Abstract
Muscle contraction acutely increases glucose transport in both healthy and type 2 diabetic individuals. Since glucose uptake during muscle contraction has been observed in the absence of insulin, the existence of an insulin-independent pathway has been suggested to explain this phenomenon. However, the exact mechanism behind the translocation of GLUT4 vesicles through the sarcolemma during muscle contraction is still unknown. Some substances, such as AMPK and calcium activated proteins, have been suggested as potential mediators but the exact mechanisms of their involvement remain to be elucidated. A hypothetical convergence point between the insulin cascade and the potential pathways triggered by muscle contraction has been suggested. Therefore, the earliest concept that two different routes exist in skeletal muscle has been progressively modified to the notion that glucose uptake is induced by muscle contraction via components of the insulin pathway. With further consideration, increased glucose uptake and enhanced insulin sensitivity observed during/after exercise might be explained by a metabolic- and calcium-dependent activation of several intermediate molecules of the insulin cascade. This paper aimed to review the literature in order to examine in detail these concepts behind muscle contraction-induced glucose uptake.
Key words
insulin - diabetes mellitus - GLUT4 - AS160 - aPKC
References
-
1
Ai H, Ralston E, Lauritzen H P, Galbo H, Ploug T.
Disruption of microtubules in rat skeletal muscle does not inhibit insulin- or contraction-stimulated glucose transport.
Am J Physiol.
2003;
285
E836-E844
-
2
American Diabetes Association .
Diagnosis and classification of diabetes mellitus.
Diabetes Care.
2006;
29 (Suppl 1)
S43-S48
-
3
Andreasson K, Galuska D, Thorne A, Sonnenfeld T, Wallberg-Henriksson H.
Decreased insulin-stimulated 3-0-methylglucose transport in in vitro incubated muscle strips from type II diabetic subjects.
Acta Physiol Scand.
1991;
142
255-260
-
4
Antonescu C N, Huang C, Niu W, Liu Z, Eyers P A, Heidenreich K A, Bilan P J, Klip A.
Reduction of insulin-stimulated glucose uptake in L6 myotubes by the protein kinase inhibitor SB203580 is independent of p38MAPK activity.
Endocrinology.
2005;
146
3773-3781
-
5
Bandyopadhyay G, Sajan M P, Kanoh Y, Standaert M L, Quon M J, Reed B C, Dikic I, Farese R V.
Glucose activates protein kinase C-zeta/lambda through proline-rich tyrosine kinase-2, extracellular signal-regulated kinase, and phospholipase D: a novel mechanism for activating glucose transporter translocation.
J Biol Chem.
2001;
276
35537-35545
-
6
Bandyopadhyay G, Standaert M L, Galloway L, Moscat J, Farese R V.
Evidence for involvement of protein kinase C (PKC)-zeta and noninvolvement of diacylglycerol-sensitive PKCs in insulin-stimulated glucose transport in L6 myotubes.
Endocrinology.
1997;
138
4721-4731
-
7
Beeson M, Sajan M P, Dizon M, Grebenev D, Gomez-Daspet J, Miura A, Kanoh Y, Powe J, Bandyopadhyay G, Standaert M L, Farese R V.
Activation of protein kinase C-zeta by insulin and phosphatidylinositol-3, 4, 5-(PO4)3 is defective in muscle in type 2 diabetes and impaired glucose tolerance: amelioration by rosiglitazone and exercise.
Diabetes.
2003;
52
1926-1934
-
8
Bobbert T, Wegewitz U, Brechtel L, Freudenberg M, Mai K, Mohlig M, Diederich S, Ristow M, Rochlitz H, Pfeiffer A F, Spranger J.
Adiponectin oligomers in human serum during acute and chronic exercise: relation to lipid metabolism and insulin sensitivity.
Int J Sports Med.
2007;
28
1-8
-
9
Brownlee M.
Biochemistry and molecular cell biology of diabetic complications.
Nature.
2001;
414
813-820
-
10
Brozinick Jr J T, Reynolds T H, Dean D, Cartee G, Cushman S W.
1-[N,O‐bis-(5-isoquinolinesulphonyl)-N-methyl-L-tyrosyl]-4-phenylpiperazine (KN‐62), an inhibitor of calcium-dependent camodulin protein kinase II, inhibits both insulin- and hypoxia-stimulated glucose transport in skeletal muscle.
