A Creb3–arf4 Signalling Pathway Mediates the Response to Golgi Stress and Susceptibility to Pathogens

Nature Cell Biology

Volumn 15, Issue 12, 2013, Pages 1473-1485

  Reiling, Jan H ^a,b,c,e   Olive, Andrew J ^d   Sanyal, Sumana ^a,b   Carette, Jan E ^a,f   Brummelkamp, Thijn R ^a,g   Ploegh, Hidde L ^a,b   Starnbach, Michael N ^d   Sabatini, David M ^a,b,c  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c KOCH INSTITUTE FOR INTEGRATIVE CANCER RESEARCH   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e BioMed X Innovation Center   (Germany)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ARF4 PROTEIN, HUMAN; BREFELDIN A; CREB3 PROTEIN, HUMAN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GBF1 PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; SMALL INTERFERING RNA;

ARTICLE; CHLAMYDIA TRACHOMATIS; DISEASE PREDISPOSITION; DRUG EFFECT; GENE SILENCING; GENETICS; GOLGI COMPLEX; HELA CELL; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN TRANSPORT; SHIGELLA FLEXNERI; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; UPREGULATION; DRUG EFFECTS; HELA CELL LINE;

ADP-RIBOSYLATION FACTOR 1; ADP-RIBOSYLATION FACTORS; BREFELDIN A; CHLAMYDIA TRACHOMATIS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DISEASE SUSCEPTIBILITY; GENE KNOCKDOWN TECHNIQUES; GOLGI APPARATUS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN TRANSPORT; RNA, SMALL INTERFERING; SHIGELLA FLEXNERI; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTIONAL ACTIVATION; UP-REGULATION;

EID: 84893349228     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2865     Document Type: Article

References (70)

