Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Diabetologia
Published in: Diabetologia 1/2015

01-01-2015 | Review

Roles of TBC1D1 and TBC1D4 in insulin- and exercise-stimulated glucose transport of skeletal muscle

Author: Gregory D. Cartee

Published in: Diabetologia | Issue 1/2015

Login to get access

Abstract

This review focuses on two paralogue Rab GTPase activating proteins known as TBC1D1 Tre-2/BUB2/cdc 1 domain family (TBC1D) 1 and TBC1D4 (also called Akt Substrate of 160 kDa, AS160) and their roles in controlling skeletal muscle glucose transport in response to the independent and combined effects of insulin and exercise. Convincing evidence implicates Akt2-dependent TBC1D4 phosphorylation on T642 as a key part of the mechanism for insulin-stimulated glucose uptake by skeletal muscle. TBC1D1 phosphorylation on several insulin-responsive sites (including T596, a site corresponding to T642 in TBC1D4) does not appear to be essential for in vivo insulin-stimulated glucose uptake by skeletal muscle. In vivo exercise or ex vivo contraction of muscle result in greater TBC1D1 phosphorylation on S237 that is likely to be secondary to increased AMP-activated protein kinase activity and potentially important for contraction-stimulated glucose uptake. Several studies that evaluated both normal and insulin-resistant skeletal muscle stimulated with a physiological insulin concentration after a single exercise session found that greater post-exercise insulin-stimulated glucose uptake was accompanied by greater TBC1D4 phosphorylation on several sites. In contrast, enhanced post-exercise insulin sensitivity was not accompanied by greater insulin-stimulated TBC1D1 phosphorylation. The mechanism for greater TBC1D4 phosphorylation in insulin-stimulated muscles after acute exercise is uncertain, and a causal link between enhanced TBC1D4 phosphorylation and increased post-exercise insulin sensitivity has yet to be established. In summary, TBC1D1 and TBC1D4 have important, but distinct roles in regulating muscle glucose transport in response to insulin and exercise.
Literature
1.
Constable SH, Favier RJ, Cartee GD, Young DA, Holloszy JO (1988) Muscle glucose transport: interactions of in vitro contractions, insulin, and exercise. J Appl Physiol 64:2329–2332PubMed
2.
Cartee GD, Wojtaszewski JF (2007) Role of Akt substrate of 160 kDa in insulin-stimulated and contraction-stimulated glucose transport. Appl Physiol Nutr Metab 32:557–566PubMedCrossRef
3.
Cartee GD, Funai K (2009) Exercise and insulin: convergence or divergence at AS160 and TBC1D1? Exerc Sport Sci Rev 37:188–195PubMedCentralPubMed
4.
Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93:993–1017PubMedCrossRef
5.
Douen AG, Ramlal T, Rastogi S et al (1990) 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 265:13427–13430PubMed
6.
Cartee GD, Young DA, Sleeper MD, Zierath J, Wallberg-Henriksson H, Holloszy JO (1989) Prolonged increase in insulin-stimulated glucose transport in muscle after exercise. Am J Physiol 256:E494–E499PubMed
7.
Richter EA, Garetto LP, Goodman MN, Ruderman NB (1982) Muscle glucose metabolism following exercise in the rat: increased sensitivity to insulin. J Clin Invest 69:785–793PubMedCentralPubMedCrossRef
8.
Maarbjerg SJ, Sylow L, Richter EA (2011) Current understanding of increased insulin sensitivity after exercise—emerging candidates. Acta Physiol (Oxf) 202:323–335CrossRef
9.
Frøsig C, Richter EA (2009) Improved insulin sensitivity after exercise: focus on insulin signaling. Obesity (Silver Spring) 17(Suppl 3):S15–S20CrossRef
10.
Perseghin G, Price TB, Petersen KF et al (1996) Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects. N Engl J Med 335:1357–1362PubMedCrossRef
11.
