Golgi stress response and organelle zones.
CREB3
GOMED
GPI-anchor
Golgi
HSP47
TFE3
apoptosis
mucin
organelle zone
proteoglycan
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
09 2019
09 2019
Historique:
received:
01
07
2019
revised:
21
07
2019
accepted:
22
07
2019
pubmed:
26
7
2019
medline:
19
6
2020
entrez:
26
7
2019
Statut:
ppublish
Résumé
Organelles have been studied traditionally as single units, but a novel concept is now emerging: each organelle has distinct functional zones that regulate specific functions. The Golgi apparatus seems to have various zones, including zones for: glycosylphosphatidylinositol-anchored proteins; proteoglycan, mucin and lipid glycosylation; transport of cholesterol and ceramides; protein degradation (Golgi membrane-associated degradation); and signalling for apoptosis. The capacity for these specific functions and the size of the corresponding zones appear to be tightly regulated by the Golgi stress response to accommodate cellular demands. For instance, the proteoglycan and mucin zones seem to be separately augmented during the differentiation of chondrocytes and goblet cells, respectively. The mammalian Golgi stress response consists of several response pathways. The TFE3 pathway regulates the general function of the Golgi, such as structural maintenance, N-glycosylation and vesicular transport, whereas the proteoglycan pathway increases the expression of glycosylation enzymes for proteoglycans. The CREB3 and HSP47 pathways regulate pro- and anti-apoptotic functions, respectively. These observations indicate that the Golgi is a dynamic organelle, the capacity of which is upregulated according to cellular needs.
Identifiants
pubmed: 31344260
doi: 10.1002/1873-3468.13554
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2330-2340Subventions
Organisme : JSPS KAKENHI
ID : 19K06645
Pays : International
Organisme : JSPS KAKENHI
ID : 19K16131
Pays : International
Organisme : JSPS KAKENHI
ID : JP17H06414
Pays : International
Organisme : JSPS KAKENHI
ID : JP17J00067
Pays : International
Organisme : JSPS Bilateral Joint Research Projects
Pays : International
Informations de copyright
© 2019 Federation of European Biochemical Societies.
Références
Yano H, Yamamoto-Hino M, Abe M, Kuwahara R, Haraguchi S, Kusaka I, Awano W, Kinoshita-Toyoda A, Toyoda H and Goto S (2005) Distinct functional units of the Golgi complex in Drosophila cells. Proc Natl Acad Sci USA 102, 13467-13472.
Shimizu S (2019) Organelle zones in mitochondria. J Biochem 165, 101-107.
Nishitoh H (2019) Paradigm shift from 'Compartment' to 'Zone' in the understanding of organelles. J Biochem 165, 97-99.
Tamura Y, Kawano S and Endo T (2019) Organelle contact zones as sites for lipid transfer. J Biochem 165, 115-123.
Sasaki K and Yoshida H (2019) Organelle zones. Cell Struct Funct, https://doi.org/10.1247/csf.19010 [Epub ahead of print].
Yamamoto-Hino M, Katsumata E, Suzuki E, Maeda Y, Kinoshita T and Goto S (2018) Nuclear envelope localization of PIG-B is essential for GPI-anchor synthesis in Drosophila. J Cell Sci 131,https://doi.org/10.1242/jcs.218024.
Sasaki K and Yoshida H (2015) Organelle autoregulation-stress responses in the ER. Golgi, mitochondria and lysosome. J Biochem 157, 185-195.
Mori K (2015) The unfolded protein response: the dawn of a new field. Proc Jpn Acad Ser B Phys Biol Sci 91, 469-480.
Karagoz GE, Acosta-Alvear D and Walter P (2019) The unfolded protein response: detecting and responding to fluctuations in the protein-folding capacity of the endoplasmic reticulum. Cold Spring Harb Perspect Biol. https://doi.org/10.1101/cshperspect.a033886 [Epub ahead of print].
Volmer R and Ron D (2015) Lipid-dependent regulation of the unfolded protein response. Curr Opin Cell Biol. 33, 67-73.
Kimata Y and Kohno K (2011) Endoplasmic reticulum stress-sensing mechanisms in yeast and mammalian cells. Curr Opin Cell Biol 23, 135-142.
Yoshida H (2007) ER stress and diseases. FEBS J 274, 630-658.
Taniguchi M and Yoshida H (2017) TFE3, HSP47, and CREB3 pathways of the mammalian golgi stress response. Cell Struct Funct 42, 27-36.