1. Chiu, V. K. et al. Ras signalling on the endoplasmic reticulum and the Golgi. Nat. Cell Biol. 4, 343–350 (2002).
2. Altan-Bonnet, N., Phair, R. D., Polishchuk, R. S., Weigert, R. & Lippincott-Schwartz, J. A role for Arf1 in mitotic Golgi disassembly, chromosome segregation, and cytokinesis. Proc. Natl Acad. Sci. USA 100, 13314–13319 (2003).
3. Sutterlin, C., Hsu, P., Mallabiabarrena, A. & Malhotra, V. Fragmentation and dispersal of the pericentriolar Golgi complex is required for entry into mitosis in mammalian cells. Cell 109, 359–369 (2002).
4. Yadav, S., Puri, S. & Linstedt, A. D. A primary role for Golgi positioning in directed secretion, cell polarity, and wound healing. Mol. Biol. Cell 20, 1728–1736 (2009).
5. Kupfer, A., Louvard, D. & Singer, S. J. Polarization of the Golgi apparatus and the microtubule-organizing center in cultured fibroblasts at the edge of an experimental wound. Proc. Natl Acad. Sci. USA 79, 2603–2607 (1982).
6. Singleton, V. L., Bohonos, N. & Ullstrup, A. J. Decumbin, a new compound from a species of Penicillium. Nature 181, 1072–1073 (1958).
7. Shao, R. G., Shimizu, T. & Pommier, Y. Brefeldin A is a potent inducer of apoptosis in human cancer cells independently of p 53. Exp. Cell Res. 227, 190–196 (1996).
8. Nojiri, H., Manya, H., Isono, H., Yamana, H. & Nojima, S. Induction of terminal differentiation and apoptosis in human colonic carcinoma cells by brefeldin A, a drug affecting ganglioside biosynthesis. FEBS Lett. 453, 140–144 (1999).
9. Sausville, E. A. et al. Antiproliferative effect in vitro and antitumor activity in vivo of brefeldin A. The Cancer J. Sci. Am. 2, 52–58 (1996).
10. Anadu, N. O., Davisson, V. J. & Cushman, M. Synthesis and anticancer activity of brefeldin A ester derivatives. J. Med. Chem. 49, 3897–3905 (2006).
11. Donaldson, J. G. & Jackson, C. L. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12, 362–375 (2011).
12. D’Souza-Schorey, C. & Chavrier, P. ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347–358 (2006).
13. Peyroche, A. et al. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain. Mol. Cell 3, 275–285 (1999).
14. D’Souza-Schorey, C., Li, G., Colombo, M. I. & Stahl, P. D. A regulatory role for ARF6 in receptor-mediated endocytosis. Science 267, 1175–1178 (1995).
15. Peters, P. J. et al. Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J. Cell Biol. 128, 1003–1017 (1995).
16. Cavenagh, M. M. et al. Intracellular distribution of Arf proteins in mammalian cells. Arf6 is uniquely localized to the plasma membrane. J. Biol. Chem. 271, 21767–21774 (1996).
17. Reiling, J. H. et al. A haploid genetic screen identifies the major facilitator domain containing 2A (MFSD2A) transporter as a key mediator in the response to tunicamycin. Proc. Natl Acad. Sci. USA 108, 11756–11765 (2011).
18. Carette, J. E. et al. Haploid genetic screens in human cells identify host factors used by pathogens. Science 326, 1231–1235 (2009).
19. Carette, J. E. et al. Global gene disruption in human cells to assign genes to phenotypes by deep sequencing. Nature Biotechnol. 29, 542–546 (2011).
20. Volpicelli-Daley, L. A., Li, Y., Zhang, C. J. & Kahn, R. A. Isoform-selective effects of the depletion of ADP-ribosylation factors 1-5 on membrane traffic. Mol. Biol. Cell 16, 4495–4508 (2005).
21. Nakai, W. et al. ARF1 and ARF4 regulate recycling endosomal morphology and retrograde transport from endosomes to the Golgi apparatus. Mol. Biol. Cell 24, 2570–2581 (2013).
22. Kondo, Y. et al. ARF1 and ARF3 are required for the integrity of recycling endosomes and the recycling pathway. Cell Struct. Funct. 37, 141–154 (2012).
23. Claude, A. et al. GBF1: a novel Golgi-associated BFA-resistant guanine nucleotide exchange factor that displays specificity for ADP-ribosylation factor 5. J. Cell Biol. 146, 71–84 (1999).
24. Ooi, C. E., Dell’Angelica, E. C. & Bonifacino, J. S. ADP-Ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes. J. Cell Biol. 142, 391–402 (1998).
25. Shinotsuka, C., Yoshida, Y., Kawamoto, K., Takatsu, H. & Nakayama, K. Overexpression of an ADP-ribosylation factor-guanine nucleotide exchange factor, BIG2, uncouples brefeldin A-induced adaptor protein-1 coat dissociation and membrane tubulation. J. Biol. Chem. 277, 9468–9473 (2002).
26. Alvarez, C., Garcia-Mata, R., Brandon, E. & Sztul, E. COPI recruitment is modulated by a Rab1b-dependent mechanism. Mol. Biol. Cell 14, 2116–2127 (2003).
27. Teal, S. B., Hsu, V. W., Peters, P. J., Klausner, R. D. & Donaldson, J. G. An activating mutation in ARF1 stabilizes coatomer binding to Golgi membranes. J. Biol. Chem. 269, 3135–3138 (1994).
28. Santy, L. C. & Casanova, J. E. Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599–610 (2001).
29. Manolea, F. et al. Arf3 is activated uniquely at the trans-Golgi network by brefeldin A-inhibited guanine nucleotide exchange factors. Mol. Biol. Cell 21, 1836–1849 (2010).
30. Bui, Q. T., Golinelli-Cohen, M. P. & Jackson, C. L. Large Arf1 guanine nucleotide exchange factors: evolution, domain structure, and roles in membrane trafficking and human disease. Mol. Genet. Genom. 282, 329–350 (2009).
31. Nakagomi, S. et al. A Golgi fragmentation pathway in neurodegeneration. Neurobiol. Dis. 29, 221–231 (2008).
32. Lee, T. H. & Linstedt, A. D. Potential role for protein kinases in regulation of bidirectional endoplasmic reticulum-to-Golgi transport revealed by protein kinase inhibitor H89. Mol. Biol. Cell 11, 2577–2590 (2000).
33. Nickel, W., Helms, J. B., Kneusel, R. E. & Wieland, F. T. Forskolin stimulates detoxification of brefeldin A. J. Biol. Chem. 271, 15870–15873 (1996).
34. Jang, S. Y., Jang, S. W. & Ko, J. Regulation of ADP-ribosylation factor 4 expression by small leucine zipper protein and involvement in breast cancer cell migration. Cancer Lett. 314, 185–197 (2012).
