The ras superfamily of small GTP-binding proteins in glucose transporter type 4-mediated glucose uptake in insulin-responsive tissues

Glucose Uptake: Regulation, Signaling Pathways and Health Implications

Volumn , Issue , 2013, Pages 235-252

  Satoh, Takaya ^a  

^a Osaka Prefecture University   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84895399943     PISSN: None     EISSN: None     Source Type: Book    
DOI: None     Document Type: Chapter

References (74)

1. Abel, E. D., Peroni, O., Kim, J. K., Kim, Y. B., Boss, O., Hadro, E., Minnemann, T., Shulman, G. I., and Kahn, B. B. (2001). Adipose-selective targeting of the GLUT4 gene impairs insulin action in muscle and liver. Nature, 409, 729-733.
2. Balamatsias, D., Kong, A. M., Waters, J. E., Sriratana, A., Gurung, R., Bailey, C. G., Rasko, J. E., Tiganis, T., Macaulay, S. L., and Mitchell, C. A. (2011). Identification of P-Rex1 as a novel Rac1-guanine nucleotide exchange factor (GEF) that promotes actin remodeling and GLUT4 protein trafficking in adipocytes. J. Biol. Chem., 286, 43229-43240.
3. Bose, A., Guilherme, A., Robida, S. I., Nicoloro, S. M., Zhou, Q. L., Jiang, Z. Y., Pomerleau, D. P., and Czech, M. P. (2002). Glucose transporter recycling in response to insulin is facilitated by myosin Myo1c. Nature, 420, 821-824.
4. Brozinick, J. T. Jr, Hawkins, E. D., Strawbridge, A. B., and Elmendorf, J. S. (2004). Disruption of cortical actin in skeletal muscle demonstrates an essential role of the cytoskeleton in glucose transporter 4 translocation in insulin-sensitive tissues. J. Biol. Chem. 279, 40699-40706.
5. Bruss, M. D., Arias, E. B., Lienhard, G. E., and Cartee, G. D. (2005). Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes, 54, 41-50.
6. Bryant, D. M., Datta, A., Rodríguez-Fraticelli, A. E., Peränen, J., Martín-Belmonte, F., and Mostov, K. E. (2010). A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol., 12, 1035-1045.
7. Chen, X. W., Leto, D., Chiang, S. H., Wang, Q., and Saltiel, A. R. (2007). Activation of RalA is required for insulin-stimulated Glut4 trafficking to the plasma membrane via the exocyst and the motor protein Myo1c. Dev. Cell, 13, 391-404.
8. Chen, X. W., Leto, D., Xiao, J., Goss, J., Wang, Q., Shavit, J. A., Xiong, T., Yu, G., Ginsburg, D., Toomre, D., Xu, Z., and Saltiel, A. R. (2011a). Exocyst function is regulated by effector phosphorylation. Nat. Cell Biol., 13, 580-588.
9. Chen, X. W., Leto, D., Xiong, T., Yu, G., Cheng, A., Decker, S., and Saltiel, A. R. (2011b). A Ral GAP complex links PI 3-kinase/Akt signaling to RalA activation in insulin action. Mol. Biol. Cell, 22, 141-152.
10. Chiang, S. H., Baumann, C. A., Kanzaki, M., Thurmond, D. C., Watson, R. T., Neudauer, C. L., Macara, I. G., Pessin, J. E., and Saltiel, A. R. (2001). Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature, 410, 944-948.
11. Chiu, T. T., Jensen, T. E., Sylow, L., Richter, E. A., and Klip, A. (2011). Rac1 signalling towards GLUT4/glucose uptake in skeletal muscle. Cell. Signal., 23, 1546-1554.
12. Cormont, M., Bortoluzzi, M. N., Gautier, N., Mari, M., van Obberghen, E., and Le Marchand-Brustel, Y. (1996). Potential role of Rab4 in the regulation of subcellular localization of Glut4 in adipocytes. Mol. Cell. Biol., 16, 6879-6886.