Sasaki K, Komori R, Taniguchi M, Shimaoka A, Midori S, Yamamoto M, Okuda C, Tanaka R, Sakamoto M, Wakabayashi S et al. (2019) PGSE is a novel enhancer regulating the proteoglycan pathway of the mammalian Golgi stress response. Cell Struct Funct 44, 1-19.
Jamaludin MI, Wakabayashi S, Sasaki K, Kawamura H, Takase H, Sakamoto M and Yoshida H (2019) MGSE regulates crosstalk from the mucin pathway to the TFE3 pathway of the Golgi stress response. Cell Struct Funct. in press.
Eisenberg-Bord M, Shai N, Schuldiner M and Bohnert M (2016) A tether is a tether is a tether: tethering at membrane contact sites. Dev Cell 39, 395-409.
Toulmay A and Prinz WA (2012) A conserved membrane-binding domain targets proteins to organelle contact sites. J Cell Sci 125, 49-58.
Helle SC, Kanfer G, Kolar K, Lang A, Michel AH and Kornmann B (2013) Organization and function of membrane contact sites. Biochim Biophys Acta 1833, 2526-2541.
Lang A, John Peter AT and Kornmann B (2015) ER-mitochondria contact sites in yeast: beyond the myths of ERMES. Curr Opin Cell Biol 35, 7-12.
Lee S and Min KT (2018) The interface between er and mitochondria: molecular compositions and functions. Mol Cells 41, 1000-1007.
Elbaz-Alon Y, Rosenfeld-Gur E, Shinder V, Futerman AH, Geiger T and Schuldiner M (2014) A dynamic interface between vacuoles and mitochondria in yeast. Dev Cell 30, 95-102.
Malia PC and Ungermann C (2016) Vacuole membrane contact sites and domains: emerging hubs to coordinate organelle function with cellular metabolism. Biochem Soc Trans 44, 528-533.
Kozjak-Pavlovic V (2017) The MICOS complex of human mitochondria. Cell Tissue Res 367, 83-93.
Kurokawa K and Nakano A (2019) The ER exit sites are specialized ER zones for the transport of cargo proteins from the ER to the Golgi apparatus. J Biochem 165, 109-114.
Avezov E, Frenkel Z, Ehrlich M, Herscovics A and Lederkremer GZ (2008) Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol Biol Cell 19, 216-225.
Benyair R, Ogen-Shtern N, Mazkereth N, Shai B, Ehrlich M and Lederkremer GZ (2015) Mammalian ER mannosidase I resides in quality control vesicles, where it encounters its glycoprotein substrates. Mol Biol Cell 26, 172-184.
Nasu Y, Benke A, Arakawa S, Yoshida GJ, Kawamura G, Manley S, Shimizu S and Ozawa T (2016) In situ characterization of bak clusters responsible for cell death using single molecule localization microscopy. Sci Rep 6, 27505.
Berger EG and Roth J (1997) The Golgi Apparatus. Birkheuser Verlag, Basel, Switzerland.
Ishikawa HO, Takeuchi H, Haltiwanger RS and Irvine KD (2008) Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 321, 401-404.
Jacob R and Naim HY (2001) Apical membrane proteins are transported in distinct vesicular carriers. Curr Biol 11, 1444-1450.
Thompson A, Nessler R, Wisco D, Anderson E, Winckler B and Sheff D (2007) Recycling endosomes of polarized epithelial cells actively sort apical and basolateral cargos into separate subdomains. Mol Biol Cell 18, 2687-2697.
Olkkonen VM (2015) OSBP-related protein family in lipid transport over membrane contact sites. Lipid Insights 8, 1-9.
Yamaji T and Hanada K (2015) Sphingolipid metabolism and interorganellar transport: localization of sphingolipid enzymes and lipid transfer proteins. Traffic 16, 101-122.
Yamaguchi H, Arakawa S, Kanaseki T, Miyatsuka T, Fujitani Y, Watada H, Tsujimoto Y and Shimizu S (2016) Golgi membrane-associated degradation pathway in yeast and mammals. EMBO J 35, 1991-2007.
Arakawa S, Honda S, Yamaguchi H and Shimizu S (2017) Molecular mechanisms and physiological roles of Atg5/Atg7-independent alternative autophagy. Proc Jpn Acad Ser B Phys Biol Sci 93, 378-385.
Hampton RY and Sommer T (2012) Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 24, 460-466.
Yoshida H, Haze K, Yanagi H, Yura T and 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.
Haze K, Yoshida H, Yanagi H, Yura T and 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, 3787-3399.
Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS and Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6, 1355-1364.
Okada T, Yoshida H, Akazawa R, Negishi M and 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.
Mori K, Ma W, Gething MJ and Sambrook J (1993) A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74, 743-756.
Niwa M, Sidrauski C, Kaufman RJ and Walter P (1999) A role for presenilin-1 in nuclear accumulation of Ire1 fragments and induction of the mammalian unfolded protein response. Cell 99, 691-702.
Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M and Ron D (1998) Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 17, 5708-5717.
Iwawaki T, Hosoda A, Okuda T, Kamigori Y, Nomura-Furuwatari C, Kimata Y, Tsuru A and Kohno K (2001) Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat Cell Biol 3, 158-164.
Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP and Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287, 664-666.
Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG and Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96.
Yoshida H, Matsui T, Yamamoto A, Okada T and Mori K (2001) 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.
Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, Yoshida H, Morimoto R, Kurnit DM, Mori K et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107, 893-903.
Harding HP, Zhang Y, Bertolotti A, Zeng H and Ron D (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5, 897-904.
Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M and Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6, 1099-1108.
Oku M, Tanakura S, Uemura A, Sohda M, Misumi Y, Taniguchi M, Wakabayashi S and Yoshida H (2011) Novel cis-acting element GASE regulates transcriptional induction by the Golgi stress response. Cell Struct Funct 36, 1-12.
Taniguchi M, Nadanaka S, Tanakura S, Sawaguchi S, Midori S, Kawai Y, Yamaguchi S, Shimada Y, Nakamura Y, Matsumura Y et al. (2015) TFE3 Is a bHLH-ZIP-type transcription factor that regulates the mammalian Golgi stress response. Cell Struct Funct 40, 13-30.
Sohda M, Misumi Y, Yamamoto A, Yano A, Nakamura N and Ikehara Y (2001) Identification and characterization of a novel Golgi protein, GCP60, that interacts with the integral membrane protein giantin. J Biol Chem 276, 45298-45306.
Dinter A and Berger EG (1998) Golgi-disturbing agents. Histochem Cell Biol 109, 571-590.
Nadanaka S and Kitagawa H (2008) Heparan sulphate biosynthesis and disease. J Biochem 144, 7-14.
Reiling JH, Olive AJ, Sanyal S, Carette JE, Brummelkamp TR, Ploegh HL, Starnbach MN and Sabatini DM (2013) A CREB3-ARF4 signalling pathway mediates the response to Golgi stress and susceptibility to pathogens. Nat Cell Biol 15, 1473-1485.
Gendarme M, Baumann J, Ignashkova TI, Lindemann RK and Reiling JH (2017) Image-based drug screen identifies HDAC inhibitors as novel Golgi disruptors synergizing with JQ1. Mol Biol Cell 28, 3756-3772.
Ignashkova TI, Gendarme M, Peschk K, Eggenweiler HM, Lindemann RK and Reiling JH (2017) Cell survival and protein secretion associated with Golgi integrity in response to Golgi stress-inducing agents. Traffic 18, 530-544.
Alborzinia H, Ignashkova TI, Dejure FR, Gendarme M, Theobald J, Wolfl S, Lindemann RK and Reiling JH (2018) Golgi stress mediates redox imbalance and ferroptosis in human cells. Commun Biol 1, 210.
van Raam BJ, Lacina T, Lindemann RK and Reiling JH (2017) Secretory stressors induce intracellular death receptor accumulation to control apoptosis. Cell Death Dis 8, e3069.
Ramirez-Peinado S, Ignashkova TI, van Raam BJ, Baumann J, Sennott EL, Gendarme M, Lindemann RK, Starnbach MN and Reiling JH (2017) TRAPPC13 modulates autophagy and the response to Golgi stress. J Cell Sci 130, 2251-2265.
Baumann J, Ignashkova TI, Chirasani SR, Ramirez-Peinado S, Alborzinia H, Gendarme M, Kuhnigk K, Kramer V, Lindemann RK and Reiling JH (2018) Golgi stress-induced transcriptional changes mediated by MAPK signaling and three ETS transcription factors regulate MCL1 splicing. Mol Biol Cell 29, 42-52.
Miyata S, Mizuno T, Koyama Y, Katayama T and Tohyama M (2013) The endoplasmic reticulum-resident chaperone heat shock protein 47 protects the Golgi apparatus from the effects of O-glycosylation inhibition. PLoS ONE 8, e69732.