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Molecular and Cellular Biochemistry

, Volume 366, Issue 1–2, pp 175–182 | Cite as

Sar1 translocation onto the ER-membrane for vesicle budding has different pathways for promotion and suppression of ER-to-Golgi transport mediated through H89-sensitive kinase and ER-resident G protein

  • Hiroshi Nakagawa
  • Masakazu Ishizaki
  • Shuichi Miyazaki
  • Takuto Abe
  • Kazuhiko Nishimura
  • Masayuki Komori
  • Saburo Matsuo
Article

Abstract

ER-to-Golgi protein transport involves transport vesicles of which formation is initiated by assembly of Sar1. The assembly of Sar1 is suppressed by protein kinase inhibitor H89, suggesting that ER-to-Golgi transport is regulated progressively by H89 sensitive kinase. ER-resident Gi2 protein suppresses vesicle formation with inhibition of Sar1 assembly. This study examined whether these promotion and suppression of vesicle transport share the same signal pathway, by examining the effects of Gi/o protein activator mastoparan 7 (Mp-7) and H89 on Sar1 and Sec23 recruitment onto microsomes. In a cell-free system for Sar1 translocation assay, GTPγS addition induced the translocation of Sar1 onto microsomes. Mp-7 and H89 decreased the Sar1 translocation. Double treatment of Mp-7 and H89 strongly decreased Sar1 translocation. In single and double treatments, however, Gi/o protein inactivator pertussis toxin (IAP) partially restored the suppressive effect of Mp-7, but had not any effect on H89-induced effect. Then, the assembly of Sec23 onto the microsome was also increased by the addition of GTPγS. Sec23 translocation was decreased by Mp-7 and/or H89 treatment and recovered by IAP pretreatment except for H89 single treatment, similarly to Sar1 translocation in each treatment. Inhibitory effects of H89 and Mp-7on ER-to-Golgi vesicle transport by H89 or Mp-7 were also confirmed in a cell culture system by BFA-dispersion and BFA-reconstruction experiments. These findings indicate that promotion and suppression of ER-to-Golgi vesicle transport are modulated through separate signal pathways.

Keywords

ER-to-Golgi transport Sar1 Coat assembly H89 sensitive kinase ER-resident Gi protein 

