. Biol. Chem., October 1, 1999; 274(40): 28279 - 28285. [Abstract] [Full Text] [PDF]
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M. L. Standaert, G. Bandyopadhyay, L. Perez, D. Price, L. Galloway, A. Poklepovic, M. P. Sajan, V. Cenni, A. Sirri, J. Moscat, et al. Insulin Activates Protein Kinases C-zeta and C-lambda by an Autophosphorylation-dependent Mechanism and Stimulates Their Translocation to GLUT4 Vesicles and Other Membrane Fractions in Rat Adipocytes J. Biol. Chem., September 3, 1999; 274(36): 25308 - 25316. [Abstract] [Full Text] [PDF]
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G. J. Etgen, K. M. Valasek, C. L. Broderick, and A. R. Miller In Vivo Adenoviral Delivery of Recombinant Human Protein Kinase C-zeta Stimulates Glucose Transport Activity in Rat Skeletal Muscle J. Biol. Chem., August 6, 1999; 274(32): 22139 - 22142. [Abstract] [Full Text] [PDF]
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B. Yu, L. A. Poirier, and L. E. Nagy Mobilization of GLUT-4 from intracellular vesicles by insulin and K+ depolarization in cultured H9c2 myotubes Am J Physiol Endocrinol Metab, August 1, 1999; 277(2): E259 - E267. [Abstract] [Full Text] [PDF]
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Q. Wang, R. Somwar, P. J. Bilan, Z. Liu, J. Jin, J. R. Woodgett, and A. Klip Protein Kinase B/Akt Participates in GLUT4 Translocation by Insulin in L6 Myoblasts Mol. Cell. Biol., June 1, 1999; 19(6): 4008 - 4018. [Abstract] [Full Text] [PDF]
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M. L. Standaert, G. Bandyopadhyay, M. P. Sajan, L. Cong, M. J. Quon, and R. V. Farese Okadaic Acid Activates Atypical Protein Kinase C (zeta /lambda ) in Rat and 3T3/L1 Adipocytes. AN APPARENT REQUIREMENT FOR ACTIVATION OF GLUT4 TRANSLOCATION AND GLUCOSE TRANSPORT J. Biol. Chem., May 14, 1999; 274(20): 14074 - 14078. [Abstract] [Full Text] [PDF]
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M. L. Standaert, G. Bandyopadhyay, E. K. Antwi, and R. V. Farese RO 31-8220 Activates c-Jun N-Terminal Kinase and Glycogen Synthase in Rat Adipocytes and L6 Myotubes. Comparison to Actions of Insulin Endocrinology, May 1, 1999; 140(5): 2145 - 2151. [Abstract] [Full Text]
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D. R. Tyson, J. T. Swarthout, and N. C. Partridge Increased Osteoblastic c-fos Expression by Parathyroid Hormone Requires Protein Kinase A Phosphorylation of the Cyclic Adenosine 3',5'-Monophosphate Response Element-Binding Protein at Serine 133 Endocrinology, March 1, 1999; 140(3): 1255 - 1261. [Abstract] [Full Text]
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J. J. Evans Modulation of Gonadotropin Levels by Peptides Acting at the Anterior Pituitary Gland Endocr. Rev., February 1, 1999; 20(1): 46 - 67. [Abstract] [Full Text]
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Z. A. Khayat, T. Tsakiridis, A. Ueyama, R. Somwar, Y. Ebina, and A. Klip Rapid stimulation of glucose transport by mitochondrial uncoupling depends in part on cytosolic Ca2+ and cPKC Am J Physiol Cell Physiol, December 1, 1998; 275(6): C1487 - C1497. [Abstract] [Full Text] [PDF]
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 Y. Izumi, T. Hirose, Y. Tamai, S.-i. Hirai, Y. Nagashima, T. Fujimoto, Y. Tabuse, K. J. Kemphues, and S. Ohno An Atypical PKC Directly Associates and Colocalizes at the Epithelial Tight Junction with ASIP, a Mammalian Homologue of Caenorhabditis elegans Polarity Protein PAR-3 J. Cell Biol., October 5, 1998; 143(1): 95 - 106. [Abstract] [Full Text] [PDF]
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Y. Kanoh, G. Bandyopadhyay, M. P. Sajan, M. L. Standaert, and R. V. Farese Thiazolidinedione Treatment Enhances Insulin Effects on Protein Kinase C-zeta /lambda Activation and Glucose Transport in Adipocytes of Nondiabetic and Goto-Kakizaki Type II Diabetic Rats J. Biol. Chem., May 26, 2000; 275(22): 16690 - 16696. [Abstract] [Full Text] [PDF]
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G. Bandyopadhyay, M. P. Sajan, Y. Kanoh, M. L. Standaert, T. R. Burke Jr., M. J. Quon, B. C. Reed, I. Dikic, L. E. Noel, C. B. Newgard, et al. Glucose Activates Mitogen-activated Protein Kinase (Extracellular Signal-regulated Kinase) through Proline-rich Tyrosine Kinase-2 and the Glut1 Glucose Transporter J. Biol. Chem., December 22, 2000; 275(52): 40817 - 40826. [Abstract] [Full Text] [PDF]
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N. A. Patel, C. E. Chalfant, J. E. Watson, J. R. Wyatt, N. M. Dean, D. C. Eichler, and D. R. Cooper Insulin Regulates Alternative Splicing of Protein Kinase C beta II through a Phosphatidylinositol 3-Kinase-dependent Pathway Involving the Nuclear Serine/Arginine-rich Splicing Factor, SRp40, in Skeletal Muscle Cells J. Biol. Chem., June 15, 2001; 276(25): 22648 - 22654. [Abstract] [Full Text] [PDF]
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F. Oriente, P. Formisano, C. Miele, F. Fiory, M. A. Maitan, G. Vigliotta, A. Trencia, S. Santopietro, M. Caruso, E. Van Obberghen, et al. Insulin Receptor Substrate-2 Phosphorylation Is Necessary for Protein Kinase Czeta Activation by Insulin in L6hIR Cells J. Biol. Chem., September 28, 2001; 276(40): 37109 - 37119. [Abstract] [Full Text] [PDF]
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