Biochem J.
1999;
339 (Pt 3)
533-540
-
11
Bruss M D, Arias E B, Lienhard G E, Cartee G D.
Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity.
Diabetes.
2005;
54
41-50
-
12
Buhl E S, Jessen N, Pold R, Ledet T, Flyvbjerg A, Pedersen S B, Pedersen O, Schmitz O, Lund S.
Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome.
Diabetes.
2002;
51
2199-2206
-
13
Cartee G D, Holloszy J O.
Exercise increases susceptibility of muscle glucose transport to activation by various stimuli.
Am J Physiol.
1990;
258
E390-E393
-
14
Cauza E, Hanusch-Enserer U, Strasser B, Ludvik B, Kostner K, Dunky A, Haber P.
Continuous glucose monitoring in diabetic long distance runners.
Int J Sports Med.
2005;
26
774-780
-
15
Chang L, Chiang S H, Saltiel A R.
Insulin signaling and the regulation of glucose transport.
Mol Med.
2004;
10
65-71
-
16
Cheatham B, Vlahos C J, Cheatham L, Wang L, Blenis J, Kahn C R.
Phosphatidylinositol 3-kinase activation is required for insulin stimulation of pp70 S6 kinase, DNA synthesis, and glucose transporter translocation.
Mol Cell Biol.
1994;
14
4902-4911
-
17
Chen H C, Bandyopadhyay G, Sajan M P, Kanoh Y, Standaert M, Farese Jr R V, Farese R V.
Activation of the ERK pathway and atypical protein kinase C isoforms in exercise- and aminoimidazole-4-carboxamide-1-beta-D-riboside (AICAR)-stimulated glucose transport.
J Biol Chem.
2002;
277
23554-23562
-
18
Cleland P J, Appleby G J, Rattigan S, Clark M G.
Exercise-induced translocation of protein kinase C and production of diacylglycerol and phosphatidic acid in rat skeletal muscle in vivo. Relationship to changes in glucose transport.
J Biol Chem.
1989;
264
17704-17711
-
19
Coderre L, Kandror K V, Vallega G, Pilch P F.
Identification and characterization of an exercise-sensitive pool of glucose transporters in skeletal muscle.
J Biol Chem.
1995;
270
27584-27588
-
20
Corcoran E E, Means A R.
Defining Ca2+/calmodulin-dependent protein kinase cascades in transcriptional regulation.
J Biol Chem.
2001;
276
2975-2978
-
21
DeFronzo R A.
Pharmacologic therapy for type 2 diabetes mellitus.
Ann Intern Med.
1999;
131
281-303
-
22
Dentel J N, Blanchard S G, Ankrapp D P, McCabe L R, Wiseman R W.
Inhibition of cross-bridge formation has no effect on contraction-associated phosphorylation of p38 MAPK in mouse skeletal muscle.
Am J Physiol.
2005;
288
C824-C830
-
23
Derave W, Ai H, Ihlemann J, Witters L A, Kristiansen S, Richter E A, Ploug T.
Dissociation of AMP-activated protein kinase activation and glucose transport in contracting slow-twitch muscle.
Diabetes.
2000;
49
1281-1287
-
24
Deshmukh A, Coffey V G, Zhong Z, Chibalin A V, Hawley J A, Zierath J R.
Exercise-induced phosphorylation of the novel Akt substrates AS160 and filamin A in human skeletal muscle.
Diabetes.
2006;
55
1776-1782
-
25
Dolan P L, Tapscott E B, Dorton P J, Dohm G L.
Contractile activity restores insulin responsiveness in skeletal muscle of obese Zucker rats.
Biochem J.
1993;
289 (Pt 2)
423-426
-
26
Douen A G, Ramlal T, Rastogi S, Bilan P J, Cartee G D, Vranic M, Holloszy J O, Klip A.
Exercise induces recruitment of the “insulin-responsive glucose transporter”. Evidence for distinct intracellular insulin- and exercise-recruitable transporter pools in skeletal muscle.
J Biol Chem.
1990;
265
13427-13430
-
27
Dugani C B, Klip A.
Glucose transporter 4: cycling, compartments and controversies.
EMBO Rep.
2005;
6
1137-1142
-
28
Eguez L, Lee A, Chavez J A, Miinea C P, Kane S, Lienhard G E, McGraw T E.
Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein.
Cell Metab.
2005;
2
263-272
-
29
Fiedler M, Zierath J R, Selen G, Wallberg-Henriksson H, Liang Y, Sakariassen K S.
5-aminoimidazole-4-carboxy-amide-1-beta-D-ribofuranoside treatment ameliorates hyperglycaemia and hyperinsulinaemia but not dyslipidaemia in KKAy-CETP mice.
Diabetologia.
2001;
44
2180-2186
-
30
Fisher J S, Gao J, Han D H, Holloszy J O, Nolte L A.
Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin.
Am J Physiol.
2002;
282
E18-E23
-
31
Fujii N, Aschenbach W G, Musi N, Hirshman M F, Goodyear L J.
Regulation of glucose transport by the AMP-activated protein kinase.
Proc Nutr Soc.
2004;
63
205-210
-
32
Fujii N, Hirshman M F, Kane E M, Ho R C, Peter L E, Seifert M M, Goodyear L J.
AMP-activated protein kinase alpha2 activity is not essential for contraction- and hyperosmolarity-induced glucose transport in skeletal muscle.
J Biol Chem.
2005;
280
39033-39041
-
33
Fukunaga K, Yamamoto H, Saitoh Y, Ohta Y, Miyamoto E.
[Calmodulin and protein phosphorylation] Abstract.
Tanpakushitsu Kakusan Koso.
1988;
33
2102-2115
-
34
Furtado L M, Somwar R, Sweeney G, Niu W, Klip A.
Activation of the glucose transporter GLUT4 by insulin.
Biochem Cell Biol.
2002;
80
569-578
-
35
Goodyear L J, Giorgino F, Balon T W, Condorelli G, Smith R J.
Effects of contractile activity on tyrosine phosphoproteins and PI 3-kinase activity in rat skeletal muscle.
Am J Physiol.
1995;
268
E987-E995
-
36
Goodyear L J, Giorgino F, Sherman L A, Carey J, Smith R J, Dohm G L.
Insulin receptor phosphorylation, insulin receptor substrate-1 phosphorylation, and phosphatidylinositol 3-kinase activity are decreased in intact skeletal muscle strips from obese subjects.
J Clin Invest.
1995;
95
2195-2204
-
37
Griffin M E, Marcucci M J, Cline G W, Bell K, Barucci N, Lee D, Goodyear L J, Kraegen E W, White M F, Shulman G I.
Free fatty acid-induced insulin resistance is associated with activation of protein kinase C theta and alterations in the insulin signaling cascade.
Diabetes.
1999;
48
1270-1274
-
38
Haasch D, Berg C, Clampit J E, Pederson T, Frost L, Kroeger P, Rondinone C M.
PKC theta is a key player in the development of insulin resistance.
Biochem Biophys Res Commun.
2006;
343
361-368
-
39
Hajduch E, Litherland G J, Hundal H S.
Protein kinase B (PKB/Akt)–a key regulator of glucose transport?.
FEBS Lett.
2001;
492
199-203
-
40
Hannukainen J, Kalliokoski K K, Nuutila P, Fujimoto T, Kemppainen J, Viljanen T, Laaksonen M S, Parkkola R, Knuuti J, Kjaer M.
In vivo measurements of glucose uptake in human Achilles tendon during different exercise intensities.
Int J Sports Med.
2005;
26
727-731
-
41
Hardie D G.
New roles for the LKB1–>AMPK pathway.
Curr Opin Cell Biol.
2005;
17
167-173
-
42
Hardie D G, Carling D.
The AMP-activated protein kinase–fuel gauge of the mammalian cell?.
Eur J Biochem.
1997;
246
259-273
-
43
Hawley S A, Pan D A, Mustard K J, Ross L, Bain J, Edelman A M, Frenguelli B G, Hardie D G.
Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase.
Cell Metab.
2005;
2
9-19
-
44
Hayashi T, Hirshman M F, Kurth E J, Winder W W, Goodyear L J.
Evidence for 5′ AMP-activated protein kinase mediation of the effect of muscle contraction on glucose transport.
Diabetes.
1998;
47
1369-1373
-
45
Hayashi T, Wojtaszewski J F, Goodyear L J.
Exercise regulation of glucose transport in skeletal muscle.
Am J Physiol.