References

  1. 1.
    Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S, Salama N, Rexach MF, Ravazzola M, Amherdt M, Schekman R (1994) COPII: a membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895–907PubMedCrossRefGoogle Scholar
  2. 2.
    Matsuoka K, Orci L, Amherdt M, Bednarek SY, Hamamoto S, Schekman R, Yeung T (1998) COPII-coated vesicle formation reconstituted with purified coat proteins and chemically defined liposomes. Cell 93:263–275PubMedCrossRefGoogle Scholar
  3. 3.
    Barlowe C, Schekman R (1993) SEC12 encodes a guanine-nucleotide-exchange factor essential for transport vesicle budding from the ER. Nature 365:347–349PubMedCrossRefGoogle Scholar
  4. 4.
    Bi X, Corpina RA, Goldberg J (2002) Structure of the Sec23/24–Sar1 pre-budding complex of the COPII vesicle coat. Nature 419:271–277PubMedCrossRefGoogle Scholar
  5. 5.
    Huang M, Weissman JT, Beraud-Dufour S, Luan P, Wang C, Chen W, Aridor M, Wilson IA, Balch WE (2001) Crystal structure of Sar1-GDP at 1.7 A resolution and the role of the NH2 terminus in ER export. J Cell Biol 155:937–948PubMedCrossRefGoogle Scholar
  6. 6.
    Balch WE, McCaffery JM, Plutner H, Farquhar MG (1994) Vesicular stomatitis virus glycoprotein is sorted and concentrated during export from the endoplasmic reticulum. Cell 76:841–852PubMedCrossRefGoogle Scholar
  7. 7.
    Springer S, Schekman R (1998) Nucleation of COPII vesicular coat complex by endoplasmic reticulum to Golgi vesicle SNAREs. Science 281:698–700PubMedCrossRefGoogle Scholar
  8. 8.
    Yoshihisa T, Barlowe C, Schekman R (1993) Requirement for a GTPase-activating protein in vesicle budding from the endoplasmic reticulum. Science 259:1466–1468PubMedCrossRefGoogle Scholar
  9. 9.
    Davidson HW, McGowan CH, Balch WE (1992) Evidence for the regulation of exocytic transport by protein phosphorylation. J Cell Biol 116:1343–1355PubMedCrossRefGoogle Scholar
  10. 10.
    Davidson HW, Balch WE (1993) Differential inhibition of multiple vesicular transport steps between the endoplasmic reticulum and trans Golgi network. J Biol Chem 268:4216–4226PubMedGoogle Scholar
  11. 11.
    Aridor M, Balch WE (2000) Kinase signaling initiates coat complex II (COP II) recruitment and export from the mammalian endoplasmic reticulum. J Biol Chem 275:35673–35676PubMedCrossRefGoogle Scholar
  12. 12.
    Nakagawa H, Miyazaki S, Abe T, Umadome H, Tanaka K, Nishimura K, Komori M, Matsuo S (2011) H89 sensitive kinase regulates the translocation of Sar1 onto the ER membrane through phosphorylation of ER-coupled β-tubulin. Int J Biochem Cell Biol 43:423–430PubMedCrossRefGoogle Scholar
  13. 13.
    Balch WE (1992) From G minor to G major. Curr Biol 2:157–160PubMedCrossRefGoogle Scholar
  14. 14.
    Barr FA, Leyte A, Huttner WB (1992) Trimeric G proteins and vesicle formation. Trends Cell Biol 2:91–94PubMedCrossRefGoogle Scholar
  15. 15.
    Stow JL, de Almeida JB, Narula N, Holtzman EJ, Ercolani L, Ausiello DA (1991) A heterotrimeric G protein, G alpha i-3, on Golgi membranes regulates the secretion of a heparan sulfate proteoglycan in LLC-PK1 epithelial cells. J Cell Biol 114:1113–1124PubMedCrossRefGoogle Scholar
  16. 16.
    Beckers CJ, Balch WE (1989) Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J Cell Biol 108:1245–1256PubMedCrossRefGoogle Scholar
  17. 17.
    Robinson MS, Kreis TE (1992) Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69:129–138PubMedCrossRefGoogle Scholar
  18. 18.
    Matsuo S, Kiyomiya K, Kurebe M (1998) Mechanism of toxic action of fluoride in dental fluorosis: whether trimeric G proteins participate in the disturbance of intracellular transport of secretory ameloblast exposed to fluoride. Arch Toxicol 72:798–806PubMedCrossRefGoogle Scholar
  19. 19.
    Matsuo S, Nakagawa H, Kiyomiya K, Kurebe M (2000) Fluoride-induced ultrastructural changes in exocrine pancreas cells of rats: fluoride disrupts the export of zymogens from the rough endoplasmic reticulum (rER). Arch Toxicol 73:611–617PubMedCrossRefGoogle Scholar
  20. 20.
    Ito M, Nakagawa H, Okada T, Miyazaki S, Matssuo S (2009) ER-stress caused by accumulated intracisternal granules activates autophagy through a different signal pathway from unfolded protein response in expcrine pancreas cells of rats exposed to fluoride. Arch Toxicol 83:151–159PubMedCrossRefGoogle Scholar
  21. 21.
    Nakagawa H, Umadome H, Miyazaki S, Tanaka K, Nishimura K, Komori M, Matsuo S (2011) ER-resodent Gi2 protein controls Sar1 translocation onto the ER during budding of transport vesicles. J Cell Biochem 112:2250–2256PubMedCrossRefGoogle Scholar