Kane S, Sano H, Liu SC et al (2002) A method to identify serine kinase substrates. Akt phosphorylates a novel adipocyte protein with a Rab GTPase-activating protein (GAP) domain. J Biol Chem 277:22115–22118PubMedCrossRef
12.
Bruss MD, Arias EB, Lienhard GE, Cartee GD (2005) Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54:41–50PubMedCrossRef
13.
Arias EB, Kim J, Cartee GD (2004) Prolonged incubation in PUGNAc results in increased protein O-Linked glycosylation and insulin resistance in rat skeletal muscle. Diabetes 53:921–930PubMedCrossRef
14.
Sano H, Kane S, Sano E et al (2003) Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J Biol Chem 278:14599–14602PubMedCrossRef
15.
Zhang H, Zha X, Tan Y et al (2002) Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J Biol Chem 277:39379–39387PubMedCrossRef
16.
Roach WG, Chavez JA, Miinea CP, Lienhard GE (2007) Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem J 403:353–358PubMedCentralPubMedCrossRef
17.
Chen S, Murphy J, Toth R, Campbell DG, Morrice NA, Mackintosh C (2008) Complementary regulation of TBC1D1 and AS160 by growth factors, insulin and AMPK activators. Biochem J 409:449–459PubMedCrossRef
18.
Taylor EB, An D, Kramer HF et al (2008) Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J Biol Chem 283:9787–9796PubMedCentralPubMedCrossRef
19.
Castorena CM, Mackrell JG, Bogan JS, Kanzaki M, Cartee GD (2011) Clustering of GLUT4, TUG, and RUVBL2 protein levels correlate with myosin heavy chain isoform pattern in skeletal muscles, but AS160 and TBC1D1 levels do not. J Appl Physiol 111:1106–1117PubMedCentralPubMedCrossRef
20.
Jensen TE, Leutert R, Rasmussen ST et al (2012) EMG-normalised kinase activation during exercise is higher in human gastrocnemius compared to soleus muscle. PLoS One 7:e31054PubMedCentralPubMedCrossRef
21.
Geraghty KM, Chen S, Harthill JE et al (2007) Regulation of multisite phosphorylation and 14-3-3 binding of AS160 in response to IGF-1, EGF, PMA and AICAR. Biochem J 407:231–241PubMedCentralPubMedCrossRef
22.
Chen S, Synowsky S, Tinti M, MacKintosh C (2011) The capture of phosphoproteins by 14-3-3 proteins mediates actions of insulin. Trends Endocrinol Metab 22:429–436PubMedCrossRef
23.
Ramm G, Larance M, Guilhaus M, James DE (2006) A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J Biol Chem 281:29174–29180PubMedCrossRef
24.
Miinea CP, Sano H, Kane S et al (2005) AS160, the Akt substrate regulating GLUT4 translocation, has a functional Rab GTPase-activating protein domain. Biochem J 391:87–93PubMedCentralPubMedCrossRef
25.
Sano H, Eguez L, Teruel MN et al (2007) Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane. Cell Metab 5:293–303PubMedCrossRef
26.
Klip A, Sun Y, Chiu TT, Foley KP (2014) Signal transduction meets vesicle traffic: the software and hardware of GLUT4 translocation. Am J Physiol Cell Physiol 306:C879–C886PubMedCrossRef
27.
28.
Foley K, Boguslavsky S, Klip A (2011) Endocytosis, recycling, and regulated exocytosis of glucose transporter 4. Biochemistry 50:3048–3061PubMedCrossRef
29.
30.
Brewer PD, Habtemichael EN, Romenskaia I, Mastick CC, Coster AC (2014) Insulin-regulated Glut4 translocation: membrane protein trafficking with six distinctive steps. J Biol Chem 289:17280–17298PubMedCrossRef
31.
Tan SX, Ng Y, Burchfield JG et al (2012) The Rab GTPase-activating protein TBC1D4/AS160 contains an atypical phosphotyrosine-binding domain that interacts with plasma membrane phospholipids to facilitate GLUT4 trafficking in adipocytes. Mol Cell Biol 32:4946–4959PubMedCentralPubMedCrossRef
32.
Ishikura S, Bilan PJ, Klip A (2007) Rabs 8A and 14 are targets of the insulin-regulated Rab-GAP AS160 regulating GLUT4 traffic in muscle cells. Biochem Biophys Res Commun 353:1074–1079PubMedCrossRef
33.
