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Autophagy in Stationary Phase of Growth

  • José L. Aguilar-López
  • Soledad FunesEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

The growth of microorganisms can be modeled depending on the nutrient availability of the surrounding medium in different stages. Stationary phase is characterized by a general depletion of nutrients and an excess of potentially harmful molecules accumulated during the exponential phase of growth. This situation causes a characteristic stress response where lipid metabolism is essential. Autophagy is a eukaryotic self-degradative process started by various cues when cells enter the stationary phase of growth, and is characterized by degradation of cytosolic contents either damaged or simply used for recycling of biological building blocks. Lipid metabolism is essential for this process since the molecules which are going to be degraded are engulfed by double membrane vesicles that later fuse with the vacuole or the lysosome. In bacteria, there are also several catabolic processes which specifically degrade lipids or proteins and change the metabolic state of the cells in order to resist the stress produced during stationary phase. In this chapter, we discuss the general lipid metabolism associated with entrance of microorganisms to stationary phase that modulate cell fate.

Notes

Acknowledgments

Our work is supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT, México-CB 237344) and the Dirección General de Asuntos del Personal Académico (DGAPA-UNAM, México IN202715).

References

  1. Abeliovich H, Klionsky DJ (2001) Autophagy in yeast: mechanistic insights and physiological function. Microbiol Mol Biol Rev 65:463–479. Table of contents.  https://doi.org/10.1128/MMBR.65.3.463-479.2001CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376.  https://doi.org/10.1007/s00253-002-1135-0CrossRefGoogle Scholar
  3. Antonioli M, Di Rienzo M, Piacentini M, Fimia GM (2017) Emerging mechanisms in initiating and terminating autophagy. Trends Biochem Sci 42:28–41.  https://doi.org/10.1016/j.tibs.2016.09.008CrossRefPubMedGoogle Scholar
  4. Arlia-Ciommo A, Piano A, Leonov A et al (2014) Quasi-programmed aging of budding yeast: a trade-off between programmed processes of cell proliferation, differentiation, stress response, survival and death defines yeast lifespan. Cell Cycle 13:3336–3349.  https://doi.org/10.4161/15384101.2014.965063CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bertram PG, Choi JH, Carvalho J et al (2002) Convergence of TOR-nitrogen and Snf1-glucose signaling pathways onto Gln3. Mol Cell Biol 22:1246–1252.  https://doi.org/10.1128/MCB.22.4.1246-1252.2002CrossRefPubMedPubMedCentralGoogle Scholar
  6. Blommaart EF, Krause U, Schellens JP et al (1997) The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur J Biochem 243:240–246CrossRefGoogle Scholar
  7. Bouchez I, Pouteaux M, Canonge M et al (2015) Regulation of lipid droplet dynamics in Saccharomyces cerevisiae depends on the Rab7-like Ypt7p, HOPS complex and V1-ATPase. Biol Open 4:764–775.  https://doi.org/10.1242/bio.20148615CrossRefPubMedPubMedCentralGoogle Scholar
  8. Burman C, Ktistakis NT (2010) Regulation of autophagy by phosphatidylinositol 3-phosphate. FEBS Lett 584:1302–1312.  https://doi.org/10.1016/j.febslet.2010.01.011CrossRefPubMedGoogle Scholar
  9. Cebollero E, Reggiori F (2009) Regulation of autophagy in yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1793:1413–1421.  https://doi.org/10.1016/j.bbamcr.2009.01.008CrossRefPubMedGoogle Scholar
  10. Cebollero E, van der Vaart A, Zhao M et al (2012) Phosphatidylinositol-3-phosphate clearance plays a key role in autophagosome completion. Curr Biol 22:1545–1553.  https://doi.org/10.1016/j.cub.2012.06.029CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cingolani F, Czaja MJ (2016) Regulation and functions of autophagic lipolysis. Trends Endocrinol Metab 27:696–705.  https://doi.org/10.1016/j.tem.2016.06.003CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cutler NS, Heitman J, Cardenas ME (1999) TOR kinase homologs function in a signal transduction pathway that is conserved from yeast to mammals. Mol Cell Endocrinol 155:135–142CrossRefGoogle Scholar