13. Eguez, L., Lee, A., Chavez, J. A., Miinea, C. P., Kane, S., Lienhard, G. E., and McGraw, T. E. (2005). Full intracellular retention of GLUT4 requires AS160 Rab GTPase activating protein. Cell Metab., 2, 263-272.
14. Fazakerley, D. J., Lawrence, S. P., Lizunov, V. A., Cushman, S. W., and Holman, G. D. (2009). A common trafficking route for GLUT4 in cardiomyocytes in response to insulin, contraction and energy-status signalling. J. Cell Sci., 122, 727-734.
15. Feig, L. A. (2003). Ral-GTPases: approaching their 15 minutes of fame. Trends Cell Biol., 13, 419-425.
16. Franke, T. F. (2008). PI3K/Akt: getting it right matters. Oncogene, 27, 6473-6488.
17. Grosshans, B. L., Ortiz, D. and Novick, P. (2006). Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. US, 103, 11821-11827.
18. Hafner, M., Schmitz, A., Grüne, I., Srivatsan, S. G., Paul, B., Kolanus, W., Quast, T., Kremmer, E., Bauer, I., and Famulok, M. (2006). Inhibition of cytohesins by SecinH3 leads to hepatic insulin resistance. Nature, 444, 941-944.
19. Hou, J. C., Shigematsu, S., Crawford, H. C., Anastasiadis, P. Z., and Pessin, J. E. (2006). Dual regulation of Rho and Rac by p120 catenin controls adipocyte plasma membrane trafficking. J. Biol. Chem., 281, 23307-23312.
20. Huang, J., Imamura, T. and Olefsky, J. M. (2001). Insulin can regulate GLUT4 internalization by signaling to Rab5 and the motor protein dynein. Proc. Natl. Acad. Sci. US, 98, 13084-13089.
21. Huang, S. and Czech, M. P. (2007). The GLUT4 glucose transporter. Cell Metab., 5, 237-252.
22. Imamura, T., Huang, J., Usui, I., Satoh, H., Bever, J. and Olefsky, J. M. (2003). Insulininduced GLUT4 translocation involves protein kinase C-lambda-mediated functional coupling between Rab4 and the motor protein kinesin. Mol. Cell. Biol., 23, 4892-4900.
23. Inoue, M., Chang, L., Hwang, J., Chiang, S. H., and Saltiel, A. R. (2003). The exocyst complex is required for targeting of Glut4 to the plasma membrane by insulin. Nature, 422, 629-633.
24. Ishikura, S. and Klip, A. (2008). Muscle cells engage Rab8A and myosin Vb in insulindependent GLUT4 translocation. Am. J. Physiol. Cell Physiol., 295, C1016-C1025.
25. JeBailey, L., Rudich, A., Huang, X., Di Ciano-Oliveira, C., Kapus, A., and Klip, A. (2004). Skeletal muscle cells and adipocytes differ in their reliance on TC10 and Rac for insulininduced actin remodeling. Mol. Endocrinol., 18, 359-372.
26. JeBailey, L., Wanono, O., Niu, W., Roessler, J., Rudich, A., and Klip, A. (2007). Ceramideand oxidant-induced insulin resistance involve loss of insulin-dependent Rac-activation and actin remodeling in muscle cells. Diabetes, 56, 394-403.
27. Kane, S., Sano, H., Liu, S. C., Asara, J. M., Lane, W. S., Garner, C. C., and Lienhard, G. E. (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, 22115-22118.
28. Kanzaki, M. and Pessin, J. E. (2001). Insulin-stimulated GLUT4 translocation in adipocytes is dependent upon cortical actin remodeling. J. Biol. Chem., 276, 42436-42444.
29. Kanzaki, M. and Pessin, J. E. (2003). Insulin signaling: GLUT4 vesicles exit via the exocyst. Curr. Biol., 13, R574-R576.
30. Kanzaki, M., Watson, R. T., Hou, J. C., Stamnes, M., Saltiel, A. R. and Pessin, J. E. (2002). Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes. Mol. Biol. Cell, 13, 2334-2346.