1997;
273
E1039-E1051
-
46
Helmrich S P, Ragland D R, Leung R W, Paffenbarger Jr R S.
Physical activity and reduced occurrence of non-insulin-dependent diabetes mellitus.
N Engl J Med.
1991;
325
147-152
-
47
Henriksen E J.
Invited review: effects of acute exercise and exercise training on insulin resistance.
J Appl Physiol.
2002;
93
788-796
-
48
Henriksen E J, Rodnick K J, Holloszy J O.
Activation of glucose transport in skeletal muscle by phospholipase C and phorbol ester. Evaluation of the regulatory roles of protein kinase C and calcium.
J Biol Chem.
1989;
264
21536-21543
-
49
Higaki Y, Hirshman M F, Fujii N, Goodyear L J.
Nitric oxide increases glucose uptake through a mechanism that is distinct from the insulin and contraction pathways in rat skeletal muscle.
Diabetes.
2001;
50
241-247
-
50
Ho R C, Alcazar O, Fujii N, Hirshman M F, Goodyear L J.
p38gamma MAPK regulation of glucose transporter expression and glucose uptake in L6 myotubes and mouse skeletal muscle.
Am J Physiol.
2004;
286
R342-R349
-
51
Ho R C, Fujii N, Witters L A, Hirshman M F, Goodyear L J.
Dissociation of AMP-activated protein kinase and p38 mitogen-activated protein kinase signaling in skeletal muscle.
Biochem Biophys Res Commun.
2007;
362
354-359
-
52
Hutber C A, Hardie D G, Winder W W.
Electrical stimulation inactivates muscle acetyl-CoA carboxylase and increases AMP-activated protein kinase.
Am J Physiol.
1997;
272
E262-E266
-
53
Iannello S, Camuto M, Cavaleri A, Milazzo P, Pisano M G, Bellomia D, Belfiore F.
Effects of short-term metformin treatment on insulin sensitivity of blood glucose and free fatty acids.
Diabetes Obes Metab.
2004;
6
8-15
-
54
Ihlemann J, Galbo H, Ploug T.
Calphostin C is an inhibitor of contraction, but not insulin-stimulated glucose transport, in skeletal muscle.
Acta Physiol Scand.
1999;
167
69-75
-
55
Imamura T, Huang J, Usui I, Satoh H, Bever J, Olefsky J M.
Insulin-induced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin.
Mol Cell Biol.
2003;
23
4892-4900
-
56
Ishizuka T, Cooper D R, Hernandez H, Buckley D, Standaert M, Farese R V.
Effects of insulin on diacylglycerol-protein kinase C signaling in rat diaphragm and soleus muscles and relationship to glucose transport.
Diabetes.
1990;
39
181-190
-
57
Jensen T E, Rose A J, Hellsten Y, Wojtaszewski J F, Richter E A.
Caffeine-induced Ca(2+) release increases AMPK-dependent glucose uptake in rodent soleus muscle.
Am J Physiol.
2007;
293
E286-E292
-
58
Jensen T E, Rose A J, Jorgensen S B, Brandt N, Schjerling P, Wojtaszewski J F, Richter E A.
Possible CaMKK-dependent regulation of AMPK phosphorylation and glucose uptake at the onset of mild tetanic skeletal muscle contraction.
Am J Physiol.
2007;
292
E1308-E1317
-
59
Jessen N, Goodyear L J.
Contraction signaling to glucose transport in skeletal muscle.
J Appl Physiol.
2005;
99
330-337
-
60
Jorgensen S B, Viollet B, Andreelli F, Frosig C, Birk J B, Schjerling P, Vaulont S, Richter E A, Wojtaszewski J F.
Knockout of the alpha2 but not alpha1 5′-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle.
J Biol Chem.
2004;
279
1070-1079
-
61
Kane S, Sano H, Liu S C, Asara J M, Lane W S, Garner C C, Lienhard G E.
A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain.
J Biol Chem.
2002;
277
22115-22118
-
62
Kanzaki M, Mora S, Hwang J B, Saltiel A R, Pessin J E.
Atypical protein kinase C (PKCzeta/lambda) is a convergent downstream target of the insulin-stimulated phosphatidylinositol 3-kinase and TC10 signaling pathways.
J Cell Biol.
2004;
164
279-290
-
63
Karlsson H K, Zierath J R, Kane S, Krook A, Lienhard G E, Wallberg-Henriksson H.
