Phosphorylation of eIF2 alpha in Sf9 cells: A stress, survival and suicidal signal

Apoptosis

Volumn 15, Issue 6, 2010, Pages 679-692

  Aarti, Iyer ^a   Rajesh, Kamindla ^a   Ramaiah, Kolluru V A ^a  

^a UNIVERSITY OF HYDERABAD   (India)

Author keywords

Baculovirus; Bip; Caspase; Eif2 phosphorylation; Er and non er stressors; Sf9 cells

Indexed keywords

BENZYLOXYCARBONYL VALYLALANYLASPARTIC ACID FLUOROMETHYLKETONE; CASPASE; CASPASE INHIBITOR; CELL EXTRACT; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; PROTEIN P35; STRESS ACTIVATED PROTEIN KINASE; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BACULOVIRUS; CELL DEATH; CELL STIMULATION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE; GENE EXPRESSION; LEPIDOPTERA; NONHUMAN; OVARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; TRANSLATION REGULATION; VIRUS INFECTION;

ANIMALS; APOPTOSIS; CASPASES; CELL DEATH; CELL SURVIVAL; EUKARYOTIC INITIATION FACTOR-2; INSECT PROTEINS; NUCLEOPOLYHEDROVIRUS; PHOSPHORYLATION; SPODOPTERA; STRESS, PHYSIOLOGICAL;

EUKARYOTA; SPODOPTERA FRUGIPERDA;

EID: 77954620534     PISSN: 13608185     EISSN: 1573675X     Source Type: Journal    
DOI: 10.1007/s10495-010-0474-z     Document Type: Article

References (67)

