A crucial role for RACK1 in the regulation of glucose-stimulated IRE1α activation in pancreatic β cells

Science Signaling

Volumn 3, Issue 106, 2010, Pages

  Qiu, Yifu ^a   Mao, Ting ^a   Zhang, Yongliang ^a   Shao, Mengle ^a   You, Jia ^a   Ding, Qiurong ^a   Chen, Yan ^a   Wu, Dongmei ^a   Xie, Dong ^a   Lin, Xu ^a   Gao, Xiang ^b   Kaufman, Randal J ^c   Li, Wenjun ^a   Liu, Yong ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^b NANJING UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN IRE1; PROTEIN IRE1ALPHA; RECEPTOR FOR ACTIVATED C KINASE 1; UNCLASSIFIED DRUG; CELL SURFACE RECEPTOR; GNB2L1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; IRE1ALPHA PROTEIN, HUMAN; MULTIPROTEIN COMPLEX; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN SERINE THREONINE KINASE; RIBONUCLEASE; TUMOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHOSPHORYLATION; COMPLEX FORMATION; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME REGULATION; INSULIN SYNTHESIS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL LINE; CELL STRAIN HT29; DRUG EFFECT; ENDOPLASMIC RETICULUM; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; MORBID OBESITY; PANCREAS ISLET; PHOSPHORYLATION; PROTEIN BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TWO HYBRID SYSTEM; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; FEMALE; GLUCOSE; GTP-BINDING PROTEINS; HT29 CELLS; HUMANS; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; OBESITY, MORBID; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN PHOSPHATASE 2; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 77951645463     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000514     Document Type: Article

References (51)

