Role of the inositol polyphosphate kinase Vip1 in autophagy and pathogenesis in Candida albicans

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References

• 1. Boer VM, Crutchfield CA, Bradley PH et al. Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol. Biol. Cell 21(1), 198–211 (2010).
  Medline CASGoogle Scholar
• 2. Wundenberg T, Mayr GW. Synthesis and biological actions of diphosphoinositol phosphates (inositol pyrophosphates), regulators of cell homeostasis. Biol. Chem. 393(9), 979–998 (2012).
  Medline CASGoogle Scholar
• 3. Passarino G, Rose G, Bellizzi D. Mitochondrial function, mitochondrial DNA and ageing: a reappraisal. Biogerontology 11(5), 575–588 (2010).
  Medline CASGoogle Scholar
• 4. Saiardi A, Resnick AC, Snowman AM et al. Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. Proc. Natl Acad. Sci. USA 102(6), 1911–1914 (2005).
  Medline CASGoogle Scholar
• 5. York SJ, Armbruster BN, Greenwell P et al. Inositol diphosphate signaling regulates telomere length. J. Biol. Chem. 280(6), 4264–4269 (2005).
  Medline CASGoogle Scholar
• 6. Bakkenist CJ, Kastan MB. Initiating cellular stress responses. Cell 118(1), 9–17 (2004).
  Medline CASGoogle Scholar
• 7. Onnebo SM, Saiardi A. Inositol pyrophosphates modulate hydrogen peroxide signalling. Biochem. J. 423(1), 109–118 (2009).
  Medline CASGoogle Scholar
• 8. Jennifer P, Carmen R, Constanze S et al. The Vip1 inositol polyphosphate kinase family regulates polarized growth and modulates the microtubule cytoskeleton in fungi. PLoS. Genet. 10(9), 4586–4624 (2014). •• Uncovers that the modulation of microtubule dynamics was correlated to Vip1 kinase activity and inositol pyrophosphates were conserved in fungi biological processes.
  Google Scholar
• 9. Streb H, Irvine RF, Berridge MJ, Schulz I. Release of Ca2⁺ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306, 67–69 (1983).
  Medline CASGoogle Scholar
• 10. Putney JW Jr. The role of phosphoinositide metabolism in signal transduction in secretory cells. J. Exp. Biol. 139, 135–150 (1988).
  Medline CASGoogle Scholar
• 11. Saiardi A, Caffrey JJ, Snyder SH, Shears SB. Inositol polyphosphate multikinase (ArgRIII) determines nuclear mRNA export in Saccharomyces cerevisiae. FEBS Lett. 468(1), 28–32 (2000).
  Medline CASGoogle Scholar
• 12. Auesukaree C, Tochio H, Shirakawa M, Kaneko Y, Harashima S. Plc1p, Arg82p, and Kcs1p, enzymes involved in inositol pyrophosphate synthesis, are essential for phosphate regulation and polyphosphate accumulation in Saccharomyces cerevisiae. J. Biol. Chem. 280(26), 25127–25133 (2005).
  Medline CASGoogle Scholar
• 13. Hale AN, Ledbetter DJ, Gawriluk TR, Rucker EB. Autophagy: regulation and role in development. Autophagy 9(7), 951–972 (2013).
  Medline CASGoogle Scholar
• 14. Klionsky DJ, Ohsumi Y. Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell. Dev. Biol. 15, 1–32 (1999).
  Medline CASGoogle Scholar
• 15. Harding TM, Hefner-Gravink A, Thumm M, Klionsky DJ. Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem. 271(30), 17621–17624 (1996).
  Medline CASGoogle Scholar
• 16. Scott SV, Hefner - Gravink A, Morano KA, Noda T, Ohsumi Y, Klionsky DJ. Cytoplasm - to - vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl Acad. Sci. USA 93(22), 12304–12308 (1996).
  Medline CASGoogle Scholar
• 17. Ichimura Y, Kirisako T, Takao T et al. A ubiquitin-like system mediates protein lipidation. Nature 408(6811), 488–492 (2000).
  Medline CASGoogle Scholar
• 18. Kirisako T, Ichimura Y, Okada H et al. The reversible modification regulates the membrane binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J. Cell Biol. 151(2), 263–276 (2000).
  Medline CASGoogle Scholar
• 19. Kirisako T, Baba M, Ishihara N et al. Formation process of autophagosome is traced with Apg8/Aut7p in yeast. J. Cell Biol. 147(2), 435–446 (1999).
  Medline CASGoogle Scholar
• 20. Stromhaug PE, Reggiori F, Guan J, Wang CW, Klionsky DJ. Atg21 is a phosphoinositide binding protein required for efficient lipidation and localization of Atg8 during uptake of aminopeptidase I by selective autophagy. Mol. Biol. Cell 15(8), 3553–3566 (2004).
  Medline CASGoogle Scholar
• 21. Lev Sophie, Li Cecilia, Desmarini Desmarini et al. Fungal inositol pyrophosphate IP7 is crucial for metabolic adaptation to the host environment and pathogenicity. mBio 6(3), 531–546 (2015).
  Google Scholar
• 22. Kihara A, Noda T, Ishihara N, Ohsumi Y. Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J. Cell Biol. 152(3), 519–530 (2001).
