Abstract
Insulin-like growth factor I (IGF-I), an autocrine/paracrine growth factor involved in myogenesis, has rapid effects on muscle metabolism. In a manner analogous to insulin and mechanical stimuli such as stretch, IGF-I stimulates glucose transport through recruitment of glucose transporters to surface membranes in skeletal muscles. It is known that IGF-I is secreted from skeletal muscle cells in response to stretch. Therefore, we examined whether IGF-I is involved in the mechanism by which mechanical stretch regulates glucose transport using cultured C2C12 myotubes. IGF-I increased 2-deoxy-D-glucose (2-DG) uptake, and this created an additive effect with mechanical stretch, suggesting that these stimuli enhance glucose transport through different mechanisms. In fact, IGF-I-stimulated 2-DG uptake was not blocked by dantrolene (an inhibitor of Ca2+release from sarcoplasmic reticulum), whereas the stretch-stimulated effect was abolished. Conversely, the IGF-I-stimulated 2-DG uptake was prevented by phosphatidylinositol 3-kinase inhibitor wortmannin, which did not prevent the stretch-stimulated 2-DG uptake. In addition, experiments using media conditioned by stretched myotubes indicated that a mechanically induced release of locally acting autocrine/paracrine growth factors was not sufficient for induction of 2-DG uptake. Thus, our results demonstrate that mechanical stretch signaling for glucose transport is independent of the mechanism through which IGF-I increases this transport.
Key words
growth factor - skeletal muscle - autocrine/paracrine
References
-
1
Pereira LO, Lancha Jr AH.
Effect of insulin and contraction up on glucose transport in skeletal muscle.
Prog Biophys Mol Biol.
2004;
84
1-27
-
2
Holloszy JO.
A forty-year memoir of research on the regulation of glucose transport into muscle.
Am J Physiol Endcrinol Metab.
2003;
284
E453-E467
-
3
Vandenburgh HH.
Mechanical forces and their second messengers in stimulating cell growth in vitro.
Am J Physiol Regul Integr Comp Physiol.
1992;
262
R350-R355
-
4
Adachi R, Yabusaki K, Obinata T.
Uptake of albumin is coupled with stretch-induced hypertrophy of skeletal muscle cells in culture.
Zoolog Sci.
2003;
20
557-565
-
5
Ito Y, Obara K, Ikeda R, Ishii M, Tanabe Y, Ishikawa T, Nakayama K.
Passive stretching produces Akt- and MAPK-dependent augmentations of GLUT4 translocation and glucose uptake in skeletal muscles of mice.
Pflugers Arch.
2006;
451
803-813
-
6
Ihlemann J, Ploug T, Hellsten Y, Galbo H.
Effect of tension on contraction-induced glucose transport in rat skeletal muscle.
Am J Physiol Endocrinol Metab.
1999;
277
E208-E214
-
7
Mitsumoto Y, Downey GP, Klip A.
Stimulation of glucose transport in L6 muscle cells by long-term intermittent stretch-relaxation.
FEBS Lett.
1992;
301
94-98
-
8
Iwata M, Hayakawa K, Murakami T, Naruse K, Kawakami K, Inoue-Miyazu M, Yuge L, Suzuki S.
Uniaxial cyclic stretch-stimulated glucose transport is mediated by a Ca2+-dependent mechanism in cultured skeletal muscle cells.
Pathobiology.
2007;
74
159-168
-
9
Holloszy JO, Narahara HT.
Enhanced permeability to sugar associated with muscle contraction. Studies of the role of Ca2+.
J Gen Physiol.
1967;
50
551-562
-
10
Youn JH, Gulve EA, Holloszy JO.
Calcium stimulates glucose transport in skeletal muscle by a pathway independent of contraction.
Am J Physiol Cell Physiol.
1991;
260
C555-C561
-
11
Clarke MS, Feeback DL.
