Endosomal Rab GTPases regulate secretory granule maturation in Drosophila larval salivary glands

References

• Biyasheva A, Do T-V, Lu Y, et al. Glue secretion in the Drosophila salivary gland: a model for steroid-regulated exocytosis. Dev Biol. 2001;231:234–251.
   PubMed Web of Science ®Google Scholar
• Burgess J, Jauregui M, Tan J, et al. AP-1 and clathrin are essential for secretory granule biogenesis in Drosophila. Mol Biol Cell. 2011;22:2094–2105.
   PubMed Web of Science ®Google Scholar
• Burgess J, Del Bel LM, Ma C-IJ, et al. Type II phosphatidylinositol 4-kinase regulates trafficking of secretory granule proteins in Drosophila. Development. 2012;139:3040–3050.
   PubMed Web of Science ®Google Scholar
• Torres IL, Rosa-Ferreira C, Munro S. The Arf family G protein Arl1 is required for secretory granule biogenesis in Drosophila. J Cell Sci. 2014;127:2151–2160.
   PubMed Web of Science ®Google Scholar
• Ashburner, M. (1990). Drosophila: A Laboratory Handbook. Cold Spring Harbor, NY: Cold Spring Harbor Press.
   Google Scholar
• Costantino BF, Bricker DK, Alexandre K, et al. (2008). A novel ecdysone receptor mediates steroid-regulated developmental events during the mid-third instar of Drosophila. PLoS Genet 4, e1000102.
   Google Scholar
• Ma C-IJ, Yang Y, Kim T, et al. An early endosome-derived retrograde trafficking pathway promotes secretory granule maturation. J Cell Biol. 2020;219. DOI:https://doi.org/10.1083/jcb.201808017
   Google Scholar
• Marks MS, Heijnen HF, Raposo G. Lysosome-related organelles: unusual compartments become mainstream. Curr Opin Cell Biol. 2013;25:495–505.
   PubMed Web of Science ®Google Scholar
• Dunst S, Kazimiers T, von Zadow F, et al. Endogenously tagged Rab proteins: a resource to study membrane trafficking in Drosophila. Dev Cell. 2015;33:351–365.
   PubMed Web of Science ®Google Scholar
• Barr FA. Rab GTPases and membrane identity: causal or inconsequential. J Cell Biol. 2013;202:191–199.
   PubMed Web of Science ®Google Scholar
• Bustos MA, Lucchesi O, Ruete MC, et al. Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis. Proc Natl Acad Sci USA. 2012;109:E2057–E2066.
   PubMed Web of Science ®Google Scholar
• Cazares VA, Subramani A, Saldate JJ, et al. Distinct actions of rab3 and rab27 GTPases on late stages of exocytosis of insulin. Traffic. 2014;15:997–1015.
   PubMed Web of Science ®Google Scholar
• Handley MTW, Haynes LP, Burgoyne RD. Differential dynamics of Rab3A and Rab27A on secretory granules. J Cell Sci. 2007;120:973–984.
   PubMed Web of Science ®Google Scholar
• Kögel T, Rudolf R, Hodneland E, et al. Rab3D is critical for secretory granule maturation in PC12 Cells. PLoS One. 2013;8:e57321.
   PubMed Web of Science ®Google Scholar
• Schonn J-S, Van Weering JRT, Mohrmann R, et al. Rab3 proteins involved in vesicle biogenesis and priming in embryonic mouse chromaffin cells. Traffic. 2010;11:1415–1428.
   PubMed Web of Science ®Google Scholar
• Wang H, Ishizaki R, Xu J, et al. The Rab27a effector exophilin7 promotes fusion of secretory granules that have not been docked to the plasma membrane. Mol Biol Cell. 2013;24:319–330.
   PubMed Web of Science ®Google Scholar
• Yi Z, Yokota H, Torii S, et al. The Rab27a/Granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol. 2002;22:1858–1867.
   PubMed Web of Science ®Google Scholar
• Cho SH, Kuo IY, Lu PJF, et al. Rab37 mediates exocytosis of secreted frizzled-related protein 1 to inhibit Wnt signaling and thus suppress lung cancer stemness. Cell Death Dis. 2018;9:1–13.
   PubMed Web of Science ®Google Scholar
• Johnson JL, He J, Ramadass M, et al. Munc13-4 Is a Rab11-binding protein that regulates Rab11-positive vesicle trafficking and docking at the plasma membrane. J Biol Chem. 2016;291:3423–3438.
   PubMed Web of Science ®Google Scholar
• Ljubicic S, Bezzi P, Brajkovic S, et al. The GTPase Rab37 participates in the control of insulin exocytosis. PLoS One. 2013;8:e68255.
   PubMed Web of Science ®Google Scholar
• Masuda ES, Luo Y, Young C, et al. Rab37 is a novel mast cell specific GTPase localized to secretory granules. FEBS Lett. 2000;470:61–64.
   PubMed Web of Science ®Google Scholar
• Sugawara K, Shibasaki T, Mizoguchi A, et al. Rab11 and its effector Rip11 participate in regulation of insulin granule exocytosis. Genes Cells. 2009;14:445–456.