  13. Dall’Armi C, Devereaux KA, Di Paolo G (2013) The role of lipids in the control of autophagy. Curr Biol 23:R33–R45.  https://doi.org/10.1016/j.cub.2012.10.041CrossRefPubMedPubMedCentralGoogle Scholar
  14. Epple UD, Suriapranata I, Eskelinen EL, Thumm M (2001) Aut5/Cvt17p, a putative lipase essential for disintegration of autophagic bodies inside the vacuole. J Bacteriol 183:5942–5955.  https://doi.org/10.1128/JB.183.20.5942-5955.2001CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fujimoto T, Ohsaki Y, Cheng J et al (2008) Lipid droplets: a classic organelle with new outfits. Histochem Cell Biol 130:263–279.  https://doi.org/10.1007/s00418-008-0449-0CrossRefPubMedPubMedCentralGoogle Scholar
  16. Galdieri L, Mehrotra S, Yu S, Vancura A (2010) Transcriptional regulation in yeast during diauxic shift and stationary phase. OMICS 14:629–638.  https://doi.org/10.1089/omi.2010.0069CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gao Q, Goodman JM (2015) The lipid droplet-a well-connected organelle. Front Cell Dev Biol 3:49.  https://doi.org/10.3389/fcell.2015.00049CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gillooly DJ, Morrow IC, Lindsay M et al (2000) Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells. EMBO J 19:4577–4588.  https://doi.org/10.1093/emboj/19.17.4577CrossRefPubMedPubMedCentralGoogle Scholar
  19. Glick D, Barth S, Macleod KF (2010) Autophagy: cellular and molecular mechanisms. J Pathol 221:3–12.  https://doi.org/10.1002/path.2697CrossRefPubMedPubMedCentralGoogle Scholar
  20. Grogan DW, Cronan JE (1997) Cyclopropane ring formation in membrane lipids of bacteria. Microbiol Mol Biol Rev 61(4):429–441PubMedPubMedCentralGoogle Scholar
  21. Hengge-Aronis R (2002) Recent insights into the general stress response regulatory network in Escherichia coli. J Mol Microbiol Biotechnol 4:341–346PubMedGoogle Scholar
  22. Huisman GW, Siegele DA, Zambrano MM, Kolter R (1996) Morphological and physiological changes during stationary phase. In: Neidhardt FC, Curtis R III, Ingraham JL, ECC L, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology, vol 2, 2nd edn. ASM Press, Washington, DC, pp 1672–1682Google Scholar
  23. Jaber N, Zong W-X (2013) Class III PI3K Vps34: essential roles in autophagy, endocytosis, and heart and liver function. Ann N Y Acad Sci 1280:48–51.  https://doi.org/10.1111/nyas.12026CrossRefPubMedGoogle Scholar
  24. Kihara A, Noda T, Ishihara N, Ohsumi Y (2001) Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae. J Cell Biol 152:519–530CrossRefGoogle Scholar
  25. Klionsky DJ, Codogno P (2013) The mechanism and physiological function of macroautophagy. J Innate Immun 5:427–433.  https://doi.org/10.1159/000351979CrossRefPubMedGoogle Scholar
  26. Knævelsrud H, Simonsen A (2012) Lipids in autophagy: constituents, signaling molecules and cargo with relevance to disease. Biochim Biophys Acta 1821:1133–1145.  https://doi.org/10.1016/j.bbalip.2012.01.001CrossRefPubMedGoogle Scholar
  27. Książek K (2010) Let’s stop overlooking bacterial aging. Biogerontology 11:717–723.  https://doi.org/10.1007/s10522-010-9278-3CrossRefPubMedGoogle Scholar
  28. Lillie SH, Pringle JR (1980) Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143:1384–1394PubMedPubMedCentralGoogle Scholar
  29. Lippai M, Szatmári Z (2017) Autophagy-from molecular mechanisms to clinical relevance. Cell Biol Toxicol 33:145–168.  https://doi.org/10.1007/s10565-016-9374-5CrossRefPubMedGoogle Scholar
  30. Loewith R, Jacinto E, Wullschleger S et al (2002) Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol Cell 10:457–468CrossRefGoogle Scholar