Insulin-stimulated phosphorylation of the Akt substrate AS160 is impaired in skeletal muscle of type 2 diabetic subjects.
Diabetes.
2005;
54
1692-1697
-
64
Karylowski O, Zeigerer A, Cohen A, McGraw T E.
GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes.
Mol Biol Cell.
2004;
15
870-882
-
65
Kemp B E, Stapleton D, Campbell D J, Chen Z P, Murthy S, Walter M, Gupta A, Adams J J, Katsis F, van Denderen B, Jennings I G, Iseli T, Michell B J, Witters L A.
AMP-activated protein kinase, super metabolic regulator.
Biochem Soc Trans.
2003;
31
162-168
-
66
Kingwell B A, Formosa M, Muhlmann M, Bradley S J, McConell G K.
Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects.
Diabetes.
2002;
51
2572-2580
-
67
Kishi K, Muromoto N, Nakaya Y, Miyata I, Hagi A, Hayashi H, Ebina Y.
Bradykinin directly triggers GLUT4 translocation via an insulin-independent pathway.
Diabetes.
1998;
47
550-558
-
68
Kotani K, Ogawa W, Matsumoto M, Kitamura T, Sakaue H, Hino Y, Miyake K, Sano W, Akimoto K, Ohno S, Kasuga M.
Requirement of atypical protein kinase c lambda for insulin stimulation of glucose uptake but not for Akt activation in 3T3-L1 adipocytes.
Mol Cell Biol.
1998;
18
6971-6982
-
69
Kramer H F, Witczak C A, Fujii N, Jessen N, Taylor E B, Arnolds D E, Sakamoto K, Hirshman M F, Goodyear L J.
Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle.
Diabetes.
2006;
55
2067-2076
-
70
Kumar N, Dey C S.
Metformin enhances insulin signalling in insulin-dependent and-independent pathways in insulin resistant muscle cells.
Br J Pharmacol.
2002;
137
329-336
-
71
Kurth-Kraczek E J, Hirshman M F, Goodyear L J, Winder W W.
5′ AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle.
Diabetes.
1999;
48
1667-1671
-
72
Lemieux K, Konrad D, Klip A, Marette A.
The AMP-activated protein kinase activator AICAR does not induce GLUT4 translocation to transverse tubules but stimulates glucose uptake and p38 mitogen-activated protein kinases alpha and beta in skeletal muscle.
Faseb J.
2003;
17
1658-1665
-
73
Leng Y, Steiler T L, Zierath J R.
Effects of insulin, contraction, and phorbol esters on mitogen-activated protein kinase signaling in skeletal muscle from lean and ob/ob mice.
Diabetes.
2004;
53
1436-1444
-
74
Litherland G J, Hajduch E, Hundal H S.
Intracellular signalling mechanisms regulating glucose transport in insulin-sensitive tissues (review).
Mol Membr Biol.
2001;
18
195-204
-
75
Long Y C, Zierath J R.
Fine-tuning insulin and nitric oxide signalling by turning up the AMPs: new insights into AMP-activated protein kinase signalling.
Diabetologia.
2005;
48
2451-2453
-
76
Luna V, Casauban L, Sajan M P, Gomez-Daspet J, Powe J L, Miura A, Rivas J, Standaert M L, Farese R V.
Metformin improves atypical protein kinase C activation by insulin and phosphatidylinositol-3,4,5-(PO4)3 in muscle of diabetic subjects.
Diabetologia.
2006;
49
375-382
-
77
Moller D E.
New drug targets for type 2 diabetes and the metabolic syndrome.
Nature.
2001;
414
821-827
-
78
Mu J, Brozinick Jr J T, Valladares O, Bucan M, Birnbaum M J.
A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle.
Mol Cell.
2001;
7
1085-1094
-
79
Musi N, Fujii N, Hirshman M F, Ekberg I, Froberg S, Ljungqvist O, Thorell A, Goodyear L J.
AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise.
Diabetes.
2001;
50
921-927
-
80
Musi N, Goodyear L J.
AMP-activated protein kinase and muscle glucose uptake.
Acta Physiol Scand.
2003;
178
337-345
-
81
Musi N, Hirshman M F, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O, Zhou G, Williamson J M, Ljunqvist O, Efendic S, Moller D E, Thorell A, Goodyear L J.
Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes.
Diabetes.
2002;
51
2074-2081
-
82
Musi N, Yu H, Goodyear L J.
AMP-activated protein kinase regulation and action in skeletal muscle during exercise.
Biochem Soc Trans.
2003;
31
191-195
-
83
Nesher R, Karl I E, Kipnis D M.
Dissociation of effects of insulin and contraction on glucose transport in rat epitrochlearis muscle.
Am J Physiol.
1985;
249
C226-C232
-
84
Newton A C.
Protein kinase C: structure, function, and regulation.
J Biol Chem.
1995;
270
28495-28498
-
85
Nielsen J N, Frosig C, Sajan M P, Miura A, Standaert M L, Graham D A, Wojtaszewski J F, Farese R V, Richter E A.
Increased atypical PKC activity in endurance-trained human skeletal muscle.
Biochem Biophys Res Commun.
2003;
312
1147-1153
-
86
O'Gorman D J, Del Aguila L F, Williamson D L, Krishnan R K, Kirwan J P.
Insulin and exercise differentially regulate PI3-kinase and glycogen synthase in human skeletal muscle.
J Appl Physiol.
2000;
89
1412-1419
-
87
Ojuka E O.
Role of calcium and AMP kinase in the regulation of mitochondrial biogenesis and GLUT4 levels in muscle.
Proc Nutr Soc.
2004;
63
275-278
-
88
Okada T, Kawano Y, Sakakibara T, Hazeki O, Ui M.
Essential role of phosphatidylinositol 3-kinase in insulin-induced glucose transport and antilipolysis in rat adipocytes. Studies with a selective inhibitor wortmannin.
J Biol Chem.
1994;
269
3568-3573
-
89
Olson E N, Williams R S.
Remodeling muscles with calcineurin.
Bioessays.
2000;
22
510-519
-
90
Ostenson C G.
The pathophysiology of type 2 diabetes mellitus: an overview.
Acta Physiol Scand.
2001;
171
241-247
-
91
Peltoniemi P, Yki-Jarvinen H, Oikonen V, Oksanen A, Takala T O, Ronnemaa T, Erkinjuntti M, Knuuti M J, Nuutila P.
Resistance to exercise-induced increase in glucose uptake during hyperinsulinemia in insulin-resistant skeletal muscle of patients with type 1 diabetes.
Diabetes.
2001;
50
1371-1377
-
92
Perrini S, Henriksson J, Zierath J R, Widegren U.
Exercise-induced protein kinase C isoform-specific activation in human skeletal muscle.
Diabetes.
2004;
53
21-24
-
93
Rasmussen B B, Winder W W.
Effect of exercise intensity on skeletal muscle malonyl-CoA and acetyl-CoA carboxylase.
J Appl Physiol.
1997;
83
1104-1109
-
94
Ribe D, Yang J, Patel S, Koumanov F, Cushman S W, Holman G D.
Endofacial competitive inhibition of glucose transporter-4 intrinsic activity by the mitogen-activated protein kinase inhibitor SB203580.
Endocrinology.
2005;
146
1713-1717
-
95
Richter E A, Garetto L P, Goodman M N, Ruderman N B.
Muscle glucose metabolism following exercise in the rat: increased sensitivity to insulin.
J Clin Invest.
1982;
69
785-793
-
96
Richter E A, Mikines K J, Galbo H, Kiens B.
Effect of exercise on insulin action in human skeletal muscle.
J Appl Physiol.
1989;
66
876-885
-
97
Richter E A, Nielsen J N, Jorgensen S B, Frosig C, Birk J B, Wojtaszewski J F.
Exercise signalling to glucose transport in skeletal muscle.
Proc Nutr Soc.
2004;
63
211-216
-
98
Rose A J, Michell B J, Kemp B E, Hargreaves M.
Effect of exercise on protein kinase C activity and localization in human skeletal muscle.
J Physiol.
2004;
561
861-870
-
99
Ryder J W, Chibalin A V, Zierath J R.
Intracellular mechanisms underlying increases in glucose uptake in response to insulin or exercise in skeletal muscle.
Acta Physiol Scand.
2001;
171
249-257
-
100
Sakamoto K, Goransson O, Hardie D G, Alessi D R.
Activity of LKB1 and AMPK-related kinases in skeletal muscle: effects of contraction, phenformin, and AICAR.
