Rab6 is a modulator of the unfolded protein response: Implications for Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 28, Issue 4, 2012, Pages 917-929

  Elfrink, Hyung Lim ^a   Zwart, Rob ^a   Cavanillas, María L ^a   Schindler, Adam Jay ^b   Baas, Frank ^a   Scheper, Wiep ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b DUKE UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; endoplasmic reticulum stress; Rab6; unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; MESSENGER RNA; PROTEIN RAB6; RAB PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DEGENERATIVE DISEASE; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84858022581     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-110971     Document Type: Article

References (39)

1. Hoozemans JJ, Veerhuis R, van Haastert ES, Rozemuller JM, Baas F, Eikelenboom P, Scheper W (2005) The unfolded protein response is activated in Alzheimer's disease. Acta Neuropathol 110, 165-172. (Pubitemid 41245205)
2. Hoozemans JJ, van Haastert ES, Nijholt DA, Rozemuller AJ, Eikelenboom P, Scheper W (2009) The unfolded protein response is activated in pretangle neurons in Alzheimer's disease hippocampus. Am J Pathol 174, 1241-1251.
3. Kaufman RJ (1999) Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev 13, 1211-1233.
4. Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8, 519-529. (Pubitemid 46985379)
5. Yoshida H, Haze K, Yanagi H, Yura T, Mori K (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273, 33741-33749.
6. Yamamoto K, Yoshida H, Kokame K, Kaufman RJ, Mori K (2004) Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem 136, 343-350. (Pubitemid 39545794)
7. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258.
8. Ng DT, Spear ED, Walter P (2000) The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150, 77-88. (Pubitemid 30480228)
9. Yorimitsu T, Nair U, Yang Z, Klionsky DJ (2006) Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281, 30299-30304. (Pubitemid 44537037)
10. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, Shiosaka S, Hammarback JA, Urano F, Imaizumi K (2006) Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26, 9220-9231. (Pubitemid 44904418)
11. Ding WX, Ni HM, Gao W, Hou YF, Melan MA, Chen X, Stolz DB, Shao ZM, Yin XM (2007) Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem 282, 4702-4710. (Pubitemid 47101001)
12. Wang XZ, Lawson B, Brewer JW, Zinszner H, Sanjay A, Mi LJ, Boorstein R, Kreibich G, Hendershot LM, Ron D (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16, 4273-4280. (Pubitemid 26251229)
13. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12, 982-995. (Pubitemid 28204605)
14. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91, 119-149.
15. Martinez O, Antony C, Pehau-Arnaudet G, Berger EG, Salamero J, Goud B (1997) GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc Natl Acad Sci U S A 94, 1828-1833. (Pubitemid 27113921)
16. Girod A, Storrie B, Simpson JC, Johannes L, Goud B, Roberts LM, Lord JM, Nilsson T, Pepperkok R (1999) Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum. Nat Cell Biol 1, 423-430. (Pubitemid 129502809)
17. White J, Johannes L, Mallard F, Girod A, Grill S, Reinsch S, Keller P, Tzschaschel B, Echard A, Goud B, Stelzer EH (1999) Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J Cell Biol 147, 743-760.
18. Darchen F, Goud B (2000) Multiple aspects of Rab protein action in the secretory pathway: Focus on Rab3 and Rab6. Biochimie 82, 375-384. (Pubitemid 30391915)
19. Grigoriev I, Splinter D, Keijzer N, Wulf PS, Demmers J, Ohtsuka T, Modesti M, Maly IV, Grosveld F, Hoogenraad CC, Akhmanova A (2007) Rab6 regulates transport and targeting of exocytotic carriers. Dev Cell 13, 305-314. (Pubitemid 47163607)