1. D. Ron, P. Walter, Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529 (2007).
2. J. S. Cox, C. E. Shamu, P. Walter, Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73, 1197-1206 (1993).
3. +/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756 (1993).
4. H. Yoshida, T. Matsui, A. Yamamoto, T. Okada, K. Mori, XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891 (2001).
5. M. Calfon, H. Zeng, F. Urano, J. H. Till, S. R. Hubbard, H. P. Harding, S. G. Clark, D. Ron, IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96 (2002).
6. A. M. Reimold, N. N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E. M. Gravallese, D. Friend, M. J. Grusby, F. Alt, L. H. Glimcher, Plasma cell differentiation requires the transcription factor XBP-1. Nature 412, 300-307 (2001).
7. N. N. Iwakoshi, A. H. Lee, P. Vallabhajosyula, K. L. Otipoby, K. Rajewsky, L. H. Glimcher, Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4, 321-329 (2003).
8. K. Zhang, H. N. Wong, B. Song, C. N. Miller, D. Scheuner, R. J. Kaufman, The unfolded protein response sensor IRE1a is required at 2 distinct steps in B cell lymphopoiesis. J. Clin. Invest. 115, 268-281 (2005).
9. J. H. Lin, H. Li, D. Yasumura, H. R. Cohen, C. Zhang, B. Panning, K. M. Shokat, M. M. Lavail, P. Walter, IRE1 signaling affects cell fate during the unfolded protein response. Science 318, 944-949 (2007).
10. K. L. Lipson, S. G. Fonseca, S. Ishigaki, L. X. Nguyen, E. Foss, R. Bortell, A. A. Rossini, F. Urano, Regulation of insulin biosynthesis in pancreatic beta cells by an endoplasmic reticulum-resident protein kinase IRE1. Cell Metab. 4, 245-254 (2006).
11. U. Ozcan, Q. Cao, E. Yilmaz, A. H. Lee, N. N. Iwakoshi, E. Ozdelen, G. Tuncman, C. Gorgun, L. H. Glimcher, G. S. Hotamisligil, Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306, 457-461 (2004).
12. U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R. O. Smith, C. Z. Görgün, G. S. Hotamisligil, Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137-1140 (2006).
13. D. Scheuner, R. J. Kaufman, The unfolded protein response: A pathway that links insulin demand with β-cell failure and diabetes. Endocr. Rev. 29, 317-333 (2008).
14. D. L. Eizirik, A. K. Cardozo, M. Cnop, The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 29, 42-61 (2008).
15. D. Ron, C. H. Chen, J. Caldwell, L. Jamieson, E. Orr, D. Mochly-Rosen, Cloning of an intracellular receptor for protein kinase C: A homolog of the β subunit of G proteins. Proc. Natl. Acad. Sci. U. S. A. 91, 839-843 (1994).
16. A. McCahill, J. Warwicker, G. B. Bolger, M. D. Houslay, S. J. Yarwood, The RACK1 scaffold protein: A dynamic cog in cell response mechanisms. Mol. Pharmacol. 62, 1261-1273 (2002).
17. K. Arimoto, H. Fukuda, S. Imajoh-Ohmi, H. Saito, M. Takekawa, Formation of stress granules inhibits apoptosis by suppressing stress-responsive MAPK pathways. Nat. Cell Biol. 10, 1324-1332 (2008).
18. P. López-Bergami, H. Habelhah, A. Bhoumik, W. Zhang, L. H. Wang, Z. Ronai, RACK1 mediates activation of JNK by protein kinase C. Mol. Cell 19, 309-320 (2005).
19. A. H. Lee, N. N. Iwakoshi, L. H. Glimcher, XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459 (2003).
20. E. Gomez, M. L. Powell, I. C. Greenman, T. P. Herbert, Glucose-stimulated protein synthesis in pancreatic β-cells parallels an increase in the availability of the translational ternary complex (eIF2-GTP. Met-tRNAi) and the dephosphorylation of eIF2α. J. Biol. Chem. 279, 53937-53946 (2004).
21. D. Vander Mierde, D. Scheuner, R. Quintens, R. Patel, B. Song, K. Tsukamoto, M. Beullens, R. J. Kaufman, M. Bollen, F. C. Schuit, Glucose activates a protein phosphatase-1-mediated signaling pathway to enhance overall translation in pancreatic β-cells. Endocrinology 148, 609-617 (2007).
22. S. C. Martinez, K. Tanabe, C. Cras-Meneur, N. A. Abumrad, E. Bernal-Mizrachi, M. A. Permutt, Inhibition of Foxo1 protects pancreatic islet β-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 57, 846-859 (2008).
23. S. Khoo, M. H. Cobb, Activation of mitogen-activating protein kinase by glucose is not required for insulin secretion. Proc. Natl. Acad. Sci. U. S. A. 94, 5599-5604 (1997).
24. D. Arnette, T. B. Gibson, M. C. Lawrence, B. January, S. Khoo, K. McGlynn, C. A. Vanderbilt, M. H. Cobb, Regulation of ERK1 and ERK2 by glucose and peptide hormones in pancreatic β cells. J. Biol. Chem. 278, 32517-32525 (2003). (Pubitemid 37055689)
25. J. Zhou, C. Y. Liu, S. H. Back, R. L. Clark, D. Peisach, Z. Xu, R. J. Kaufman, The crystal structure of human IRE1 luminal domain reveals a conserved dimerization interface required for activation of the unfolded protein response. Proc. Natl. Acad. Sci. U. S. A. 103, 14343-14348 (2006).
26. W. Tirasophon, A. A. Welihinda, R. J. Kaufman, A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 12, 1812-1824 (1998).
27. W. Tirasophon, K. Lee, B. Callaghan, A. Welihinda, R. J. Kaufman, The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 14, 2725-2736 (2000).
28. P. A. Kiely, D. O'Gorman, K. Luong, D. Ron, R. O'Connor, Insulin-like growth factor I controls a mutually exclusive association of RACK1 with protein phosphatase 2A and β1 integrin to promote cell migration. Mol. Cell. Biol. 26, 4041-4051 (2006).