31. Karylowski, O., Zeigerer, A., Cohen, A., and McGraw, T. E. (2004). GLUT4 is retained by an intracellular cycle of vesicle formation and fusion with endosomes. Mol. Biol. Cell, 15, 870-882.
32. Khayat, Z. A., Tong, P., Yaworsky, K., Bloch, R. J., and Klip, A. (2000). Insulin-induced actin filament remodeling colocalizes actin with phosphatidylinositol 3-kinase and GLUT4 in L6 myotubes. J. Cell Sci., 113, 279-290.
33. Kramer, H. F., Witczak, C. A., Fujii, N., Jessen, N., Taylor, E. B., Arnolds, D. E., Sakamoto, K., Hirshman, M. F., and Goodyear, L. J. (2006a). Distinct signals regulate AS160 phosphorylation in response to insulin, AICAR, and contraction in mouse skeletal muscle. Diabetes, 55, 2067-2076.
34. Kramer, H. F., Witczak, C. A., Taylor, E. B., Fujii, N., Hirshman, M. F., and Goodyear, L. J. (2006b). AS160 regulates insulin-and contraction-stimulated glucose uptake in mouse skeletal muscle. J. Biol. Chem., 281, 31478-31485.
35. Larance, M., Ramm, G., Stöckli, J., van Dam, E. M., Winata, S., Wasinger, V., Simpson, F., Graham, M., Junutula, J. R., Guilhaus, M., and James, D. E. (2005). Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J. Biol. Chem., 280, 37803-37813.
36. Lewis, J. P., Palmer, N. D., Ellington, J. B., Divers, J., Ng, M. C., Lu, L., Langefeld, C. D., Freedman, B. I., and Bowden, D. W. (2010). Analysis of candidate genes on chromosome 20q12-13.1 reveals evidence for BMI mediated association of PREX1 with type 2 diabetes in European Americans. Genomics, 96, 211-219.
37. Li, J., Malaby, A. W., Famulok, M., Sabe, H., Lambright, D. G., and Hsu, V. W. (2012). Grp1 plays a key role in linking insulin signaling to glut4 recycling. Dev. Cell, 22, 1286-1298.
38. Lodhi, I. J., Chiang, S. H., Chang, L., Vollenweider, D., Watson, R. T., Inoue, M., Pessin, J. E., and Saltiel, A. R. (2007). Gapex-5, a Rab31 guanine nucleotide exchange factor that regulates Glut4 trafficking in adipocytes. Cell Metab., 5, 59-72.
39. Loubéry, S. and Coudrier, E. (2008). Myosins in the secretory pathway: tethers or transporters? Cell. Mol. Life Sci., 65, 2790-2800.
40. Moskalenko, S., Henry, D. O., Rosse, C., Mirey, G., Camonis, J. H. and White, M. A. (2002). The exocyst is a Ral effector complex. Nat. Cell Biol., 4, 66-72.
41. Nozaki, S., Ueda, S., Takenaka, N., Kataoka, T., and Satoh, T. (2012). Role of RalA downstream of Rac1 in insulin-dependent glucose uptake in muscle cells. Cell. Signal., 24, 2111-2117.
42. Nozaki, S., Takeda, T., Kitaura, T., Takenaka, N., Kataoka, T. and Satoh, T. (2013). Akt2 regulates Rac1 activity in the insulin-dependent signaling pathway leading to GLUT4 translocation to the plasma membrane in skeletal muscle cells. Cell. Signal., in press.
43. Ramm, G., Larance, M., Guilhaus, M., and James, D. E. (2006). A role for 14-3-3 in insulinstimulated GLUT4 translocation through its interaction with the RabGAP AS160. J. Biol. Chem., 281, 29174-29180.
44. Randhawa, V. K., Ishikura, S., Talior-Volodarsky, I., Cheng, A. W., Patel, N., Hartwig, J. H., and Klip, A. (2008). GLUT4 vesicle recruitment and fusion are differentially regulated by Rac, AS160, and Rab8A in muscle cells. J. Biol. Chem., 283, 27208-27219.