  22. 22.
    Rowe T, Aridor M, McCaffery JM, Plutner H, Nuoffer C, Balch WE (1996) COPII vesicles derived from mammalian endoplasmic reticulum microsomes recruit COPI. J Cell Biol 135:895–911PubMedCrossRefGoogle Scholar
  23. 23.
    Aridor M, Bannykh SI, Rowe T, Balch WE (1995) Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J Cell Biol 131:875–893PubMedCrossRefGoogle Scholar
  24. 24.
    Sonoda H, Okada T, Jahangeer S, Nakamura S (2007) Requirement of phospholipase D for ilimaquinone-induced Golgi membrane fragmentation. J Biol Chem 282:34085–34092PubMedCrossRefGoogle Scholar
  25. 25.
    Du X, Kristiana I, Wong J, Brown AJ (2006) Involvement of Akt in ER-to-Golgi transport of SCAP/SREBP: a link between a key cell proliferative pathway and membrane synthesis. Mol Biol Cell 17:2735–2745PubMedCrossRefGoogle Scholar
  26. 26.
    Nagaya H, Wada I, Jia Y, Kanoh H (2002) Diacylglycerol kinase delta suppresses ER-to-Golgi traffic via its SAM and PH domains. Mol Biol Cell 13:302–316PubMedCrossRefGoogle Scholar
  27. 27.
    Palmer KJ, Konkel JE, Stephens DJ (2005) PCTAIRE protein kinases interact directly with the COPII complex and modulate secretory cargo transport. J Cell Sci 118:3839–3847PubMedCrossRefGoogle Scholar
  28. 28.
    Bigay J, Deterre P, Pfister C, Chabre M (1987) Fluoride complexes of aluminum or beryllium act on G-proteins as reversibly bound analogues of the gamma phosphate of GTP. EMBO J 6:2907–2913PubMedGoogle Scholar
  29. 29.
    Sternweis PC, Gilman AG (1982) Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride. Proc Natl Acad Sci USA 79:4888–4891PubMedCrossRefGoogle Scholar
  30. 30.
    Mittal R, Ahmdian MR, Goody RS, Wittinghofer A (1996) Formation of a transition-state analog of the Ras GTPase reaction by Ras-GDP, tetrafluoroaluminate, and GTPase-activating proteins. Science 273:115–117PubMedCrossRefGoogle Scholar
  31. 31.
    Weidman PJ, Winter WM (1994) The G protein-activating peptide, mastoparan, and the synthetic NH2-terminal ARF peptide, ARFp13, inhibit in vitro Golgi transport by irreversibly damaging membranes. J Cell Biol 27:1815–1827CrossRefGoogle Scholar
  32. 32.
    Amin RH, Chen HQ, Veluthakal R, Silver RB, Li J, Li G, Kowluru A (2003) Mastoparan-induced insulin secretion from insulin-secreting betaTC3 and INS-1 cells: evidence for its regulation by Rho subfamily of G proteins. Endocrinology 144:4508–4518PubMedCrossRefGoogle Scholar
  33. 33.
    Fourest-Lieuvin A, Peris L, Gache V, Garcia-Saez I, Juillan-Binard C, Lantez V, Job D (2006) Microtubule regulation in mitosis: tubulin phosphorylation by the cyclin-dependent kinase Cdk1. Mol Biol Cell 17:1041–1050PubMedCrossRefGoogle Scholar
  34. 34.
    Limas CJ, Limas C (1983) Involvement of microtubules in the isoproterenol-induced ‘down’-regulation of myocardial beta-adrenergic receptors. Biochim Biophys Acta 735:181–184PubMedCrossRefGoogle Scholar
  35. 35.
    Kohtz DS, Puszkin S (1989) Phosphorylation of tubulin by casein kinase II regulates its binding to a neuronal protein (NP 185) associated with brain coated vesicles. J Neurochem 52:285–295PubMedCrossRefGoogle Scholar
  36. 36.
    Donaldson JG, Klausner RD (1994) ARF; a key regulatory switch in membrane traffic and organelle structure. Curr Opin Cell Biol 6:527–532PubMedCrossRefGoogle Scholar
  37. 37.
    Puri S, Linstedt AD (2003) Capacity of the Golgi apparatus for Biogenesis from the endoplasmic reticulum. Mol Biol Cell 14:5011–5018PubMedCrossRefGoogle Scholar
  38. 38.
    Siddhanta A, Backer JM, Shiekds D (2000) Inhibition of phosphatidic acid synthesis alters the structure of the Golgi apparatus and inhibits secretion in endocrine cells. J Biol Chem 275:12023–12031PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2012

Authors and Affiliations

  • Hiroshi Nakagawa
    • 1
  • Masakazu Ishizaki
    • 1
  • Shuichi Miyazaki
    • 2
  • Takuto Abe
    • 1
  • Kazuhiko Nishimura
    • 1
  • Masayuki Komori
    • 3
  • Saburo Matsuo
    • 1
  1. 1.Laboratory of Toxicology, Course of Veterinary Science, Graduate School of Life and Environmental BiosciencesOsaka Prefecture UniversityIzumisanoJapan
  2. 2.The Center for Advanced Research, Graduate School of Medical SciencesToho University of MedicineTokyoJapan
  3. 3.Laboratory of Cellular and Molecular Biology, Course of Veterinary Science, Graduate School of Life and Environmental BiosciencesOsaka Prefecture UniversityIzumisanoJapan

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