  Medline CASGoogle Scholar
• 23. Sarkar S, Floto RA, Berger Z et al. Lithium induces autophagy by inhibiting inositol monophosphatase. J. Cell Biol. 170(7), 1101–1111 (2005).
  Medline CASGoogle Scholar
• 24. Nagata E, Saiardi A, Tsukamoto H et al. Inositol hexakisphosphate kinases promote autophagy. Int. J. Biochem. Cell Biol. 42(12), 2065–2071 (2010).
  Medline CASGoogle Scholar
• 25. Sudbery PE. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9(10), 737–748 (2011).
  Medline CASGoogle Scholar
• 26. Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence 4(2), 119–128 (2013).
  MedlineGoogle Scholar
• 27. Muller M, Reichert AS. Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem. Soc. Trans. 39(5), 1514–1519 (2011).
  MedlineGoogle Scholar
• 28. Chen H, Chan DC. Mitochondrial dynamics – fusion, fission, movement, and mitophagy – in neurodegenerative diseases. Hum. Mol. Genet. 18(2), 169–176 (2009).
  Google Scholar
• 29. Wilson RB, Davis D, Mitchell AP. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181(6), 1868–1874 (1999).
  Medline CASGoogle Scholar
• 30. Wilson RB, Davis D, Mitchell AP. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181(6), 1868–1874 (1999).
  Medline CASGoogle Scholar
• 31. Martínez-Muñoz GA, Kane P. Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J. Biol. Chem. 283(29), 20309–20319 (2008).
  Medline CASGoogle Scholar
• 32. Chang J, Qilin Y, Ning X et al. Role of TFP1 in vacuolar acidification, oxidative stress and filamentous development in Candida albicans. Fungal Genet. Biol. 71, 58–67 (2014). •• Shows that V-ATPase was essential for vacuolar function and C. albicans’ pathogenesis. The methods of filamentous growth assay and virulence assay in this study were helpful for our study.
  MedlineGoogle Scholar
• 33. Brand A, MacCallum DM, Brown AJ, Gow NA, Odds FC. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot. Cell 3(4), 900–909 (2004).
  Medline CASGoogle Scholar
• 34. Thomas AV, Scott DE. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779–792 (1995).
  MedlineGoogle Scholar
• 35. Miguel AP. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64. Fungal. Genet. Biol. 12(42), 963–975 (2005).
  Google Scholar
• 36. Pamela JP, Morris FM, Sergio G, Nicolas D. Alternative mechanisms of vacuolar acidification in H1 - ATPase - deficient Yeast. J. Biol. Chem. 274(52), 37270–37279 (1999).
  MedlineGoogle Scholar
• 37. Theodore TD, Maureen T, Patricia MK. Measurement of vacuolar and cytosolic pH in vivo in yeast cell suspensions. J. Vis. Exp. 74, 50261–50273 (2013).
  Google Scholar
• 38. Kanki T, Wang K, Klionsky DJ. A genomic screen for yeast mutants defective in mitophagy. Autophagy 6(2), 278–280 (2010).
  Medline CASGoogle Scholar
• 39. Baba M, Osumi M, Ohsumi Y. Analysis of the membrane structures involved in autophagy in yeast by freeze - replica method. Cell Struct. Funct. 20(6), 465–471 (1995).
  Medline CASGoogle Scholar
• 40. Baba M, Takeshige K, Baba N, Ohsumi Y. Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J. Cell Biol. 124(6), 903–913 (1994).
  Medline CASGoogle Scholar
• 41. Yorimitsu T, Klionsky DJ. Autophagy: molecular machinery for self-eating. Cell. Death Differ. 12(Suppl. 2), 1542–1552 (2005).
  Medline CASGoogle Scholar
• 42. Johnson RG, Scarpa A. Internal pH of isolated chromaffin vesicles. J. Biol. Chem. 251(7), 2189–2191 (1976).
  Medline CASGoogle Scholar
• 43. Michaelson DM, Angel I. Determination of delta pH in cholinergic synaptic vesicles: its effect on storage and release of acetylcholine. Life Sci. 27(1), 39–44 (1980).
  Medline CASGoogle Scholar
• 44. Füldner HH, Stadler H. 31P-NMR analysis of synaptic vesicles. Status of ATP and internal pH. Eur. J. Biochem. 121(3), 519–524 (1982).
  Medline CASGoogle Scholar
• 45. Sambade M, Kane PM. The yeast vacuolar proton-translocating ATPase contains a subunit homologous to the Manduca sexta and bovine e subunits that is essential for function. J. Biol. Chem. 279(17), 17361–17365 (2004).
  Medline CASGoogle Scholar
• 46. Kane PM. The where, when, and how of organelle acidification by the yeast vacuolar H⁺-ATPase. Microbiol. Mol. Biol. Rev. 70(1), 177–191 (2006).
  Medline CASGoogle Scholar
• 47. Perzov N, Padler - Karavani V, Nelson H, Nelson N. Characterization of yeast V-ATPase mutants lacking Vph1p or Stv1p and the effect on endocytosis. J. Exp. Biol. 205(9), 1209–1219 (2002).
  Medline CASGoogle Scholar
• 48. Drummond DR, Cross RA. Dynamics of interphase microtubules in Schizosaccharomyces pombe. Curr. Biol. 10(13), 766–775 (2000).
  Medline CASGoogle Scholar