45. Roach, W. G., Chavez, J. A., Mîinea, C. P., and Lienhard, G. E. (2007). Substrate specificity and effect on GLUT4 translocation of the Rab GTPase-activating protein Tbc1d1. Biochem. J., 403, 353-358.
46. Roland, J. T., Bryant, D. M., Datta, A., Itzen, A., Mostov, K. E., and Goldenring, J. R. (2011). Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc. Natl. Acad. Sci. US, 108, 2789-2794.
47. Roland, J. T., Kenworthy, A. K., Peranen, J., Caplan, S., and Goldenring, J. R. (2007). Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol. Biol. Cell, 18, 2828-2837.
48. Saltiel, A. R. and Kahn, C. R. (2001). Insulin signalling and the regulation of glucose and lipid metabolism. Nature, 414, 799-806.
49. Sano, H., Eguez, L., Teruel, M. N., Fukuda, M., Chuang, T. D., Chavez, J. A., Lienhard, G. E., and McGraw, T. E. (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, 293-303.
50. Sano, H., Kane, S., Sano, E., Mîinea, C. P., Asara, J. M., Lane, W. S., Garner, C. W., and Lienhard, G. E. (2003). Insulin-stimulated phosphorylation of a Rab GTPase-activating protein regulates GLUT4 translocation. J. Biol. Chem., 278, 14599-14602.
51. Sano, H., Peck, G. R., Kettenbach, A. N., Gerber, S. A., and Lienhard, G. E. (2011). Insulinstimulated GLUT4 protein translocation in adipocytes requires the Rab10 guanine nucleotide exchange factor Dennd4C. J. Biol. Chem., 286, 16541-16545.
52. Schertzer, J. D., Antonescu, C. N., Bilan, P. J., Jain, S., Huang, X., Liu, Z., Bonen, A., and Klip, A. (2009). A transgenic mouse model to study glucose transporter 4myc regulation in skeletal muscle. Endocrinology, 150, 1935-1940.
53. Semiz, S., Park, J. G., Nicoloro, S. M., Furcinitti, P., Zhang, C., Chawla, A,, Leszyk, J., and Czech, M. P. (2003). Conventional kinesin KIF5B mediates insulin-stimulated GLUT4 movements on microtubules. EMBO J., 22, 2387-2399.
54. Sherman, L. A., Hirshman, M. F., Cormont, M., Le Marchand-Brustel, Y., and Goodyear, L. J. (1996). Differential effects of insulin and exercise on Rab4 distribution in rat skeletal muscle. Endocrinology, 137, 266-273.
55. Shibata, H., Omata, W. and Kojima, I. (1997). Insulin stimulates guanine nucleotide exchange on Rab4 via a wortmannin-sensitive signaling pathway in rat adipocytes. J. Biol. Chem., 272, 14542-14546.
56. Sugihara, K., Asano, S., Tanaka, K., Iwamatsu, A., Okawa, K., and Ohta, Y. (2002). The exocyst complex binds the small GTPase RalA to mediate filopodia formation. Nat. Cell Biol., 4, 73-78.
57. Sun, Y., Bilan, P. J., Liu, Z., and Klip, A. (2010). Rab8A and Rab13 are activated by insulin and regulate GLUT4 translocation in muscle cells. Proc. Natl. Acad. Sci. US, 107, 19909-19914.
58. Sylow, L., Jensen, T. E., Kleinert, M., Hojlund, K., Kiens, B., Wojtaszewski, J., Prats, C., Schjerling, P., and Richter, E. A. (2013a). Rac1 signaling is required for insulinstimulated glucose uptake and is dysregulated in insulin resistant murine and human skeletal muscle. Diabetes, in press.
59. Sylow, L., Jensen, T. E., Kleinert, M., Mouatt, J. R., Maarbjerg, S. J., Jeppesen, J., Prats, C., Chiu, T. T., Boguslavsky, S., Klip, A., Schjerling, P., and Richter, E. A. (2013b). Rac1 Is a novel regulator of contraction-stimulated glucose uptake in skeletal muscle. Diabetes, in press.