Thong FS, Bilan PJ, Klip A (2007) The Rab GTPase-activating protein AS160 integrates Akt, protein kinase C, and AMP-activated protein kinase signals regulating GLUT4 traffic. Diabetes 56:414–423PubMedCrossRef
34.
Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ (2006) AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 281:31478–31485PubMedCrossRef
35.
Chen S, Wasserman DH, MacKintosh C, Sakamoto K (2011) Mice with AS160/TBC1D4-Thr649Ala knockin mutation are glucose intolerant with reduced insulin sensitivity and altered GLUT4 trafficking. Cell Metab 13:68–79PubMedCentralPubMedCrossRef
36.
Cho H, Mu J, Kim JK et al (2001) Insulin resistance and a diabetes mellitus-like syndrome in mice lacking the protein kinase Akt2 (PKB beta). Science 292:1728–1731PubMedCrossRef
37.
McCurdy CE, Cartee GD (2005) Akt2 is essential for the full effect of calorie restriction on insulin-stimulated glucose uptake in skeletal muscle. Diabetes 54:1349–1356PubMedCrossRef
38.
Kramer HF, Witczak CA, Fujii N et al (2006) Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes 55:2067–2076PubMedCrossRef
39.
Chavez JA, Roach WG, Keller SR, Lane WS, Lienhard GE (2008) Inhibition of GLUT4 translocation by Tbc1d1, a Rab GTPase-activating protein abundant in skeletal muscle, is partially relieved by AMP-activated protein kinase activation. J Biol Chem 283:9187–9195PubMedCentralPubMedCrossRef
40.
Pehmøller C, Brandt N, Birk JB et al (2012) Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes 61:2743–2752PubMedCentralPubMedCrossRef
41.
Pehmøller C, Treebak JT, Birk JB et al (2009) Genetic disruption of AMPK signaling abolishes both contraction- and insulin-stimulated TBC1D1 phosphorylation and 14-3-3 binding in mouse skeletal muscle. Am J Physiol Endocrinol Metab 297:E665–E675PubMedCentralPubMedCrossRef
42.
43.
Peck GR, Chavez JA, Roach WG et al (2009) Insulin-stimulated phosphorylation of the Rab GTPase-activating protein TBC1D1 regulates GLUT4 translocation. J Biol Chem 284:30016–30023PubMedCentralPubMedCrossRef
44.
Cheng KK, Zhu W, Chen B et al (2014) The adaptor protein APPL2 inhibits insulin-stimulated glucose uptake by interacting with TBC1D1 in skeletal muscle. Diabetes. doi:10.​2337/​db14-0337
45.
Funai K, Schweitzer GG, Castorena CM, Kanzaki M, Cartee GD (2010) In vivo exercise followed by in vitro contraction additively elevates subsequent insulin-stimulated glucose transport by rat skeletal muscle. Am J Physiol Endocrinol Metab 298:E999–E1010PubMedCentralPubMedCrossRef
46.
An D, Toyoda T, Taylor EB et al (2010) TBC1D1 regulates insulin- and contraction-induced glucose transport in mouse skeletal muscle. Diabetes 59:1358–1365PubMedCentralPubMedCrossRef
47.
Arias EB, Kim J, Funai K, Cartee GD (2007) Prior exercise increases phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle. Am J Physiol Endocrinol Metab 292:E1191–E1200PubMedCrossRef
48.
Schweitzer GG, Arias EB, Cartee GD (2012) Sustained postexercise increases in AS160 Thr642 and Ser588 phosphorylation in skeletal muscle without sustained increases in kinase phosphorylation. J Appl Physiol 113:1852–1861PubMedCentralPubMedCrossRef
49.
Funai K, Schweitzer GG, Sharma N, Kanzaki M, Cartee GD (2009) Increased AS160 phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle. Am J Physiol Endocrinol Metab 297:E242–E251PubMedCentralPubMedCrossRef
50.
Castorena CM, Arias EB, Sharma N, Cartee GD (2014) Post-exercise improvement in insulin-stimulated glucose uptake occurs concomitant with greater AS160 phosphorylation in muscle from normal and insulin resistant rats. Diabetes 63:2297–2308PubMedCrossRef
51.
Treebak JT, Birk JB, Rose AJ, Kiens B, Richter EA, Wojtaszewski JF (2007) AS160 phosphorylation is associated with activation of α2β2γ1—but not α2β2γ3—AMPK trimeric complex in skeletal muscle during exercise in humans. Am J Physiol Endocrinol Metab 292:E715–E722PubMedCrossRef
