PERK utilizes intrinsic lipid kinase activity to generate phosphatidic acid, mediate Akt activation, and promote adipocyte differentiation

Molecular and Cellular Biology

Volumn 32, Issue 12, 2012, Pages 2268-2278

  Bobrovnikova Marjon, Ekaterina ^a,b   Pytel, Dariusz ^a,b   Riese, Matthew J ^a,b   Vaites, Laura Pontano ^a,b   Singh, Nickpreet ^a   Koretzky, Gary A ^a,b   Witze, Eric S ^a,b   Diehl, J Alan ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDIC ACID; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; PKR LIKE KINASE; PROTEIN KINASE B; PROTEIN P85; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; EMBRYO; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADIPOCYTES; ANIMALS; CELL DIFFERENTIATION; CELL LINE; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; LIPID METABOLISM; MICE; PHOSPHATIDIC ACIDS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84864003561     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00063-12     Document Type: Article

References (56)

1. Antonsson B. 1997. Phosphatidylinositol synthase from mammalian tissues. Biochim. Biophys. Acta 1348:179-186.
2. Avila-Flores A, Santos T, Rincon E, Merida I. 2005. Modulation of the mammalian target of rapamycin pathway by diacylglycerol kinaseproduced phosphatidic acid. J. Biol. Chem. 280:10091-10099.
3. Backer JM, et al. 1992. Phosphatidylinositol 3́ -kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11:3469-3479.
4. Besterman JM, Duronio V, Cuatrecasas P. 1986. Rapid formation of diacylglycerol from phosphatidylcholine: a pathway for generation of a second messenger. Proc. Natl. Acad. Sci. U. S. A. 83:6785-6789.
5. Bi M, et al. 2005. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 24:3470-3481. 6.
6. Blais JD, et al. 2006. Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol. Cell. Biol. 26:9517-9532. 7.
7. Bobrovnikova-Marjon E, et al. 2010. PERK promotes cancer cell proliferation and tumor growth by limiting oxidative DNA damage. Oncogene 29:3881-3895.
8. Bobrovnikova-Marjon E, et al. 2008. PERK-dependent regulation of lipogenesis during mouse mammary gland development and adipocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 105:16314-16319. 9.
9. Brachmann SM, et al. 2005. Role of phosphoinositide 3-kinase regulatory isoforms in development and actin rearrangement. Mol. Cell. Biol. 25: 2593-2606.
10. Bunney TD, Katan M. 2010. Phosphoinositide signalling in cancer: beyond PI3K and PTEN. Nat. Rev. Cancer 10:342-352.
11. Carpenter CL, et al. 1993. Phosphoinositide 3-kinase is activated by phosphopeptides that bind to the SH2 domains of the 85-kDa subunit. J. Biol. Chem. 268:9478-9483.
12. Cullinan SB, et al. 2003. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol. Cell. Biol. 23:7198-7209.
13. Dhand R, et al. 1994. PI 3-kinase: structural and functional analysis of intersubunit interactions. EMBO J. 13:511-521.
14. Edinger AL, Thompson CB. 2002. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol. Biol. Cell 13:2276-2288.
15. Elstrom RL, et al. 2004. Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 64:3892-3899.
16. Engelman JA, Luo J, Cantley LC. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7:606-619.
17. Fagone P, Jackowski S. 2009. Membrane phospholipid synthesis and endoplasmic reticulum function. J. Lipid Res. 50(Suppl.):S311-S316.
18. Fang Y, Vilella-Bach M, Bachmann R, Flanigan A, Chen J. 2001. Phosphatidic acid-mediated mitogenic activation ofmTORsignaling. Science 294:1942-1945.
19. Fernandez PM, et al. 2000. Overexpression of the glucose-regulated stress gene GRP78 in malignant but not benign human breast lesions. Breast Cancer Res. Treat. 59:15-26.
20. Foster DA, Xu L. 2003. Phospholipase D in cell proliferation and cancer. Mol. Cancer Res. 1:789-800.
21. Fu Z, Aronoff-Spencer E, Wu H, Gerfen GJ, Backer JM. 2004. The iSH2 domain of PI 3-kinase is a rigid tether for p110 and not a conformational switch. Arch. Biochem. Biophys. 432:244-251.
22. Gazit G, Lu J, Lee AS. 1999. De-regulation of GRP stress protein expression in human breast cancer cell lines. Breast Cancer Res. Treat. 54:135-146.
23. Gottlob K, et al. 2001. Inhibition of early apoptotic events by Akt/PKB is dependent on the first committed step of glycolysis and mitochondrial hexokinase. Genes Dev. 15:1406-1418.
24. Greene MW, et al. 2010. PKC{delta} is activated in a dietary model of steatohepatitis and regulates endoplasmic reticulum stress and cell death. J. Biol. Chem. 285:42115-42129.
25. Hamanaka RB, Bobrovnikova-Marjon E, Ji X, Liebhaber SA, Diehl JA. 2009. PERK-dependent regulation of IAP translation during ER stress. Oncogene 28:910-920.