1. Hinnebusch AG (2005) Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59:407-450
2. Wek RC, Jiang HY, Anthony TG (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34:7-11
3. Chen JJ, London IM (1995) Regulation of protein synthesis by heme-regulated eIF-2 alpha kinase. Trends Biochem Sci 20:105-108
4. Wu S, Kaufman RJ (1997) A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-activated protein kinase PKR. J Biol Chem 272:1291-1296
5. Garća MA, Meurs EF, Esteban M (2007) The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811
6. Wek RC (1994) eIF-2 kinases: regulators of general and gene-specific translation initiation. Trends Biochem Sci 19: 491-496
7. Marciniak SJ, Ron D (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86:1133-1149
8. Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13:1211-1233
9. Hussain SG, Ramaiah KV (2007) Endoplasmic reticulum: stress, signaling and apoptosis. Sci 93:1684-1696
10. Dever TE (2002) Gene-specific regulation by general translation factors. Cell 108:545-556
11. Kaufman RJ (2004) Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends Biochem Sci 29:152-158
12. Holcik M, Sonenberg N (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327
13. Suragani RN, Kamindla R, Ehtesham NZ, Ramaiah KV (2005) Interaction of recombinant human eIF2 subunits with eIF2B and eIF2alpha kinases. Biochem Biophys Res Commun 338:1766-1772
14. Rajesh K, Iyer A, Suragani RN, Ramaiah KV (2008) Intersubunit and interprotein interactions of alpha-and beta-subunits of human eIF2: effect of phosphorylation. Biochem Biophys Res Commun 374:336-340
15. Clemens MJ, Pain VM, Wong ST, Henshaw EC (1982) Phos-phorylation inhibits guanine nucleotide exchange on eukaryotic initiation factor 2. Nature 296:93-95
16. Matts RL, London IM (1984) The regulation of initiation of protein synthesis by phosphorylation of eIF-2(alpha) and the role of reversing factor in the recycling of eIF-2. J Biol Chem 259:6708-6711
17. Ramaiah KV, Davies MV, Chen JJ, Kaufman RJ (1994) Expression of mutant eukaryotic initiation factor 2 alpha subunit (eIF-2 alpha) reduces inhibition of guanine nucleotide exchange activity of eIF-2B mediated by eIF-2 alpha phosphorylation. Mol Cell Biol 14:4546-4553
18. Sudhakar A, Ramachandran A, Ghosh S, Hasnain SE, Kaufman RJ, Ramaiah KV (2000) Phosphorylation of serine 51 in initiation factor 2 alpha (eIF2 alpha) promotes complex formation between eIF2 alpha(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39:12929-12938
19. Vattem KM, Wek RC (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci USA 101:11269-11274
20. Dever TE, Yang W, Aström S, Byström AS, Hinnebusch AG (1995) Modulation of tRNA(iMet), eIF-2, and eIF-2B expression shows that GCN4 translation is inversely coupled to the level of eIF-2.GTP.Met-tRNA(iMet) ternary complexes. Mol Cell Biol 15:6351-6363
21. Hinnebusch AG, Natarajan K (2002) Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot Cell 1:22-32
22. Rutkowski DT, Kaufman RJ (2003) All roads lead to ATF4. Dev Cell 4:442-444
23. Yan N, Shi Y (2005) Mechanisms of apoptosis through structural biology. Annu Rev Cell Dev Biol 21:35-56
24. Beere HM (2004) "The stress of dying": the role of heat shock proteins in the regulation of apoptosis. J Cell Sci 117:2641-2651
25. Beere HM (2005) Death versus survival: functional interaction between the apoptotic and stress-inducible heat shock protein pathways. J Clin Invest 115:2633-2639
26. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529
27. Wu J, Kaufman RJ (2006) From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 13:374-384
28. Donzé O, Picard D (1999) Hsp90 binds and regulates Gcn2, the ligand-inducible kinase of the alpha subunit of eukaryotic translation initiation factor 2. Mol Cell Biol 19:8422-8432
29. Donzé O, Abbas-Terki T, Picard D (2001) The Hsp90 chaperone complex is both a facilitator and a repressor of the dsRNA-dependent kinase PKR. EMBO J 20:3771-3780
30. Matts RL, Xu Z, Pal JK, Chen JJ (1992) Interactions of the heme-regulated eIF-2 alpha kinase with heat shock proteins in rabbit reticulocyte lysates. J Biol Chem 267:18160-18167
31. Matts RL, Hurst R, Xu Z (1993) Denatured proteins inhibit translation in hemin-supplemented rabbit reticulocyte lysate by inducing the activation of the heme-regulated eIF-2 alpha kinase. Biochemistry 32:7323-7328
32. Uma S, Barret DJ, Matts RL (1998) Changes in the expression of the heme-regulated eIF-2 alpha kinase and heat shock proteins in rabbit reticulocytes maturing during recovery from anemia. Exp Cell Res 238:273-282
33. Thulasiraman V, Xu Z, Uma S, Gu Y, Chen JJ, Matts RL (1998) Evidence that Hsc70 negatively modulates the activation of the heme-regulated eIF-2alpha kinase in rabbit reticulocyte lysate. Eur J Biochem 255:552-562
34. Scheuner D, Kaufman RJ (2008) The unfolded protein response: a pathway that links insulin demand with beta-cell failure and diabetes. Endocr Rev 29:317-333
35. Harding HP, Ron D (2002) Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51:S455-S461 (Pubitemid 35403430)
36. Scheuner D, Vander Mierde D, Song B, Flamez D, Creemers JW, Tsukamoto K, Ribick M, Schuit FC, Kaufman RJ (2005) Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat Med 11:757-764
37. Costa-Mattioli M (2008) Switching memories ON and OFF. Science 322:874-875