20. Scheper W, Hoozemans JJ, Hoogenraad CC, Rozemuller AJ, Eikelenboom P, Baas F (2007) Rab6 is increased in Alzheimer's disease brain and correlates with endoplasmic reticulum stress. Neuropathol Appl Neurobiol 33, 523-532. (Pubitemid 47390081)
21. Matanis T, Akhmanova A, Wulf P, Del NE, Weide T, Stepanova T, Galjart N, Grosveld F, Goud B, De Zeeuw CI, Barnekow A, Hoogenraad CC (2002) Bicaudal-D regulates COPI-independent Golgi-ER transport by recruiting the dynein-dynactin motor complex. Nat Cell Biol 4, 986-992. (Pubitemid 35469430)
22. Schindler AJ, Schekman R (2009) In vitro reconstitution of ER-stress induced ATF6 transport in COPII vesicles. Proc Natl Acad Sci U S A 106, 17775-17780.
23. Young J, Stauber T, Del NE, Vernos I, Pepperkok R, Nilsson T (2005) Regulation of microtubule-dependent recycling at the trans-Golgi network by Rab6A and Rab6A'. Mol Biol Cell 16, 162-177. (Pubitemid 40024300)
24. Nijholt DA, de Graaf TR, van Haastert ES, Oliveira AO, Berkers CR, Zwart R, Ovaa H, Baas F, Hoozemans JJ, Scheper W (2011) Endoplasmic reticulum stress activates autophagy but not the proteasome in neuronal cells: Implications for Alzheimer's disease. Cell Death Differ 18, 1071-1081.
25. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, Moorman AF (2009) Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37, e45.
26. Zhang K, Kaufman RJ (2004) Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem 279, 25935-25938. (Pubitemid 38798732)
27. Novoa I, Zeng H, Harding HP, Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153, 1011-1022.
28. Ma Y, Hendershot LM (2003) Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J Biol Chem 278, 34864-34873. (Pubitemid 37102245)
29. Rubio C, Pincus D, Korennykh A, Schuck S, El-Samad H, Walter P (2011) Homeostatic adaptation to endoplasmic reticulum stress depends on Ire1 kinase activity. J Cell Biol 193, 171-184.
30. Chawla A, Chakrabarti S, Ghosh G, Niwa M (2011) Attenuation of yeast UPR is essential for survival and is mediated by IRE1 kinase. J Cell Biol 193, 41-50.
31. Miserey-Lenkei S, Chalancon G, Bardin S, Formstecher E, Goud B, Echard A (2010) Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12, 645-654.
32. Schuck S, Prinz WA, Thorn KS, Voss C, Walter P (2009) Membrane expansion alleviates endoplasmic reticulum stress independently of the unfolded protein response. J Cell Biol 187, 525-536.
33. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B, Liu K, Xu K, Strathearn KE, Liu F, Cao S, Caldwell KA, Caldwell GA, Marsischky G, Kolodner RD, Labaer J, Rochet JC, Bonini NM, Lindquist S (2006) Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313, 324-328. (Pubitemid 44480951)
34. Winslow AR, Chen CW, Corrochano S, Acevedo-Arozena A, Gordon DE, Peden AA, Lichtenberg M, Menzies FM, Ravikumar B, Imarisio S, Brown S, O'Kane CJ, Rubinsztein DC (2010) alpha-Synuclein impairs macroautophagy: Implications for Parkinson's disease. J Cell Biol 190, 1023-1037.
35. de Haan CA, Molinari M, Reggiori F (2010) Autophagy-independent LC3 function in vesicular traffic. Autophagy 6, 994-996.
36. Martinez O, Goud B (1998) Rab proteins. Biochim Biophys Acta 1404, 101-112. (Pubitemid 28375709)
37. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, Nixon RA (2008) Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28, 6926-6937.
38. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, Wolfe DM, Martinez-Vicente M, Massey AC, Sovak G, Uchiyama Y, Westaway D, Cuervo AM, Nixon RA (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158.
39. Scheper W, Zwart R, Baas F (2004) Rab6 membrane association is dependent of Presenilin 1 and cellular phosphorylation events. Brain Res Mol Brain Res 122, 17-23. (Pubitemid 38264543)