Am J Physiol.
2004;
287
E310-E317
-
101
Saltiel A R, Kahn C R.
Insulin signalling and the regulation of glucose and lipid metabolism.
Nature.
2001;
414
799-806
-
102
Sigal R J, Kenny G P, Wasserman D H, Castaneda-Sceppa C.
Physical activity/exercise and type 2 diabetes.
Diabetes Care.
2004;
27
2518-2539
-
103
Somwar R, Perreault M, Kapur S, Taha C, Sweeney G, Ramlal T, Kim D Y, Keen J, Cote C H, Klip A, Marette A.
Activation of p38 mitogen-activated protein kinase alpha and beta by insulin and contraction in rat skeletal muscle: potential role in the stimulation of glucose transport.
Diabetes.
2000;
49
1794-1800
-
104
Soos M A, Jensen J, Brown R A, O'Rahilly S, Shepherd P R, Whitehead J P.
Class II phosphoinositide 3-kinase is activated by insulin but not by contraction in skeletal muscle.
Arch Biochem Biophys.
2001;
396
244-248
-
105
Sriwijitkamol A, Coletta D K, Wajcberg E, Balbontin G B, Reyna S M, Barrientes J, Eagan P A, Jenkinson C P, Cersosimo E, DeFronzo R A, Sakamoto K, Musi N.
Effect of acute exercise on AMPK signaling in skeletal muscle of subjects with type 2 diabetes: a time-course and dose-response study.
Diabetes.
2007;
56
836-848
-
106
Stapleton D, Mitchelhill K I, Gao G, Widmer J, Michell B J, Teh T, House C M, Fernandez C S, Cox T, Witters L A, Kemp B E.
Mammalian AMP-activated protein kinase subfamily.
J Biol Chem.
1996;
271
611-614
-
107
Sweeney G, Somwar R, Ramlal T, Volchuk A, Ueyama A, Klip A.
An inhibitor of p38 mitogen-activated protein kinase prevents insulin-stimulated glucose transport but not glucose transporter translocation in 3T3-L1 adipocytes and L6 myotubes.
J Biol Chem.
1999;
274
10071-10078
-
108
Tanti J F, Grillo S, Gremeaux T, Coffer P J, Van Obberghen E, Le Marchand-Brustel Y.
Potential role of protein kinase B in glucose transporter 4 translocation in adipocytes.
Endocrinology.
1997;
138
2005-2010
-
109
Taylor E B, Ellingson W J, Lamb J D, Chesser D G, Winder W W.
Long-chain acyl-CoA esters inhibit phosphorylation of AMP-activated protein kinase at threonine-172 by LKB1/STRAD/MO25.
Am J Physiol.
2005;
288
E1055-E1061
-
110
Thong F S, Bilan P J, Klip A.
The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic.
Diabetes.
2007;
56
414-423
-
111
Tomas E, Zorzano A, Ruderman N B.
Exercise and insulin signaling: a historical perspective.
J Appl Physiol.
2002;
93
765-772
-
112
Treebak J T, Glund S, Deshmukh A, Klein D K, Long Y C, Jensen T E, Jorgensen S B, Viollet B, Andersson L, Neumann D, Wallimann T, Richter E A, Chibalin A V, Zierath J R, Wojtaszewski J F.
AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits.
Diabetes.
2006;
55
2051-2058
-
113
Wallberg-Henriksson H, Constable S H, Young D A, Holloszy J O.
Glucose transport into rat skeletal muscle: interaction between exercise and insulin.
J Appl Physiol.
1988;
65
909-913
-
114
Wang Q, Somwar R, Bilan P J, Liu Z, Jin J, Woodgett J R, Klip A.
Protein kinase B/Akt participates in GLUT4 translocation by insulin in L6 myoblasts.
Mol Cell Biol.
1999;
19
4008-4018
-
115
Whitehead J P, Soos M A, Aslesen R, O'Rahilly S, Jensen J.
Contraction inhibits insulin-stimulated insulin receptor substrate-1/2-associated phosphoinositide 3-kinase activity, but not protein kinase B activation or glucose uptake, in rat muscle.
Biochem J.
2000;
349 (Pt 3)
775-781
-
116
Wicklmayr M, Dietze G, Gunther B, Bottger I, Mayer L, Janetschek P.