29. I. Novoa, H. Zeng, H. P. Harding, D. Ron, Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153, 1011-1022 (2001).
30. A. A. Welihinda, W. Tirasophon, S. R. Green, R. J. Kaufman, Protein serine/threonine phosphatase Ptc2p negatively regulates the unfolded-protein response by dephosphorylating Ire1p kinase. Mol. Cell. Biol. 18, 1967-1977 (1998). (Pubitemid 28152645)
31. J. Guo, M. Polymenis, Dcr2 targets Ire1 and downregulates the unfolded protein response in Saccharomyces cerevisiae. EMBO Rep. 7, 1124-1127 (2006).
32. H. Puthalakath, L. A. O'Reilly, P. Gunn, L. Lee, P. N. Kelly, N. D. Huntington, P. D. Hughes, E. M. Michalak, J. McKimm-Breschkin, N. Motoyama, T. Gotoh, S. Akira, P. Bouillet, A. Strasser, ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129, 1337-1349 (2007).
33. J. Hollien, J. S. Weissman, Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313, 104-107 (2006).
34. K. L. Lipson, R. Ghosh, F. Urano, The role of IRE1α in the degradation of insulin mRNA in pancreatic β-cells. PLoS One 3, e1648 (2008).
35. D. Han, A. G. Lerner, L. Vande Walle, J. P. Upton, W. Xu, A. Hagen, B. J. Backes, S. A. Oakes, F. R. Papa, IRE1α kinase activation modes control alternate endoribonuclease outputs to determine divergent cell fates. Cell 138, 562-575 (2009).
36. J. Hollien, J. H. Lin, H. Li, N. Stevens, P. Walter, J. S. Weissman, Regulated Ire1-dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186, 323-331 (2009).
37. J. M. Friedman, J. L. Halaas, Leptin and the regulation of body weight in mammals. Nature 395, 763-770 (1998).
38. K. P. Hummel, D. L. Coleman, P. W. Lane, The influence of genetic background on expression of mutations at the diabetes locus in the mouse. I. C57BL-KsJ and C57BL-6J strains. Biochem. Genet. 7, 1-13 (1972).
39. A. V. Korennykh, P. F. Egea, A. A. Korostelev, J. Finer-Moore, C. Zhang, K. M. Shokat, R. M. Stroud, P. Walter, The unfolded protein response signals through high-order assembly of Ire1. Nature 457, 687-693 (2009).
40. P. A. Kiely, G. S. Baillie, M. J. Lynch, M. D. Houslay, R. O'Connor, Tyrosine 302 in RACK1 is essential for insulin-like growth factor-I-mediated competitive binding of PP2A and β1 integrin and for tumor cell proliferation and migration. J. Biol. Chem. 283, 22952-22961 (2008).
41. F. Urano, X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, D. Ron, Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666 (2000).
42. T. Yoneda, K. Imaizumi, K. Oono, D. Yui, F. Gomi, T. Katayama, M. Tohyama, Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 276, 13935-13940 (2001).
43. C. Hetz, P. Bernasconi, J. Fisher, A. H. Lee, M. C. Bassik, B. Antonsson, G. S. Brandt, N. N. Iwakoshi, A. Schinzel, L. H. Glimcher, S. J. Korsmeyer, Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1α. Science 312, 572-576 (2006).
44. F. Lisbona, D. Rojas-Rivera, P. Thielen, S. Zamorano, D. Todd, F. Martinon, A. Glavic, C. Kress, J. H. Lin, P. Walter, J. C. Reed, L. H. Glimcher, C. Hetz, BAX inhibitor-1 is a negative regulator of the ER stress sensor IRE1α. Mol. Cell 33, 679-691 (2009).
45. J. H. Lin, P. Walter, T. S. Yen, Endoplasmic reticulum stress in disease pathogenesis. Annu. Rev. Pathol. 3, 399-425 (2008).
46. W. T. Godbey, K. K. Wu, G. J. Hirasaki, A. G. Mikos, Improved packingofpoly (ethylenimine)/DNA complexes increases transfection efficiency. Gene Ther. 6, 1380-1388 (1999).
47. H. Wang, P. B. Iynedjian, Modulation of glucose responsiveness of insulinoma β-cells by graded overexpression of glucokinase. Proc. Natl. Acad. Sci. U. S. A. 94, 4372-4377 (1997). (Pubitemid 27194248)
48. H. E. Hohmeier, H. Mulder, G. Chen, R. Henkel-Rieger, M. Prentki, C. B. Newgard, Isolation of INS-1-derived cell lines with robust ATP-sensitive K channel-dependent and -independent glucose-stimulated insulin secretion. Diabetes 49, 424-430 (2000).
49. L. Jiang, J. You, X. Yu, L. Gonzalez, Y. Yu, Q. Wang, G. Yang, W. Li, C. Li, Y. Liu, Tyrosine-dependent and -independent actions of leptin receptor in control of energy balance and glucose homeostasis. Proc. Natl. Acad. Sci. U. S. A. 105, 18619-18624 (2008).
50. Z. Gan, L. Zhao, L. Yang, P. Huang, F. Zhao, W. Li, Y. Liu, RNA editing by ADAR2 is metabolically regulated in pancreatic islets and β-cells. J. Biol. Chem. 281, 33386-33394 (2006).
51. This work was supported by grants from National Natural Science Foundation (Nos. 90713027, 30830033, and 30988002), the Ministry of Science and Technology (973 Program 2006CB503900 and 2007CB947100), Chinese Academy of Sciences (The Knowledge Innovation Programs Nos. KSCX1-YW-02 and KSCX2-YW-R-115, the CS program-SIBS2008006, and the CAS/SAFEA (State Administration of Foreign Experts Affairs) International Partnership Program), and Science and Technology Commission of Shanghai Municipality (No. 08dj1400601) to Y. L. and W. L., and the Ministry of Science and Technology (No. 2006BAI23B00) to X. G. Portions of this work were supported by NIH grants DK042394, HL052173, and HL057346 to R. J. K. R. J. K. is an investigator of the Howard Hughes Medical Institute. We thank J. Zhou for providing the Myc antibody, and L. Rui, Z. Liu, and C. E. Samuel for critical reading of the manuscript.