Mechanical load induces sarcoplasmic wounding and FGF release in differentiated human skeletal muscle cultures.
FASEB J.
1996;
10
502-509
-
12
Perrone CE, Fenwick-Smith D, Vandenburgh HH.
Collagen and stretch modulate autocrine secretion of insulin-like growth factor-1 and insulin-like growth factor binding proteins from differentiated skeletal muscle cells.
J Biol Chem.
1995;
270
2099-2106
-
13
Zapf J, Froesch ER.
Insulin-like growth factors/somatomedins: structure, secretion, biological actions and physiological role.
Horm Res.
1986;
24
121-130
-
14
Singleton JR, Feldman EL.
Insulin-like growth factor-I in muscle metabolism and myotherapies.
Neurobiol Dis.
2001;
8
541-554
-
15
Adams GR.
Invited Review: Autocrine/paracrine IGF-I and skeletal muscle adaptation.
J Appl Physiol.
2002;
93
1159-1167
-
16
Tidball JG.
Mechanical signal transduction in skeletal muscle growth and adaptation.
J Appl Physiol.
2005;
98
1900-1908
-
17
Bilan PJ, Mitsumoto Y, Ramlal T, Klip A.
Acute and long-term effects of insulin-like growth factor I on glucose transporters in muscle cells. Translocation and biosynthesis.
FEBS Lett.
1992;
298
285-290
-
18
Lund S, Flyvbjerg A, Holman GD, Larsen FS, Pedersen O, Schmitz O.
Comparative effects of IGF-I and insulin on the glucose transporter system in rat muscle.
Am J Physiol Endcrinol Metab.
1994;
267
E461-E466
-
19
Hu BS, Landeen LK, Aroonsakool N, Giles WR.
An analysis of the effects of stretch on IGF-I secretion from rat ventricular fibroblasts.
Am J Physiol Heart Circ Physiol.
2007;
293
H677-H683
-
20
Naruse K, Yamada T, Sokabe M.
Involvement of SA channels in orienting response of cultured endothelial cells to cyclic stretch.
Am J Physiol Heart Circ Physiol.
1998;
274
H1532-H1538
-
21
Klip A, Logan WJ, Li G.
Hexose transport in L6 muscle cells. Kinetic properties and the number of [3H] cytochalasin B binding sites.
Biochem Biophys Acta.
1982;
687
265-280
-
22
Bradford MM.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
Anal Biochem.
1976;
72
248-254
-
23
Winkle WB Van.
Calcium release from skeletal muscle sarcoplasmic reticulum: site of action of dantrolene sodium.
Science.
1976;
193
1130-1131
-
24
Domin J, Pages F, Volinia S, Rittenhouse SE, Zvelebil MJ, Stein RC, Waterfield MD.
Cloning of a human phosphoinositide 3-kinase with a C2 domain that displays reduced sensitivity to the inhibitor wortmannin.
Biochem J.
1997;
326
139-147
-
25
Shepherd PR, Withers DJ, Siddle K.
Phosphoinositide 3-kinase: the key switch mechanism in insulin signaling.
Biochem J.
1998;
333
471-490
-
26
Yaffe D, Saxel O.
Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle.
Nature.
1977;
270
725-727
-
27
Shimokawa T, Kato M, Ezaki O, Hashimoto S.
Transcriptional regulation of muscle-specific genes during myoblast differentiation.
Biochem Biophys Res Commun.
1998;
246
287-292
-
28
Richardson JM, Pessin JE.
Identification of a skeletal muscle-specific regulatory domain in the rat GLUT4/muscle-fat gene.
J Biol Chem.
1993;
268
21021-21027
-
29
Kimball SR, Farrell PA, Jefferson LS.
Invited Review: Role of insulin in translational control of protein synthesis in skeletal muscle by amino acids or exercise.
J Appl Physiol.
2000;
93
1168-1180
-
30
Sell H, Kaiser U, Eckel J.