Improvement of glucose assimilation and protein degradation by bradykinin in maturity onset diabetics and in surgical patients.
Adv Exp Med Biol.
1979;
120 A
569-576
-
117
Widegren U, Ryder J W, Zierath J R.
Mitogen-activated protein kinase signal transduction in skeletal muscle: effects of exercise and muscle contraction.
Acta Physiol Scand.
2001;
172
227-238
-
118
Wijesekara N, Tung A, Thong F, Klip A.
Muscle cell depolarization induces a gain in surface GLUT4 via reduced endocytosis independently of AMPK.
Am J Physiol.
2006;
290
E1276-E1286
-
119
Wild S, Roglic G, Green A, Sicree R, King H.
Global prevalence of diabetes: estimates for the year 2000 and projections for 2030.
Diabetes Care.
2004;
27
1047-1053
-
120 Williams G, Pickup J C. Handbook of Diabetes. London, UK; Blackwell Publishing 2005: 275
-
121
Witczak C A, Fujii N, Hirshman M F, Goodyear L J.
Ca2+/calmodulin-dependent protein kinase kinase-alpha regulates skeletal muscle glucose uptake independent of AMP-activated protein kinase and Akt activation.
Diabetes.
2007;
56
1403-1409
-
122
Wojtaszewski J F, Hansen B F, Kiens B, Richter E A.
Insulin signaling in human skeletal muscle: time course and effect of exercise.
Diabetes.
1997;
46
1775-1781
-
123
Wojtaszewski J F, Higaki Y, Hirshman M F, Michael M D, Dufresne S D, Kahn C R, Goodyear L J.
Exercise modulates postreceptor insulin signaling and glucose transport in muscle-specific insulin receptor knockout mice.
J Clin Invest.
1999;
104
1257-1264
-
124
Woodgett J R, Cohen P, Yamauchi T, Fujisawa H.
Comparison of calmodulin-dependent glycogen synthase kinase from skeletal muscle and calmodulin-dependent protein kinase-II from brain.
FEBS Lett.
1984;
170
49-54
-
125
Woods A, Dickerson K, Heath R, Hong S P, Momcilovic M, Johnstone S R, Carlson M, Carling D.
Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells.
Cell Metab.
2005;
2
21-33
-
126
Wright D C, Geiger P C, Han D H, Holloszy J O.
Are tyrosine kinases involved in mediating contraction-stimulated muscle glucose transport?.
Am J Physiol.
2006;
290
E123-E128
-
127
Wright D C, Geiger P C, Holloszy J O, Han D H.
Contraction- and hypoxia-stimulated glucose transport is mediated by a Ca2+-dependent mechanism in slow-twitch rat soleus muscle.
Am J Physiol.
2005;
288
E1062-E1066
-
128
Wright D C, Hucker K A, Holloszy J O, Han D H.
Ca2+ and AMPK both mediate stimulation of glucose transport by muscle contractions.
Diabetes.
2004;
53
330-335
-
129
Xi X, Han J, Zhang J Z.
Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase.
J Biol Chem.
2001;
276
41029-41034
-
130
Youn J H, Gulve E A, Holloszy J O.
Calcium stimulates glucose transport in skeletal muscle by a pathway independent of contraction.
Am J Physiol.
1991;
260
C555-C561
-
131
Yu C, Chen Y, Cline G W, Zhang D, Zong H, Wang Y, Bergeron R, Kim J K, Cushman S W, Cooney G J, Atcheson B, White M F, Kraegen E W, Shulman G I.
Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS‐1)-associated phosphatidylinositol 3-kinase activity in muscle.
J Biol Chem.
2002;
277
50230-50236
-
132
Yu M, Blomstrand E, Chibalin A V, Wallberg-Henriksson H, Zierath J R, Krook A.
Exercise-associated differences in an array of proteins involved in signal transduction and glucose transport.
J Appl Physiol.
2001;
90
29-34
-
133
Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman M F, Goodyear L J, Moller D E.
Role of AMP-activated protein kinase in mechanism of metformin action.
J Clin Invest.
2001;
108
1167-1174
Prof. Jose Alberto Duarte
University of Porto
CIAFEL, Faculty of Sports
Rua Dr. Plácido Costa, 91
4200-450 Porto
Portugal
Fax: + 35 12 25 50 06 89
Email: jarduarte@fade.up.pt