26. Harding HP, Zhang Y, Ron D. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
27. Haze K, Yoshida H, Yanagi H, Yura T, Mori K. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10:3787-3799.
28. Hopewell R, Martin-Sanz P, Martin A, Saxton J, Brindley DN. 1985. Regulation of the translocation of phosphatidate phosphohydrolase between the cytosol and the endoplasmic reticulum of rat liver. Effects of unsaturated fatty acids, spermine, nucleotides, albumin and chlorpromazine. Biochem. J. 232:485-491.
29. Hu P, Han Z, Couvillon AD, Exton JH. 2004. Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J. Biol. Chem. 279:49420-49429
30. Kazemi S, et al. 2007. A novel function of eIF2alpha kinases as inducers of the phosphoinositide-3 kinase signaling pathway. Mol. Biol. Cell 18:3635-3644.
31. Lee AH, Scapa EF, Cohen DE, Glimcher LH. 2008. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320:1492-1496.
32. Li M, et al. 2000. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol. Cell. Biol. 20:5096-5106.
33. Merida I, Avila-Flores A, Merino E. 2008. Diacylglycerol kinases: at the hub of cell signalling. Biochem. J. 409:1-18.
34. Mor A, et al. 2007. The lymphocyte function-associated antigen-1 receptor costimulates plasma membrane Ras via phospholipase D2. Nat. Cell Biol. 9:713-719.
35. Nishioka T, Frohman MA, Matsuda M, Kiyokawa E. 2010. Heterogeneity of phosphatidic acid levels and distribution at the plasma membrane in living cells as visualized by a Foster resonance energy transfer (FRET) biosensor. J. Biol. Chem. 285:35979-35987.
36. Park SW, et al. 2010. The regulatory subunits of PI3K, p85alpha and p85beta, interact with XBP-1 and increase its nuclear translocation. Nat. Med. 16:429-437.
37. Payrastre B, et al. 2001. Phosphoinositides: key players in cell signalling, in time and space. Cell Signal. 13:377-387.
38. Rizzo MA, et al. 1999. Phospholipase D and its product, phosphatidic acid, mediate agonist-dependent raf-1 translocation to the plasma mem-brane and the activation of the mitogen-activated protein kinase pathway. J. Biol. Chem. 274:1131-1139.
39. Robey RB, Hay N. 2009. Is Akt the "Warburg kinase" ?-Akt-energy metabolism interactions and oncogenesis. Semin. Cancer Biol. 19:25-31.
40. Rossi F, Grzeskowiak M, Della Bianca V, Sbarbati A. 1991. De novo synthesis of diacylglycerol from glucose. A new pathway of signal transduction in human neutrophils stimulated during phagocytosis of betaglucan particles. J. Biol. Chem. 266:8034-8038.
41. Sasaki T, et al. 2009. Mammalian phosphoinositide kinases and phosphatases. Prog. Lipid Res. 48:307-343.
42. Scheuner D, et al. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
43. Schewe DM, Aguirre-Ghiso JA. 2008. ATF6alpha-Rheb-mTOR signaling promotes survival of dormant tumor cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 105:10519-10524.
44. Shi Y, et al. 1998. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18:7499-7509.
45. Sriburi R, Jackowski S, Mori K, Brewer JW. 2004. XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167:35-41.
46. Tirasophon W, Welihinda AA, Kaufman RJ. 1998. 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.
47. Tolias KF, Cantley LC. 1999. Pathways for phosphoinositide synthesis. Chem. Phys. Lipids 98:69-77.
48. Toschi A, et al. 2009. Regulation of mTORC1 and mTORC2 complex assembly by phosphatidic acid: competition with rapamycin. Mol. Cell. Biol. 29:1411-1420.
49. Wang L-P, Summers SA. 2003. Diabetes mellitus. Methods Mol. Med. 83:127-136.
50. Wang XZ, et al. 1998. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 17:5708-5717.
51. Wang Y, et al. 2000. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275:27013-27020.
52. Wieman HL, Wofford JA, Rathmell JC. 2007. Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking. Mol. Biol. Cell 18:1437-1446.
53. Winnay JN, Boucher J, Mori MA, Ueki K, Kahn CR. 2010. A regulatory subunit of phosphoinositide 3-kinase increases the nuclear accumulation of X-box-binding protein-1 to modulate the unfolded protein response. Nat. Med. 16:438-445.
54. Zhang C, et al. 2012. Glycerolipid signals alter mTOR complex 2 (mTORC2) to diminish insulin signaling. Proc. Natl. Acad. Sci. U. S. A. 109:1667-1672.
55. Zhao C, Du G, Skowronek K, Frohman MA, Bar-Sagi D. 2007. Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat. Cell Biol. 9:706-712.
56. Zhao JJ, et al. 2006. The p110alpha isoform of PI3K is essential for proper growth factor signaling and oncogenic transformation. Proc. Natl. Acad. Sci. U. S. A. 103:16296-16300.