38. Zhang P, McGrath B, Li S, Frank A, Zambito F, Reinert J, Gannon M, Ma K, Mc Naughton K, Cavener DR (2002) The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol Cell Biol 22:3864-3874
39. Han AP, Yu C, Lu L, Fujiwara Y, Browne C, Chin G, Fleming M, Leboulch P, Orkin SH, Chen JJ (2001) Heme-regulated eIF2alpha kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J 20:6909-6918
40. Hussain SG, Ramaiah KV (2007) Reduced eIF2alpha phosphor-ylation and increased proapoptotic proteins in aging. Biochem Biophys Res Commun 355:365-370
41. Srivastava SP, Kumar KU, Kaufman RJ (1998) Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J Biol Chem 273:2416-2423
42. Scheuner D, Patel R, Wang F, Lee K, Kumar K, Wu J, Nilsson A, Karin M, Kaufman RJ (2006) Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 281:21458-21468
43. Ron D (2002) Translational control in the endoplasmic reticulum stress response. J Clin Invest 110:1383-1388 (Pubitemid 35396906)
44. Saelens X, Kalai M, Vandenabeele P (2001) Translation inhibition in apoptosis: caspase-dependent PKR activation and eIF2-alpha phosphorylation. J Biol Chem 276:41620-41628
45. Aparna G, Bhuyan AK, Sahdev S, Hasnain SE, Kaufman RJ, Ramaiah KV (2003) Stress-induced apoptosis in Spodoptera frugiperda (Sf9) cells: baculovirus p35 mitigates eIF2 alpha phosphorylation. Biochemistry 42:15352-15360
46. Hasnain SE, Begum R, Ramaiah KV, Sahdev S, Shajil EM, Taneja TK, Mohan M, Athar M, Sah NK, Krishnaveni M (2003) Hostpathogen interactions during apoptosis. J Biosci 28:349-358
47. Suragani RN, Ghosh S, Ehtesham NZ, Ramaiah KV (2006) Expression and purification of the subunits of human translational initiation factor 2 (eIF2): phosphorylation of eIF2 alpha and beta. Protein Expr Purif 47:225-233
48. Dever TE, Sripriya R, McLachlin JR, Lu J, Fabian JR, Kimball SR, Miller LK (1998) Disruption of cellular translational control by a viral truncated eukaryotic translation initiation factor 2alpha kinase homolog. Proc Natl Acad Sci USA 95:4164-4169
49. Li Y, Miller LK (1995) Expression and functional analysis of a baculovirus gene encoding a truncated protein kinase homolog. Virology 206:314-323
50. Boyce M, Bryant KF, Jousse C, Long K, Harding HP, Scheuner D, Kaufman RJ, Ma D, Coen DM, Ron D, Yuan J (2005) A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307:935-939
51. Sudhakar A, Krishnamoorthy T, Jain A, Chatterjee U, Hasnain SE, Kaufman RJ, Ramaiah KV (1999) Serine 48 in initiation factor 2 alpha (eIF2 alpha) is required for high-affinity interaction between eIF2 alpha(P) and eIF2B. Biochemistry 38:15398-15405
52. Liu J, Lin A (2005) Role of JNK activation in apoptosis: a double-edged sword. Cell Res 5:36-42
53. Oyadomari S, Mori M (2004) Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ 11:381-389
54. Lin A (2003) Activation of the JNK signaling pathway: breaking the brake on apoptosis. Bioessays 25:17-24
55. Dudek J, Benedix J, Cappel S, Greiner M, Jalal C, Müller L, Zimmermann R (2009) Functions and pathologies of BiP and its interaction partners. Cell Mol Life Sci 66:1556-1569
56. Dong D, Ni M, Li J, Xiong S, Ye W, Virrey JJ, Mao C, Ye R, Wang M, Pen L, Dubeau L, Groshen S, Hofman FM, Lee AS (2008) Critical role of the stress chaperone GRP78/BiP in tumor proliferation, survival, and tumor angiogenesis in transgene-induced mammary tumor development. Cancer Res 68:498-505
57. Li J, Lee AS (2006) Stress induction of GRP78/BiP and its role in cancer. Curr Mol Med 6:45-54
58. Luo S, Mao C, Lee B, Lee AS (2006) GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apop-tosis during early mouse embryonic development. Mol Cell Biol 26:5688-5697
59. Ranganathan AC, Zhang L, Adam AP, Aguirre-Ghiso JA (2006) Functional coupling of p38-induced up-regulation of BiP and activation of RNA-dependent protein kinase-like endoplasmic reticulum kinase to drug resistance of dormant carcinoma cells. Cancer Res 66:1702-1711
60. Fu Y, Li J, Lee AS (2007) GRP78/BiP inhibits endoplasmic reticulum BIK and protects human breast cancer cells against estrogen starvation-induced apoptosis. Cancer Res 67:3734-3740
61. Reddy RK, Mao C, Baumeister P, Austin RC, Kaufman RJ, Lee AS (2003) Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors: role of ATP binding site in suppression of caspase-7 activation. J Biol Chem 278:20915-20924
62. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, Goldsmith PC, Ellerby LM, Ellerby HM, Bredesen DE (2002) Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett 514:122-128
63. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jung-reis R, Nagata K, Harding HP, Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18:3066-3077
64. Liu Q, Chejanovsky N (2006) Activation pathways and signal-mediated upregulation of the insect Spodoptera frugiperda cas-pase-1. Apoptosis 11:487-496
65. Pomar N, Berlanga JJ, Campuzano S, Hernández G, Eĺas M, de Haro C (2003) Functional characterization of Drosophila mela-nogaster PERK eukaryotic initiation factor 2alpha (eIF2alpha) kinase. Eur J Biochem 270:293-306
66. Prasad MD, Han SJ, Nagaraju J, Lee WJ, Brey PT (2003) Cloning and characterization of an eukaryotic initiation factor-2alpha kinase from the silkworm, Bombyx mori. Biochim Biophys Acta 1628:56-63
67. Marissen WE, Guo Y, Thomas AA, Matts RL, Lloyd RE (2000) Identification of caspase 3-mediated cleavage and functional alteration of eukaryotic initiation factor 2alpha in apoptosis. J Biol Chem 275:9314-9323