60. Takai, Y., Sasaki, T. and Matozaki, T. (2001). Small GTP-binding proteins. Physiol. Rev., 81, 153-208.
61. Tsakiridis, T., Vranic, M. and Klip, A. (1994). Disassembly of the actin network inhibits insulin-dependent stimulation of glucose transport and prevents recruitment of glucose transporters to the plasma membrane. J. Biol. Chem., 269, 29934-29942.
62. Ueda, S., Kataoka, T. and Satoh, T. (2008). Activation of the small GTPase Rac1 by a specific guanine-nucleotide-exchange factor suffices to induce glucose uptake into skeletal-muscle cells. Biol. Cell, 100, 645-657.
63. Ueda, S., Kitazawa, S., Ishida, K., Nishikawa, Y., Matsui, M., Matsumoto, H., Aoki, T., Nozaki, S., Takeda, T., Tamori, Y., Aiba, A., Kahn, C. R., Kataoka, T., and Satoh, T. (2010). Crucial role of the small GTPase Rac1 in insulin-stimulated translocation of glucose transporter 4 to the mouse skeletal muscle sarcolemma. FASEB J., 24, 2254-2261.
64. Uhlig, M., Passlack, W. and Eckel, J. (2005). Functional role of Rab11 in GLUT4 trafficking in cardiomyocytes. Mol. Cell. Endocrinol., 235, 1-9.
65. Vanhaesebroeck, B., Stephens, L. and Hawkins, P. (2012). PI3K signalling: the path to discovery and understanding. Nat. Rev. Mol. Cell. Biol., 13, 195-203.
66. Vollenweider, P., Martin, S. S., Haruta, T., Morris, A. J., Nelson, J. G., Cormont, M., Le Marchand-Brustel, Y., Rose, D. W., and Olefsky, J. M. (1997). The small guanosine triphosphate-binding protein Rab4 is involved in insulin-induced GLUT4 translocation and actin filament rearrangement in 3T3-L1 cells. Endocrinology, 138, 4941-4949.
67. Wang, Z., Oh, E., Clapp, D. W., Chernoff, J., and Thurmond, D. C. (2011). Inhibition or ablation of p21-activated kinase (PAK1) disrupts glucose homeostatic mechanisms in vivo. J. Biol. Chem., 286, 41359-41367.
68. Wennerberg, K., Rossman, K. L. and Der, C. J. (2005). The Ras superfamily at a glance. J. Cell Sci., 118, 843-846.
69. Wu, S., Mehta, S. Q., Pichaud, F., Bellen, H. J., and Quiocho, F. A. (2005). Sec15 interacts with Rab11 via a novel domain and affects Rab11 localization in vivo. Nat. Struct. Mol. Biol., 12, 879-885.
70. Yip, M. F., Ramm, G., Larance, M., Hoehn, K. L., Wagner, M. C., Guilhaus, M., and James, D. E. (2008). CaMKII-mediated phosphorylation of the myosin motor Myo1c is required for insulin-stimulated GLUT4 translocation in adipocytes. Cell Metab., 8, 384-398.
71. Yoshizaki, T., Imamura, T., Babendure, J. L., Lu, J. C., Sonoda, N., and Olefsky, J. M. (2007). Myosin 5a is an insulin-stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol. Cell. Biol., 27, 5172-5183.
72. Zeigerer, A., Lampson, M. A., Karylowski, O., Sabatini, D. D., Adesnik, M., Ren, M., and McGraw, T. E. (2002). GLUT4 retention in adipocytes requires two intracellular insulinregulated transport steps. Mol. Biol. Cell, 13, 2421-2435.
73. Zerial, M. and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell. Biol., 2, 107-117.
74. Zisman, A., Peroni, O. D., Abel, E. D., Michael, M. D., Mauvais-Jarvis, F., Lowell, B. B., Wojtaszewski, J. F., Hirshman, M. F., Virkamaki, A., Goodyear, L. J., Kahn, C. R., and Kahn, B. B. (2000). Targeted disruption of the glucose transporter 4 selectively in muscle causes insulin resistance and glucose intolerance. Nat. Med., 6, 924-928.