Expression of chemokine receptors in insulin-resistant human skeletal muscle cells.
Horm Metab Res.
2007;
39
244-249
-
31
Zorzano A, James DE, Ruderman NB, Pilch PF.
Insulin-like growth factor I binding and receptor kinase in red and white muscle.
FEBS Lett.
1988;
234
257-262
-
32
Dohm GL, Elton CW, Raju MS, Mooney ND, DiMarchi R, Pories WJ, Flickinger EG, Atkinson Jr SM, Caro JF.
IGF-I-stimulated glucose transport in human skeletal muscle and IGF-I resistance in obesity and NIDDM.
Diabetes.
1990;
39
1028-1032
-
33
Le Roith D, Scavo L, Butler A.
What is the role of circulating IGF-I?.
Trends Endocrinol Metab.
2001;
12
48-52
-
34
MacKoy G, Ashley W, Mander J, Yang SY, Williams N, Russell B, Goldspink G.
Expression of insulin growth factor-1 splice variants and structural genes in rabbit skeletal muscle induced by stretch and stimulation.
J Physiol.
1999;
516
583-592
-
35
LeRoith D, Werner H, Beitner-Johnson D, Roberts Jr CT.
Molecular and cellular aspects of the insulin-like growth factor I receptor.
Endocr Rev.
1995;
16
143-163
-
36
Meyts P De, Wallach B, Christoffersen CT, Ursø B, Grønskov K, Latus LJ, Yakushiji F, Ilondo MM, Shymko RM.
The insulin-like growth factor-I receptor. Structure, ligand-binding mechanism and signal transduction.
Horm Res.
1994;
42
152-169
-
37
Vroede MA de, Romanus JA, Standaert ML, Pollet RJ, Nissley SP, Rechler MM.
Interaction of insulin-like growth factors with a nonfusing mouse muscle cell line: binding, action, and receptor down-regulation.
Endocrinology.
1984;
114
1917-1929
-
38
Beguinot F, Kahn CR, Moses AC, Smith RJ.
Distinct biologically active receptors for insulin, insulin-like growth factor I, and insulin-like growth factor II in cultured skeletal muscle cells.
J Biol Chem.
1985;
260
15892-15898
-
39
Maher F, Clark S, Harrison LC.
Chronic stimulation of glucose transporter gene expression in L6 myocytes mediated via the insulin-like growth factor-1 receptor.
Mol Endocrinol.
1989;
3
2128-2135
-
40
Thong FS, Dugani CB, Klip A.
Turning signals on and off: GLUT4 traffic in the insulin-signaling highway.
Physiology.
2005;
20
271-284
-
41
Ishiki M, Randhawa VK, Poon V, Jebailey L, Klip A.
Insulin regulates the membrane arrival, fusion, and C-terminal unmasking of glucose transporter-4 via distinct phosphoinositides.
J Biol Chem.
2005;
280
28792-28802
-
42
Kanda H, Tamori Y, Shinoda H, Yoshikawa M, Sakaue M, Udagawa J, Otani H, Tashiro F, Miyazaki J, Kasuga M.
Adipocytes from Munc18c-null mice show increased sensitivity to insulin-stimulated GLUT4 externalization.
J Clin Invest.
2005;
115
291-301
-
43
Domin J, Pages F, Volinia S, Rittenhouse SE, Zvelebil MJ, Stein RC, Waterfield MD.
Cloning of a human phosphoinositide 3-kinase with a C2 domain that displays reduced sensitivity to the inhibitor wortmannin.
Biochem J.
1997;
326
139-147
Correspondence
S. SuzukiPhD
Program in Physical and Occupational Therapy
Nagoya University Graduate School of Medicine
1-1-20 Daikominami
Higashi-ku
Nagoya 461-8673
Japan
Phone: +81/52/719 13 62
Fax: +81/52/719 13 62
Email: suzuki@met.nagoya-u.ac.jp