52.
Howlett KF, Mathews A, Garnham A, Sakamoto K (2008) The effect of exercise and insulin on AS160 phosphorylation and 14-3-3 binding capacity in human skeletal muscle. Am J Physiol Endocrinol Metab 294:E401–E407PubMedCrossRef
53.
Treebak JT, Taylor EB, Witczak CA et al (2010) Identification of a novel phosphorylation site on TBC1D4 regulated by AMP-activated protein kinase in skeletal muscle. Am J Physiol Cell Physiol 298:C377–C385PubMedCentralPubMedCrossRef
54.
Treebak JT, Pehmøller C, Kristensen JM et al (2014) Acute exercise and physiological insulin induce distinct phosphorylation signatures on TBC1D1 and TBC1D4 proteins in human skeletal muscle. J Physiol 592:351–375PubMed
55.
56.
Breen L, Philp A, Shaw CS, Jeukendrup AE, Baar K, Tipton KD (2011) Beneficial effects of resistance exercise on glycemic control are not further improved by protein ingestion. PLoS One 6:e20613PubMedCentralPubMedCrossRef
57.
Howlett KF, Sakamoto K, Garnham A, Cameron-Smith D, Hargreaves M (2007) Resistance exercise and insulin regulate AS160 and interaction with 14-3-3 in human skeletal muscle. Diabetes 56:1608–1614PubMedCrossRef
58.
Dreyer HC, Drummond MJ, Glynn EL et al (2008) Resistance exercise increases human skeletal muscle AS160/TBC1D4 phosphorylation in association with enhanced leg glucose uptake during postexercise recovery. J Appl Physiol 105:1967–1974PubMedCentralPubMedCrossRef
59.
Guerra B, Guadalupe-Grau A, Fuentes T et al (2010) SIRT1, AMP-activated protein kinase phosphorylation and downstream kinases in response to a single bout of sprint exercise: influence of glucose ingestion. Eur J Appl Physiol 109:731–743PubMedCrossRef
60.
Levinger I, Jerums G, Stepto NK et al (2014) The effect of acute exercise on undercarboxylated osteocalcin and insulin sensitivity in obese men. J Bone Miner Res Off J Am Soc Bone Miner Res. doi:10.​1002/​jbmr.​2285
61.
Ducommun S, Wang HY, Sakamoto K, MacKintosh C, Chen S (2012) Thr649Ala-AS160 knock-in mutation does not impair contraction/AICAR-induced glucose transport in mouse muscle. Am J Physiol Endocrinol Metab 302:E1036–E1043PubMedCentralPubMedCrossRef
62.
Funai K, Cartee GD (2009) Inhibition of contraction-stimulated AMP-activated protein kinase inhibits contraction-stimulated increases in PAS-TBC1D1 and glucose transport without altering PAS-AS160 in rat skeletal muscle. Diabetes 58:1096–1104PubMedCentralPubMedCrossRef
63.
Frøsig C, Rose AJ, Treebak JT, Kiens B, Richter EA, Wojtaszewski JF (2007) Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes 56:2093–2102PubMedCrossRef
64.
Kramer HF, Taylor EB, Witczak CA, Fujii N, Hirshman MF, Goodyear LJ (2007) Calmodulin-binding domain of AS160 regulates contraction- but not insulin-stimulated glucose uptake in skeletal muscle. Diabetes 56:2854–2862PubMedCrossRef
65.
Hinkley JM, Ferey JL, Brault JJ, Smith CA, Gilliam LA, Witczak CA (2014) Constitutively active CaMKKalpha stimulates skeletal muscle glucose uptake in insulin-resistant mice in vivo. Diabetes 63:142–151PubMedCrossRef
66.
Treebak JT, Glund S, Deshmukh A et al (2006) AMPK-mediated AS160 phosphorylation in skeletal muscle is dependent on AMPK catalytic and regulatory subunits. Diabetes 55:2051–2058PubMedCrossRef
67.
Sakamoto K, Hirshman MF, Aschenbach WG, Goodyear LJ (2002) Contraction regulation of Akt in rat skeletal muscle. J Biol Chem 277:11910–11917PubMedCrossRef
68.
Sakamoto K, Aschenbach WG, Hirshman MF, Goodyear LJ (2003) Akt signaling in skeletal muscle: regulation by exercise and passive stretch. Am J Physiol Endocrinol Metab 285:E1081–E1088PubMed
69.
Sakamoto K, Arnolds DE, Fujii N, Kramer HF, Hirshman MF, Goodyear LJ (2006) Role of Akt2 in contraction-stimulated cell signaling and glucose uptake in skeletal muscle. Am J Physiol Endocrinol Metab 291:E1031–E1037PubMedCrossRef
