Selective activation of the transcription factor ATF6 mediates endoplasmic reticulum proliferation triggered by a membrane protein

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 19, 2011, Pages 7832-7837

  Maiuolo, Jessica ^a   Bulotta, Stefania ^a   Verderio, Claudia ^b   Benfante, Roberta ^b   Borgese, Nica ^a,b  

^a UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Membrane biogenesis; Phospholipid biosynthesis; Tail anchored proteins

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CYTOCHROME B5; DOXYCYCLINE; GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; GENE CONTROL; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; LIPID BILAYER; MOLECULAR MECHANICS; PHOSPHOLIPID SYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 6; BASE SEQUENCE; CALCIUM; CYTOCHROMES B5; DNA-BINDING PROTEINS; DOXYCYCLINE; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; GREEN FLUORESCENT PROTEINS; HEAT-SHOCK PROTEINS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; PHOSPHATIDYLCHOLINES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE;

EID: 79956352017     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1101379108     Document Type: Article

References (36)

1. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529. (Pubitemid 46985379)
2. Cox JS, Chapman RE, Walter P (1997) The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol Biol Cell 8:1805-1814. (Pubitemid 27411143)
3. 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.
4. Bommiasamy H, et al. (2009) ATF6alpha induces XBP1-independent expansion of the endoplasmic reticulum. J Cell Sci 122:1626-1636.
5. Orrenius S, Ericsson JL, Ernster L (1965) Phenobarbital-induced synthesis of the microsomal drug-metabolizing enzyme system and its relationship to the proliferation of endoplasmic membranes. A morphological and biochemical study. J Cell Biol 25:627-639.
6. Schunck WH, et al. (1991) Comparison of two cytochromes P-450 from Candida maltosa: Primary structures, substrate specificities and effects of their expression in Saccharomyces cerevisiae on the proliferation of the endoplasmic reticulum. Eur J Cell Biol 55:336-345.
7. Szczesna-Skorupa E, Chen CD, Liu H, Kemper B (2004) Gene expression changes associated with the endoplasmic reticulum stress response induced by microsomal cytochrome p450 overproduction. J Biol Chem 279:13953-13961. (Pubitemid 38468928)
8. Vergères G, Yen TS, Aggeler J, Lausier J, Waskell L (1993) A model system for studying membrane biogenesis. Overexpression of cytochrome b5 in yeast results in marked proliferation of the intracellular membrane. J Cell Sci 106:249-259. (Pubitemid 23286797)
9. Menzel R, Vogel F, Kärgel E, Schunck WH (1997) Inducible membranes in yeast: Relation to the unfolded-protein-response pathway. Yeast 13:1211-1229. (Pubitemid 27468101)
10. Takewaka T, Zimmer T, Hirata A, Ohta A, Takagi M (1999) Null mutation in IRE1 gene inhibits overproduction of microsomal cytochrome P450Alk1 (CYP 52A3) and proliferation of the endoplasmic reticulum in Saccharomyces cerevisiae. J Biochem 125:507-514. (Pubitemid 29164223)
11. Larson LL, Parrish ML, Koning AJ, Wright RL (2002) Proliferation of the endoplasmic reticulum occurs normally in cells that lack a functional unfolded protein response. Yeast 19:373-392.
12. Li S, et al. (2009) Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 391:257-264.
13. Pahl HL, Baeuerle PA (1997) The ER-overload response: Activation of NF-kappa B. Trends Biochem Sci 22:63-67.
14. Borgese N, Francolini M, Snapp E (2006) Endoplasmic reticulum architecture: Structures in flux. Curr Opin Cell Biol 18:358-364. (Pubitemid 44016057)
15. Sprocati T, Ronchi P, Raimondi A, Francolini M, Borgese N (2006) Dynamic and reversible restructuring of the ER induced by PDMP in cultured cells. J Cell Sci 119: 3249-3260. (Pubitemid 44322138)
16. Stäubli W, Hess R, Weibel ER (1969) Correlated morphometric and biochemical studies on the liver cell. II. Effects of phenobarbital on rat hepatocytes. J Cell Biol 42:92-112.
17. Omura T, Takesue S (1970) A new method for simultaneous purification of cytochrome b5 and NADPH-cytochrome c reductase from rat liver microsomes. J Biochem 67:249-257.
18. Cheng KC, Schenkman JB (1982) Purification and characterization of two constitutive forms of rat liver microsomal cytochrome P-450. J Biol Chem 257:2378-2385.
19. Yamaguchi A, et al. (1999) Stress-associated endoplasmic reticulum protein 1 (SERP1)/Ribosome-associated membrane protein 4 (RAMP4) stabilizes membrane proteins during stress and facilitates subsequent glycosylation. J Cell Biol 147:1195-1204. (Pubitemid 30012806)
20. 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. (Pubitemid 29534025)
21. Ye J, et al. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6:1355-1364. (Pubitemid 32045928)
22. Okada T, Yoshida H, Akazawa R, Negishi M, Mori K (2002) Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem J 366:585-594. (Pubitemid 35001703)
23. Yamamoto K, et al. (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 13:365-376. (Pubitemid 47308680)
24. 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. (Pubitemid 30431563)
25. Parker R, et al. (2001) Identification of TFII-I as the endoplasmic reticulum stress response element binding factor ERSF: Its autoregulation by stress and interaction with ATF6. Mol Cell Biol 21:3220-3233. (Pubitemid 32298387)
26. Shen J, Chen X, Hendershot L, Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3:99-111. (Pubitemid 34778399)
27. Shen J, Snapp EL, Lippincott-Schwartz J, Prywes R (2005) Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol Cell Biol 25:921-932.
28. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326-332.
29. Pincus D, et al. (2010) BiP binding to the ER-stress sensor Ire1 tunes the homeostatic behavior of the unfolded protein response. PLoS Biol 8:e1000415.
30. DuRose JB, Tam AB, Niwa M (2006) Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol Biol Cell 17:3095-3107. (Pubitemid 43993512)
31. Schindler AJ, Schekman R (2009) In vitro reconstitution of ER-stress induced ATF6 transport in COPII vesicles. Proc Natl Acad Sci USA 106:17775-17780.
32. Goldstein JL, DeBose-Boyd RA, Brown MS (2006) Protein sensors for membrane sterols. Cell 124:35-46.
33. Ceppi P, et al. (2005) Two tail-anchored protein variants, differing in transmembrane domain length and intracellular sorting, interact differently with lipids. Proc Natl Acad Sci USA 102:16269-16274. (Pubitemid 41688903)
34. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911-917.
35. Mattson MP, Barger SW, Begley JG, Mark RJ (1995) Calcium, free radicals, and excitotoxic neuronal death in primary cell culture. Methods Cell Biol 46:187-216.
36. Verderio C, et al. (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41:599-610. (Pubitemid 38253071)