   PubMed Web of Science ®Google Scholar
• Venugopal K, Chehade S, Werkmeister E, et al. Rab11A regulates dense granule transport and secretion during Toxoplasma gondii invasion of host cells and parasite replication. PLOS Pathog. 2020;16:e1008106.
   PubMed Web of Science ®Google Scholar
• Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 2011;91:119–149.
   PubMed Web of Science ®Google Scholar
• Nassari S, Del OT, Jean S. Rabs in signaling and embryonic development. Int J Mol Sci. 2020;21:1064.
   PubMed Web of Science ®Google Scholar
• Ao X, Zou L, Wu Y. Regulation of autophagy by the Rab GTPase network. Cell Death Differ. 2014;21:348–358.
   PubMed Web of Science ®Google Scholar
• Bento CF, Puri C, Moreau K, et al. The role of membrane-trafficking small GTPases in the regulation of autophagy. J Cell Sci. 2013;126:1059–1069.
   PubMed Web of Science ®Google Scholar
• Puri C, Vicinanza M, Ashkenazi A, et al. The RAB11A-positive compartment is a primary platform for autophagosome assembly mediated by WIPI2 recognition of PI3P-RAB11A. Dev Cell. 2018;45:114–131.e8.
   PubMed Web of Science ®Google Scholar
• Saito T, Nah J, Oka S, et al. An alternative mitophagy pathway mediated by Rab9 protects the heart against ischemia. J Clin Invest. 2019;129:802–819.
   PubMed Web of Science ®Google Scholar
• Zhou F, Wu Z, Zhao M, et al. Rab5-dependent autophagosome closure by ESCRT. J Cell Biol. 2019;218:1908–1927.
   PubMed Web of Science ®Google Scholar
• Azouz NP, Zur N, Efergan A, et al. Rab5 is a novel regulator of mast cell secretory granules: impact on size, cargo, and exocytosis. J Immunol. 2014;192:4043–4053.
   PubMed Web of Science ®Google Scholar
• Klein O, Roded A, Zur N, et al. Rab5 is critical for SNAP23 regulated granule-granule fusion during compound exocytosis. Sci Rep. 2017;7:15315.
   PubMed Web of Science ®Google Scholar
• Leader DP, Krause SA, Pandit A, et al. FlyAtlas 2: A new version of the Drosophila melanogaster expression atlas with RNA-Seq, miRNA-Seq and sex-specific data. Nucleic Acids Res. 2018;46:D809–D815.
   PubMed Web of Science ®Google Scholar
• Roy S, Ernst J, Kharchenko PV, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science (80-.). 2010;330:1787–1797.
   PubMed Web of Science ®Google Scholar
• Ng EL, Gan BQ, Ng F, et al. Rab GTPases regulating receptor trafficking at the late endosome-lysosome membranes. Cell Biochem Funct. 2012;30:515–523.
   PubMed Web of Science ®Google Scholar
• Fujii S, Kurokawa K, Inaba R, et al. Recycling endosomes attach to the trans-side of Golgi stacks in Drosophila and mammalian cells. J Cell Sci. 2020;133:jcs236935.
   Web of Science ®Google Scholar
• Wilcke M, Johannes L, Galli T, et al. Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-Golgi network. J Cell Biol. 2000;151:1207–1220.
   PubMed Web of Science ®Google Scholar
• Liu S, Storrie B. Are Rab proteins the link between Golgi organization and membrane trafficking? Cell Mol Life Sci. 2012;69:4093–4106.
   PubMed Web of Science ®Google Scholar
• Sandoval CO, Simmen T. Rab proteins of the endoplasmic reticulum: functions and interactors. Biochem Soc Trans. 2012;40:1426–1432.
   PubMed Web of Science ®Google Scholar
• Short B, Haas A, Barr FA. Golgins and GTPases, giving identity and structure to the Golgi apparatus. Biochim Biophys Acta. 2005;1744:383–395.
   PubMed Web of Science ®Google Scholar
• Ke H, Feng Z, Liu M, et al. Collagen secretion screening in Drosophila supports a common secretory machinery and multiple Rab requirements. J Genet Genomics. 2018;45(6):299–313.
   Web of Science ®Google Scholar
• Sechi S, Frappaolo A, Fraschini R, et al. Rab1 interacts with GOLPH3 and controls Golgi structure and contractile ring constriction during cytokinesis in Drosophila melanogaster. Open Biol. 2017;7:160257.
   PubMed Web of Science ®Google Scholar
• Chen X, Walker AK, Strahler JR, et al. Organellar proteomics: analysis of pancreatic zymogen granule membranes. Mol Cell Proteomics. 2006;5:306–312.
   PubMed Web of Science ®Google Scholar
• Iida H, Tanaka S, Shibata Y. Small GTP-binding protein, Rab6, is associated with secretory granules in atrial myocytes. Am J Physiol. 1997;272:C1594–601.
   PubMedGoogle Scholar
• Stedman TT, Sussmann AR, Joiner KA. Toxoplasma gondii Rab6 mediates a retrograde pathway for sorting of constitutively secreted proteins to the golgi complex. J Biol Chem. 2003;278(7):5433–5443.
   PubMed Web of Science ®Google Scholar