  31. Longatti A, Tooze SA (2009) Vesicular trafficking and autophagosome formation. Cell Death Differ 16:956–965.  https://doi.org/10.1038/cdd.2009.39CrossRefPubMedGoogle Scholar
  32. Longo VD, Liou LL, Valentine JS, Gralla EB (1999) Mitochondrial superoxide decreases yeast survival in stationary phase. Arch Biochem Biophys 365:131–142.  https://doi.org/10.1006/abbi.1999.1158CrossRefPubMedGoogle Scholar
  33. Lushchak O, Strilbytska O, Piskovatska V et al (2017) The role of the TOR pathway in mediating the link between nutrition and longevity. Mech Ageing Dev.  https://doi.org/10.1016/j.mad.2017.03.005CrossRefGoogle Scholar
  34. Mayordomo I, Estruch F, Sanz P (2002) Convergence of the target of rapamycin and the Snf1 protein kinase pathways in the regulation of the subcellular localization of Msn2, a transcriptional activator of STRE (stress response element)-regulated genes. J Biol Chem 277:35650–35656.  https://doi.org/10.1074/jbc.M204198200CrossRefPubMedGoogle Scholar
  35. Mitchison JM (2003) Growth during the cell cycle. Int Rev Cytol 226:165–258CrossRefGoogle Scholar
  36. Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132.  https://doi.org/10.1146/annurev-cellbio-092910-154005CrossRefPubMedGoogle Scholar
  37. Nair U, Yen W-L, Mari M et al (2012) A role for Atg8-PE deconjugation in autophagosome biogenesis. Autophagy 8:780–793.  https://doi.org/10.4161/auto.19385CrossRefPubMedPubMedCentralGoogle Scholar
  38. Navarro Llorens JM, Tormo A, Martínez-García E (2010) Stationary phase in gram-negative bacteria. FEMS Microbiol Rev 34:476–495.  https://doi.org/10.1111/j.1574-6976.2010.00213.xCrossRefPubMedGoogle Scholar
  39. Nguyen LN, Bormann J, Le GTT et al (2011) Autophagy-related lipase FgATG15 of Fusarium graminearum is important for lipid turnover and plant infection. Fungal Genet Biol 48:217–224.  https://doi.org/10.1016/j.fgb.2010.11.004CrossRefPubMedGoogle Scholar
  40. Noda NN, Inagaki F (2015) Mechanisms of autophagy. Annu Rev Biophys 44:101–122.  https://doi.org/10.1146/annurev-biophys-060414-034248CrossRefPubMedGoogle Scholar
  41. Noda T, Ohsumi Y (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273:3963–3966CrossRefGoogle Scholar
  42. Nyström T (2004) Stationary-phase physiology. Annu Rev Microbiol 58:161–181.  https://doi.org/10.1146/annurev.micro.58.030603.123818CrossRefPubMedGoogle Scholar
  43. Obara K, Ohsumi Y (2011) PtdIns 3-kinase orchestrates autophagosome formation in yeast. J Lipids 2011:498768–498769.  https://doi.org/10.1155/2011/498768CrossRefPubMedPubMedCentralGoogle Scholar
  44. Obara K, Noda T, Niimi K, Ohsumi Y (2008) Transport of phosphatidylinositol 3-phosphate into the vacuole via autophagic membranes in Saccharomyces cerevisiae. Genes Cells 13:537–547.  https://doi.org/10.1111/j.1365-2443.2008.01188.xCrossRefPubMedGoogle Scholar
  45. Oh-oka K, Nakatogawa H, Ohsumi Y (2008) Physiological pH and acidic phospholipids contribute to substrate specificity in lipidation of Atg8. J Biol Chem 283:21847–21852.  https://doi.org/10.1074/jbc.M801836200CrossRefPubMedGoogle Scholar
  46. Robinson JS, Klionsky DJ, Banta LM, Emr SD (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol Cell Biol 8:4936–4948CrossRefGoogle Scholar
  47. Sampaio-Marques B, Burhans WC, Ludovico P (2014) Longevity pathways and maintenance of the proteome: the role of autophagy and mitophagy during yeast ageing. Microb Cell 1:118–127.  https://doi.org/10.15698/mic2014.04.136CrossRefPubMedPubMedCentralGoogle Scholar
  48. Schaaf MBE, Keulers TG, Vooijs MA, Rouschop KMA (2016) LC3/GABARAP family proteins: autophagy-(un)related functions. FASEB J 30:3961–3978.  https://doi.org/10.1096/fj.201600698RCrossRefPubMedGoogle Scholar
  49. Schroeder B, Schulze RJ, Weller SG et al (2015) The small GTPase Rab7 as a central regulator of hepatocellular lipophagy. Hepatology 61:1896–1907.  https://doi.org/10.1002/hep.27667CrossRefPubMedPubMedCentralGoogle Scholar