70.
Goodyear LJ, Chang PY, Sherwood DJ, Dufresne SD, Moller DE (1996) Effects of exercise and insulin on mitogen-activated protein kinase signaling pathways in rat skeletal muscle. Am J Physiol 271:E403–E408PubMed
71.
Lund S, Pryor PR, Ostergaard S, Schmitz O, Pedersen O, Holman GD (1998) Evidence against protein kinase B as a mediator of contraction-induced glucose transport and GLUT4 translocation in rat skeletal muscle. FEBS Lett 425:472–474PubMedCrossRef
72.
Brozinick JT Jr, Birnbaum MJ (1998) Insulin, but not contraction, activates Akt/PKB in isolated rat skeletal muscle. J Biol Chem 273:14679–14682PubMedCrossRef
73.
Sakamoto K, Arnolds DE, Ekberg I, Thorell A, Goodyear LJ (2004) Exercise regulates Akt and glycogen synthase kinase-3 activities in human skeletal muscle. Biochem Biophys Res Commun 319:419–425PubMedCrossRef
74.
Markuns JF, Wojtaszewski JF, Goodyear LJ (1999) Insulin and exercise decrease glycogen synthase kinase-3 activity by different mechanisms in rat skeletal muscle. J Biol Chem 274:24896–24900PubMedCrossRef
75.
Wojtaszewski JF, Higaki Y, Hirshman MF et al (1999) Exercise modulates postreceptor insulin signaling and glucose transport in muscle-specific insulin receptor knockout mice. J Clin Invest 104:1257–1264PubMedCentralPubMedCrossRef
76.
Widegren U, Jiang XJ, Krook A et al (1998) Divergent effects of exercise on metabolic and mitogenic signaling pathways in human skeletal muscle. FASEB J 12:1379–1389PubMed
77.
Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ (2001) A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7:1085–1094PubMedCrossRef
78.
Jorgensen SB, Viollet B, Andreelli F et al (2004) Knockout of the alpha2 but not alpha1 5'-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-β-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. J Biol Chem 279:1070–1079PubMedCrossRef
79.
O’Neill HM, Maarbjerg SJ, Crane JD et al (2011) AMP-activated protein kinase (AMPK) β1β2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc Natl Acad Sci U S A 108:16092–16097PubMedCentralPubMedCrossRef
80.
Frøsig C, Pehmøller C, Birk JB, Richter EA, Wojtaszewski JF (2010) Exercise-induced TBC1D1 Ser237 phosphorylation and 14-3-3 protein binding capacity in human skeletal muscle. J Physiol 588:4539–4548PubMedCentralPubMedCrossRef
81.
Vendelbo MH, Moller AB, Treebak JT et al (2014) Sustained AS160 and TBC1D1 phosphorylations in human skeletal muscle 30 minutes after a single bout of exercise. J Appl Physiol 117:289–296PubMedCrossRef
82.
Cartee GD, Briggs-Tung C, Kietzke EW (1993) Persistent effects of exercise on skeletal muscle glucose transport across the life-span of rats. J Appl Physiol 75:972–978PubMed
83.
Wojtaszewski JF, Hansen BF, Gade et al (2000) Insulin signaling and insulin sensitivity after exercise in human skeletal muscle. Diabetes 49:325–331PubMedCrossRef
84.
Hansen PA, Nolte LA, Chen MM, Holloszy JO (1998) Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise. J Appl Physiol 85:1218–1222PubMed
85.
Howlett KF, Sakamoto K, Hirshman MF et al (2002) Insulin signaling after exercise in insulin receptor substrate-2-deficient mice. Diabetes 51:479–483PubMedCrossRef
86.
Treebak JT, Frøsig C, Pehmøller C et al (2009) Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle. Diabetologia 52:891–900PubMedCentralPubMedCrossRef
87.
Ikeda S, Tamura Y, Kakehi S et al (2013) Exercise-induced enhancement of insulin sensitivity is associated with accumulation of M2-polarized macrophages in mouse skeletal muscle. Biochem Biophys Res Commun 441:36–41PubMedCrossRef
88.
Consitt LA, Van Meter J, Newton CA et al (2013) Impairments in site-specific AS160 phosphorylation and effects of exercise training. Diabetes 62:3437–3447PubMedCentralPubMedCrossRef
89.