35. Asada, R., Kanemoto, S., Kondo, S., Saito, A. & Imaizumi, K. The signalling from endoplasmic reticulum-resident bZIP transcription factors involved in diverse cellular physiology. J. Biochem. 149, 507–518 (2011).
36. Kondo, S. et al. Activation of OASIS family, ER stress transducers, is dependent on its stabilization. Cell Death Differ. 19, 1939–1949 (2012).
37. Denboer, L. M. et al. JAB1/CSN5 inhibits the activity of Luman/CREB3 by promoting its degradation. Biochim. Biophys. Acta 1829, 921–929 (2013).
38. Heuer, D. et al. Chlamydia causes fragmentation of the Golgi compartment to ensure reproduction. Nature 457, 731–735 (2009).
39. Burnaevskiy, N. et al. Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor IpaJ. Nature 496, 106–109 (2013).
40. Hackstadt, T., Scidmore, M. A. & Rockey, D. D. Lipid metabolism in Chlamydia trachomatis-infected cells: directed trafficking of Golgi-derived sphingolipids to the chlamydial inclusion. Proc. Natl Acad. Sci. USA 92, 4877–4881 (1995).
41. Elwell, C. A. et al. Chlamydia trachomatis co-opts GBF1 and CERT to acquire host sphingomyelin for distinct roles during intracellular development. PLoS Pathog. 7, e1002198 (2011).
42. Gurumurthy, R. K. et al. A loss-of-function screen reveals Ras-and Raf-independent MEK-ERK signaling during Chlamydia trachomatis infection. Sci. Signal. 3, ra21 (2010).
43. Dong, N. et al. Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150, 1029–1041 (2012).
44. Brunham, R. C. & Rey-Ladino, J. Immunology of Chlamydia infection: implications for a Chlamydia trachomatis vaccine. Nat. Rev. Immunol. 5, 149–161 (2005).
45. Kotloff, K. L. et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull. World Health Organ. 77, 651–666 (1999).
46. Raggo, C. et al. Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol. Cell Biol. 22, 5639–5649 (2002).
47. DenBoer, L. M. et al. Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem. Biophys. Res. Commun. 331, 113–119 (2005).
48. Liang, G. et al. Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein Herp through an ER stress response element. Mol. Cell Biol. 26, 7999–8010 (2006).
49. Chen, X., Shen, J. & Prywes, R. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277, 13045–13052 (2002).
50. Nadanaka, S., Okada, T., Yoshida, H. & Mori, K. Role of disulfide bridges formed in the luminal domain of ATF6 in sensing endoplasmic reticulum stress. Mol. Cell Biol. 27, 1027–1043 (2007).
51. Zhang, K. et al. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic infiammatory response. Cell 124, 587–599 (2006).
52. Citterio, C. et al. Unfolded protein response and cell death after depletion of brefeldin A-inhibited guanine nucleotide-exchange protein GBF1. Proc. Natl Acad. Sci. USA 105, 2877–2882 (2008).
53. Saenz, J. B. et al. Golgicide A reveals essential roles for GBF1 in Golgi assembly and function. Nat. Chem. Biol. 5, 157–165 (2009).
54. Chun, J., Shapovalova, Z., Dejgaard, S. Y., Presley, J. F. & Melancon, P. Characterization of class I and II ADP-ribosylation factors (Arfs) in live cells: GDP-bound class II Arfs associate with the ERfiGolgi intermediate compartment independently of GBF1. Mol. Biol. Cell 19, 3488–3500 (2008).
55. Feng, Y. et al. Exo1: a new chemical inhibitor of the exocytic pathway. Proc. Natl Acad. Sci. USA 100, 6469–6474 (2003).
56. Barzilay, E., Ben-Califa, N., Hirschberg, K. & Neumann, D. Uncoupling of brefeldin a-mediated coatomer protein complex-I dissociation from Golgi redistribution. Traffic 6, 794–802 (2005).
57. Dinter, A. & Berger, E. G. Golgi-disturbing agents. Histochem. Cell Biol. 109, 571–590 (1998).
58. Zhang, G. F., Driouich, A. & Staehelin, L. A. Effect of monensin on plant Golgi: re-examination of the monensin-induced changes in cisternal architecture and functional activities of the Golgi apparatus of sycamore suspension-cultured cells. J. Cell Sci. 104, 819–831 (1993).
59. Hicks, S. W. & Machamer, C. E. Golgi structure in stress sensing and apoptosis. Biochim. Biophys. Acta 1744, 406–414 (2005).
60. Oku, M. et al. Novel cis-acting element GASE regulates transcriptional induction by the Golgi stress response. Cell Struct. Funct. 36, 1–12 (2011).
61. Huynh, D. P., Yang, H.T., Vakharia, H., Nguyen, D. & Pulst, S.M. Expansion of the polyQ repeat in ataxin-2 alters its Golgi localization, disrupts the Golgi complex and causes cell death. Human Mol. Genet. 12, 1485–1496 (2003).
62. Winslow, A.R. et al. α-Synuclein impairs macroautophagy: implications for Parkinson’s disease. J. Cell Biol. 190, 1023–1037 (2010).
63. Cooper, A. A. et al. α-synuclein blocks ERfiGolgi traffic and Rab1 rescues neuron loss in Parkinson’s models. Science 313, 324–328 (2006).
64. Walkley, S.U. & Suzuki, K. Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim. Biophys. Acta 1685, 48–62 (2004).
65. Gonatas, N. K., Stieber, A. & Gonatas, J. O. Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J. Neurol. Sci. 246, 21–30 (2006).
66. Jehl, S. P., Nogueira, C. V., Zhang, X. & Starnbach, M. N. IFNgamma inhibits the cytosolic replication of Shigella flexneri via the cytoplasmic RNA sensor RIG-I. PLoS Pathog. 8, e1002809 (2012).
67. Gondek, D. C., Olive, A. J., Stary, G. & Starnbach, M. N. CD4C T cells are necessary and sufficient to confer protection against Chlamydia trachomatis infection in the murine upper genital tract. J. Immunol. 189, 2441–2449 (2012).
68. van der Velden, A. W., Dougherty, J. T. & Starnbach, M. N. Down-modulation of TCR expression by Salmonella enterica serovar Typhimurium. J. Immunol. 180, 5569–5574 (2008).
69. Coers, J. et al. Compensatory T cell responses in IRG-deficient mice prevent sustained Chlamydia trachomatis infections. PLoS Pathog. 7, e1001346 (2011).
70. Cohen, L. A. & Donaldson, J. G. Curr. Protoc. Cell Biol. 48, 11–17 (2010).