  50. Shibutani ST, Yoshimori T (2014) A current perspective of autophagosome biogenesis. Cell Res 24:58–68.  https://doi.org/10.1038/cr.2013.159CrossRefPubMedGoogle Scholar
  51. Shpilka T, Welter E, Borovsky N et al (2015) Lipid droplets and their component triglycerides and steryl esters regulate autophagosome biogenesis. EMBO J 34:2117–2131.  https://doi.org/10.15252/embj.201490315CrossRefPubMedPubMedCentralGoogle Scholar
  52. Simonsen A, Tooze SA (2009) Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J Cell Biol 186:773–782.  https://doi.org/10.1083/jcb.200907014CrossRefPubMedPubMedCentralGoogle Scholar
  53. Singh R, Kaushik S, Wang Y et al (2009) Autophagy regulates lipid metabolism. Nature 458:1131–1135.  https://doi.org/10.1038/nature07976CrossRefPubMedPubMedCentralGoogle Scholar
  54. Spandl J, Lohmann D, Kuerschner L et al (2011) Ancient ubiquitous protein 1 (AUP1) localizes to lipid droplets and binds the E2 ubiquitin conjugase G2 (Ube2g2) via its G2 binding region. J Biol Chem 286:5599–5606.  https://doi.org/10.1074/jbc.M110.190785CrossRefPubMedGoogle Scholar
  55. Stack JH, DeWald DB, Takegawa K, Emr SD (1995) Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J Cell Biol 129:321–334CrossRefGoogle Scholar
  56. Stephan JS, Yeh Y-Y, Ramachandran V et al (2009) The Tor and PKA signaling pathways independently target the Atg1/Atg13 protein kinase complex to control autophagy. Proc Natl Acad Sci U S A 106:17049–17054.  https://doi.org/10.1073/pnas.0903316106CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sutterlin HA, Shi H, May KL et al (2016) Disruption of lipid homeostasis in the Gram-negative cell envelope activates a novel cell death pathway. Proc Natl Acad Sci U S A 113:E1565–E1574.  https://doi.org/10.1073/pnas.1601375113CrossRefPubMedPubMedCentralGoogle Scholar
  58. Tissenbaum HA, Guarente L (2002) Model organisms as a guide to mammalian aging. Dev Cell 2:9–19CrossRefGoogle Scholar
  59. Walther TC, Farese RV (2012) Lipid droplets and cellular lipid metabolism. Annu Rev Biochem 81:687–714.  https://doi.org/10.1146/annurev-biochem-061009-102430CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wang AY, Cronan JE (1994) The growth phase dependent synthesis of cyclopropane fatty acids in Escherichia coli is due to an RpoS (KatF) dependent promoter plus enzyme instability. Mol Microbiol 11:1009–1017CrossRefGoogle Scholar
  61. Wang C-W, Miao Y-H, Chang Y-S (2014) A sterol-enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast. J Cell Biol 206:357–366.  https://doi.org/10.1083/jcb.201404115CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ward C, Martinez-Lopez N, Otten EG et al (2016) Autophagy, lipophagy and lysosomal lipid storage disorders. Biochim Biophys Acta 1861:269–284.  https://doi.org/10.1016/j.bbalip.2016.01.006CrossRefPubMedGoogle Scholar
  63. Weidberg H, Shvets E, Elazar Z (2009) Lipophagy: selective catabolism designed for lipids. Dev Cell 16:628–630.  https://doi.org/10.1016/j.devcel.2009.05.001CrossRefPubMedGoogle Scholar
  64. Zhang N, Cao L (2017) Starvation signals in yeast are integrated to coordinate metabolic reprogramming and stress response to ensure longevity. Curr Genet 26:4818–4815.  https://doi.org/10.1007/s00294-017-0697-4CrossRefGoogle Scholar
  65. Zhang Y-M, Rock CO (2009) Transcriptional regulation in bacterial membrane lipid synthesis. J Lipid Res 50(Suppl):S115–S119.  https://doi.org/10.1194/jlr.R800046-JLR200CrossRefPubMedPubMedCentralGoogle Scholar
  66. van Zutphen T, Todde V, de Boer R et al (2014) Lipid droplet autophagy in the yeast Saccharomyces cerevisiae. Mol Biol Cell 25:290–301.  https://doi.org/10.1091/mbc.E13-08-0448CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Departamento de Genética Molecular, División de Investigación BásicaInstituto de Fisiología Celular, Universidad Nacional Autónoma de MéxicoMexicoMexico

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