Xie X, Chen Y, Xue P et al (2009) RUVBL2, a novel AS160-binding protein, regulates insulin-stimulated GLUT4 translocation. Cell Res 19:1090–1097PubMedCrossRef
90.
Ren W, Cheema S, Du K (2012) The association of ClipR-59 protein with AS160 modulates AS160 protein phosphorylation and adipocyte Glut4 protein membrane translocation. J Biol Chem 287:26890–26900PubMedCentralPubMedCrossRef
91.
Ho PC, Lin YW, Tsui YC, Gupta P, Wei LN (2009) A negative regulatory pathway of GLUT4 trafficking in adipocyte: new function of RIP140 in the cytoplasm via AS160. Cell Metab 10:516–523PubMedCentralPubMedCrossRef
92.
93.
Xiao Y, Sharma N, Arias EB, Castorena CM, Cartee GD (2013) A persistent increase in insulin-stimulated glucose uptake by both fast-twitch and slow-twitch skeletal muscles after a single exercise session by old rats. Age (Dordr) 35:573–582CrossRef
94.
Vind BF, Pehmøller C, Treebak JT et al (2011) Impaired insulin-induced site-specific phosphorylation of TBC1 domain family, member 4 (TBC1D4) in skeletal muscle of type 2 diabetes patients is restored by endurance exercise-training. Diabetologia 54:157–167PubMedCrossRef
95.
Brandt N, De Bock K, Richter EA, Hespel P (2010) Cafeteria diet-induced insulin resistance is not associated with decreased insulin signaling or AMPK activity and is alleviated by physical training in rats. Am J Physiol Endocrinol Metab 299:E215–E224PubMed
96.
Chadt A, Leicht K, Deshmukh A et al (2008) Tbc1d1 mutation in lean mouse strain confers leanness and protects from diet-induced obesity. Nat Genet 40:1354–1359PubMedCrossRef
97.
Szekeres F, Chadt A, Tom RZ et al (2012) The Rab-GTPase-activating protein TBC1D1 regulates skeletal muscle glucose metabolism. Am J Physiol Endocrinol Metab 303:E524–E533PubMedCrossRef
98.
Dokas J, Chadt A, Nolden T et al (2013) Conventional knockout of Tbc1d1 in mice impairs insulin- and AICAR-stimulated glucose uptake in skeletal muscle. Endocrinology 154:3502–3514PubMedCrossRef
99.
Lansey MN, Walker NN, Hargett SR, Stevens JR, Keller SR (2012) Deletion of Rab GAP AS160 modifies glucose uptake and GLUT4 translocation in primary skeletal muscles and adipocytes and impairs glucose homeostasis. Am J Physiol Endocrinol Metab 303:E1273–E1286PubMedCentralPubMedCrossRef
100.
Wang HY, Ducommun S, Quan C et al (2013) AS160 deficiency causes whole-body insulin resistance via composite effects in multiple tissues. Biochem J 449:479–489PubMedCentralPubMedCrossRef
Metadata
Title
Roles of TBC1D1 and TBC1D4 in insulin- and exercise-stimulated glucose transport of skeletal muscle
Author
Gregory D. Cartee
Publication date
01-01-2015
Publisher
Springer Berlin Heidelberg
Published in
Diabetologia / Issue 1/2015
Print ISSN: 0012-186X
Electronic ISSN: 1432-0428
DOI
https://doi.org/10.1007/s00125-014-3395-5

Other articles of this Issue 1/2015

Diabetologia 1/2015 Go to the issue

For Debate

The time has come to test the beta cell preserving effects of exercise in patients with new onset type 1 diabetes

Article

Metabolic response to 36 hours of fasting in young men born small vs appropriate for gestational age

Erratum

Erratum to: Eating two larger meals a day (breakfast and lunch) is more effective than six smaller meals in a reduced-energy regimen for patients with type 2 diabetes: a randomised crossover study

Article

The adverse association of diabetes with risk of first acute myocardial infarction is modified by physical activity and body mass index: prospective data from the HUNT Study, Norway

Erratum

Erratum to: Feature ranking of type 1 diabetes susceptibility genes improves prediction of type 1 diabetes

Article

Enterovirus infection is associated with an increased risk of childhood type 1 diabetes in Taiwan: a nationwide population-based cohort study
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits