#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

AMPK regulates ESCRT-dependent microautophagy of proteasomes concomitant with proteasome storage granule assembly during glucose starvation


Autoři: Jianhui Li aff001;  Michal Breker aff002;  Morven Graham aff003;  Maya Schuldiner aff002;  Mark Hochstrasser aff001
Působiště autorů: Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, Connecticut, United States of America aff001;  Department of Molecular Genetics, Weizmann Institute of Sciences, Rehovot, Israel aff002;  Center for Cellular and Molecular Imaging, School of Medicine, Yale University, New Haven, Connecticut, United States of America aff003;  Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America aff004
Vyšlo v časopise: AMPK regulates ESCRT-dependent microautophagy of proteasomes concomitant with proteasome storage granule assembly during glucose starvation. PLoS Genet 15(11): e1008387. doi:10.1371/journal.pgen.1008387
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008387

Souhrn

The ubiquitin-proteasome system regulates numerous cellular processes and is central to protein homeostasis. In proliferating yeast and many mammalian cells, proteasomes are highly enriched in the nucleus. In carbon-starved yeast, proteasomes migrate to the cytoplasm and collect in proteasome storage granules (PSGs). PSGs dissolve and proteasomes return to the nucleus within minutes of glucose refeeding. The mechanisms by which cells regulate proteasome homeostasis under these conditions remain largely unknown. Here we show that AMP-activated protein kinase (AMPK) together with endosomal sorting complexes required for transport (ESCRTs) drive a glucose starvation-dependent microautophagy pathway that preferentially sorts aberrant proteasomes into the vacuole, thereby biasing accumulation of functional proteasomes in PSGs. The proteasome core particle (CP) and regulatory particle (RP) are regulated differently. Without AMPK, the insoluble protein deposit (IPOD) serves as an alternative site that specifically sequesters CP aggregates. Our findings reveal a novel AMPK-controlled ESCRT-mediated microautophagy mechanism in the regulation of proteasome trafficking and homeostasis under carbon starvation.

Klíčová slova:

Autophagic cell death – Fluorescence microscopy – Glucose – Homeostasis – Immunoblot analysis – Proteasomes – Vacuoles – Yeast


Zdroje

1. Tomko RJ, Hochstrasser M. Molecular architecture and assembly of the eukaryotic proteasome. Annu Rev Biochem. 2013;82:415–45. doi: 10.1146/annurev-biochem-060410-150257 23495936

2. Finley D, Ulrich HD, Sommer T, Kaiser P. The ubiquitin–proteasome system of Saccharomyces cerevisiae. Genetics. 2012;192(2):319–60. doi: 10.1534/genetics.112.140467 23028185

3. Budenholzer L, Cheng CL, Li Y, Hochstrasser M. Proteasome structure and assembly. J Mol Biol. 2017;429(22):3500–24. doi: 10.1016/j.jmb.2017.05.027 28583440

4. Livneh I, Cohen-Kaplan V, Cohen-Rosenzweig C, Avni N, Ciechanover A. The life cycle of the 26S proteasome: from birth, through regulation and function, and onto its death. Cell Res. 2016;26(8):869–85. doi: 10.1038/cr.2016.86 27444871

5. Collins GA, Goldberg AL. The logic of the 26S proteasome. Cell. 2017;169(5):792–806. doi: 10.1016/j.cell.2017.04.023 28525752

6. Rock KL, Gramm C, Rothstein L, Clark K, Stein R, Dick L, et al. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell. 1994;78(5):761–71. doi: 10.1016/s0092-8674(94)90462-6 8087844

7. Balch WE, Morimoto RI, Dillin A, Kelly JW. Adapting proteostasis for disease intervention. Science. 2008;319(5865):916–9. doi: 10.1126/science.1141448 18276881

8. Mayor T, Sharon M, Glickman MH. Tuning the proteasome to brighten the end of the journey. Am J Physiol Cell Physiol. 2016;311(5):C793–C804. doi: 10.1152/ajpcell.00198.2016 27605452

9. Chondrogianni N, Voutetakis K, Kapetanou M, Delitsikou V, Papaevgeniou N, Sakellari M, et al. Proteasome activation: An innovative promising approach for delaying aging and retarding age-related diseases. Ageing Res Rev. 2015;23:37–55. doi: 10.1016/j.arr.2014.12.003 25540941

10. Vilchez D, Saez I, Dillin A. The role of protein clearance mechanisms in organismal ageing and age-related diseases. Nat Commun. 2014;5:5659. doi: 10.1038/ncomms6659 25482515

11. van Deventer S, Menendez-Benito V, van Leeuwen F, Neefjes J. N-terminal acetylation and replicative age affect proteasome localization and cell fitness during aging. J Cell Sci. 2015;128(1):109–17. doi: 10.1242/jcs.157354 25413350

12. Saunier R, Esposito M, Dassa EP, Delahodde A. Integrity of the Saccharomyces cerevisiae Rpn11 protein is critical for formation of proteasome storage granules (PSG) and survival in stationary phase. PLoS One. 2013;8(8):e70357. doi: 10.1371/journal.pone.0070357 23936414

13. Laporte D, Salin B, Daignan-Fornier B, Sagot I. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol. 2008;181(5):737–45. doi: 10.1083/jcb.200711154 18504300

14. Peters LZ, Hazan R, Breker M, Schuldiner M, Ben-Aroya S. Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. J Cell Biol. 2013;201(5):663–71. doi: 10.1083/jcb.201211146 23690178

15. Weberruss MH, Savulescu AF, Jando J, Bissinger T, Harel A, Glickman MH, et al. Blm10 facilitates nuclear import of proteasome core particles. EMBO J. 2013;32(20):2697–707. doi: 10.1038/emboj.2013.192 23982732

16. Peters LZ, Karmon O, David-Kadoch G, Hazan R, Yu T, Glickman MH, et al. The protein quality control machinery regulates its misassembled proteasome subunits. PLoS Genet. 2015;11(4):e1005178. doi: 10.1371/journal.pgen.1005178 25919710

17. Peters LZ, Karmon O, Miodownik S, Ben-Aroya S. Proteasome storage granules are transiently associated with the insoluble protein deposit in Saccharomyces cerevisiae. J Cell Sci. 2016;129(6):1190–7. doi: 10.1242/jcs.179648 26826189

18. Gatica D, Lahiri V, Klionsky DJ. Cargo recognition and degradation by selective autophagy. Nat Cell Biol. 2018;20(3):233–42. doi: 10.1038/s41556-018-0037-z 29476151

19. Suzuki K, Kubota Y, Sekito T, Ohsumi Y. Hierarchy of Atg proteins in pre-autophagosomal structure organization. Genes Cells. 2007;12(2):209–18. doi: 10.1111/j.1365-2443.2007.01050.x 17295840

20. Suzuki K, Ohsumi Y. Current knowledge of the pre-autophagosomal structure (PAS). FEBS Lett. 2010;584(7):1280–6. doi: 10.1016/j.febslet.2010.02.001 20138172

21. Reggiori F, Klionsky DJ. Autophagic processes in yeast: Mechanism, machinery and regulation. Genetics. 2013;194(2):341–61. doi: 10.1534/genetics.112.149013 23733851

22. Oku M, Maeda Y, Kagohashi Y, Kondo T, Yamada M, Fujimoto T, et al. Evidence for ESCRT- and clathrin-dependent microautophagy. J Cell Biol. 2017;216(10):3263–74. doi: 10.1083/jcb.201611029 28838958

23. Christ L, Raiborg C, Wenzel EM, Campsteijn C, Stenmark H. Cellular functions and molecular mechanisms of the ESCRT membrane-scission machinery. Trends Biochem Sci. 2017;42(1):42–56. doi: 10.1016/j.tibs.2016.08.016 27669649

24. Hurley JH. ESCRTs are everywhere. EMBO J. 2015;34:2398–407. doi: 10.15252/embj.201592484 26311197

25. Pack C-G, Yukii H, Toh-e A, Kudo T, Tsuchiya H, Kaiho A, et al. Quantitative live-cell imaging reveals spatio-temporal dynamics and cytoplasmic assembly of the 26S proteasome. Nat Commun. 2014;5:3396. doi: 10.1038/ncomms4396 24598877

26. Marshall RS, McLoughlin F, Vierstra RD. Autophagic turnover of inactive 26S proteasomes in yeast is directed by the ubiquitin receptor Cue5 and the Hsp42 chaperone. Cell Rep. 2016;16(6):1717–32. doi: 10.1016/j.celrep.2016.07.015 27477278

27. Waite KA, Mota-Peynado AD-L, Vontz G, Roelofs J. Starvation induces proteasome autophagy with different pathways for core and regulatory particles. J Biol Chem. 2016;291(7):3239–53. doi: 10.1074/jbc.M115.699124 26670610

28. Nemec AA, Howell LA, Peterson AK, Murray MA, Tomko RJ. Autophagic clearance of proteasomes in yeast requires the conserved sorting nexin Snx4. J Biol Chem. 2017;292(52):21466–80. doi: 10.1074/jbc.M117.817999 29109144

29. Marshall Richard S, Li F, Gemperline David C, Book Adam J, Vierstra Richard D. Autophagic Degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell. 2015;58(6):1053–66. doi: 10.1016/j.molcel.2015.04.023 26004230

30. Cohen-Kaplan V, Livneh I, Avni N, Fabre B, Ziv T, Kwon YT, et al. p62- and ubiquitin-dependent stress-induced autophagy of the mammalian 26S proteasome. Proc Natl Acad Sci USA. 2016;113(47):E7490–E9. doi: 10.1073/pnas.1615455113 27791183

31. Marshall RS, Vierstra RD. Proteasome storage granules protect proteasomes from autophagic degradation upon carbon starvation. eLife. 2018;7:e34532. doi: 10.7554/eLife.34532 29624167

32. Hedbacker K, Carlson M. SNF1/AMPK pathways in yeast. Front Biosci. 2008;13:2408–20. doi: 10.2741/2854 17981722

33. Usaite R, Jewett MC, Oliveira AP, Yates JR, Olsson L, Nielsen J. Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator. Mol Syst Biol. 2009;5(1). doi: 10.1038/msb.2009.67 19888214

34. Mihaylova MM, Shaw RJ. The AMPK signalling pathway coordinates cell growth, autophagy and metabolism. Nat Cell Biol. 2011;13:1016. doi: 10.1038/ncb2329 21892142

35. Giaever G, Chu AM, Ni L, Connelly C, Riles L, Véronneau S, et al. Functional profiling of the Saccharomyces cerevisiae genome. Nature. 2002;418:387. doi: 10.1038/nature00935 12140549

36. Yan Tong AH, Boone C. Synthetic genetic array analysis in Saccharomyces cerevisiae. In: Xiao W, editor. Yeast Protocol. Totowa, NJ: Humana Press; 2006. p. 171–91.

37. Breker M, Gymrek M, Schuldiner M. A novel single-cell screening platform reveals proteome plasticity during yeast stress responses. J Cell Biol. 2013;200(6):839–50. doi: 10.1083/jcb.201301120 23509072

38. Gu ZC, Wu E, Sailer C, Jando J, Styles E, Eisenkolb I, et al. Ubiquitin orchestrates proteasome dynamics between proliferation and quiescence in yeast. Mol Biol Cell. 2017;28(19):2479–91. doi: 10.1091/mbc.E17-03-0162 28768827

39. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011;331(6016):456–61. Epub 2010/12/23. doi: 10.1126/science.1196371 21205641

40. Kim J, Kundu M, Viollet B, Guan K-L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132. doi: 10.1038/ncb2152 21258367

41. Lefebvre C, Legouis R, Culetto E. ESCRT and autophagies: Endosomal functions and beyond. Semin Cell Dev Biol. 2018;74:21–8. doi: 10.1016/j.semcdb.2017.08.014 28807884

42. Adachi A, Koizumi M, Ohsumi Y. Autophagy induction under carbon starvation conditions is negatively regulated by carbon catabolite repression. J Biol Chem. 2017;292(48):19905–18. doi: 10.1074/jbc.M117.817510 29042435

43. Russell MRG, Shideler T, Nickerson DP, West M, Odorizzi G. Class E compartments form in response to ESCRT dysfunction in yeast due to hyperactivity of the Vps21 Rab GTPase. J Cell Sci. 2012;125(21):5208–20. doi: 10.1242/jcs.111310 22899724

44. Kaganovich D, Kopito R, Frydman J. Misfolded proteins partition between two distinct quality control compartments. Nature. 2008;454(7208):1088–95. doi: 10.1038/nature07195 18756251

45. Shpilka T, Weidberg H, Pietrokovski S, Elazar Z. Atg8: an autophagy-related ubiquitin-like protein family. Genome Biol. 2011;12(7):226–. doi: 10.1186/gb-2011-12-7-226 21867568

46. Visvanathan R, Ram R. ATG15 encodes a phospholipase and is transcriptionally regulated by YAP1 in Saccharomyces cerevisiae. FEBS Lett. 2016;590(18):3155–67. doi: 10.1002/1873-3468.12369 27543826

47. Hecht KA, O’Donnell AF, Brodsky JL. The proteolytic landscape of the yeast vacuole. Cell Logist. 2014;4:e28023. doi: 10.4161/cl.28023 24843828

48. Tomko Robert J Jr, Hochstrasser M. The intrinsically disordered Sem1 protein functions as a molecular tether during proteasome lid biogenesis. Mol Cell. 2014;53(3):433–43. doi: 10.1016/j.molcel.2013.12.009 24412063

49. Velichutina I, Connerly PL, Arendt CS, Li X, Hochstrasser M. Plasticity in eucaryotic 20S proteasome ring assembly revealed by a subunit deletion in yeast. EMBO J. 2004;23(3):500–10. doi: 10.1038/sj.emboj.7600059 14739934

50. Zhou F, Wu Z, Zhao M, Murtazina R, Cai J, Zhang A, et al. Rab5-dependent autophagosome closure by ESCRT. J Cell Biol. 2019:jcb.201811173. doi: 10.1083/jcb.201811173 31010855

51. Stoten CL, Carlton JG. ESCRT-dependent control of membrane remodelling during cell division. Semin Cell Dev Biol. 2018;74:50–65. doi: 10.1016/j.semcdb.2017.08.035 28843980

52. Monroe N, Han H, Shen PS, Sundquist WI, Hill CP. Structural basis of protein translocation by the Vps4-Vta1 AAA ATPase. eLife. 2017;6:e24487. doi: 10.7554/eLife.24487 28379137

53. de la Peña AH, Goodall EA, Gates SN, Lander GC, Martin A. Substrate-engaged 26S proteasome structures reveal mechanisms for ATP-hydrolysis–driven translocation. Science. 2018;362(6418). doi: 10.1126/science.aav0725 30309908

54. Bajorek M, Finley D, Glickman MH. Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr Biol. 2003;13(13):1140–4. doi: 10.1016/s0960-9822(03)00417-2 12842014

55. Liu X-M, Sun L-L, Hu W, Ding Y-H, Dong M-Q, Du L-L. ESCRTs cooperate with a selective autophagy receptor to mediate vacuolar targeting of soluble cargos. Mol Cell. 2015;59(6):1035–42. doi: 10.1016/j.molcel.2015.07.034 26365378

56. Zhu L, Jorgensen JR, Li M, Chuang Y-S, Emr SD. ESCRTs function directly on the lysosome membrane to downregulate ubiquitinated lysosomal membrane proteins. eLife. 2017;6:e26403. doi: 10.7554/eLife.26403 28661397

57. Bilodeau PS, Urbanowski JL, Winistorfer SC, Piper RC. The Vps27p–Hse1p complex binds ubiquitin and mediates endosomal protein sorting. Nat Cell Biol. 2002;4:534. doi: 10.1038/ncb815 12055639

58. Papinski D, Kraft C. Regulation of autophagy by signaling through the Atg1/ULK1 complex. J Mol Biol. 2016;428(9, Part A):1725–41. doi: 10.1016/j.jmb.2016.03.030 27059781

59. Oku M, Sakai Y. Three distinct types of microautophagy based on membrane dynamics and molecular machineries. BioEssays. 2018;40(6):1800008. doi: 10.1002/bies.201800008 29708272

60. Toulmay A, Prinz WA. Direct imaging reveals stable, micrometer-scale lipid domains that segregate proteins in live cells. J Cell Biol. 2013;202(1):35–44. doi: 10.1083/jcb.201301039 23836928

61. Wang C-W, Miao Y-H, Chang Y-S. A sterol-enriched vacuolar microdomain mediates stationary phase lipophagy in budding yeast. J Cell Biol. 2014;206(3):357–66. doi: 10.1083/jcb.201404115 25070953

62. Seo AY, Lau P-W, Feliciano D, Sengupta P, Gros MAL, Cinquin B, et al. AMPK and vacuole-associated Atg14p orchestrate μ-lipophagy for energy production and long-term survival under glucose starvation. eLife. 2017;6:e21690. doi: 10.7554/eLife.21690 28394250

63. Dunham MJ, Gartenberg MR, Brown GW. Methods in Yeast Genetics and Genomics: Cold Spring Harbor Laboratory Press; 2015. 233 p.

64. Li J, Fuchs S, Zhang J, Wellford S, Schuldiner M, Wang X. An unrecognized function for COPII components in recruiting the viral replication protein BMV 1a to the perinuclear ER. J Cell Sci. 2016;129(19):3597–608. doi: 10.1242/jcs.190082 27539921

65. Tokuyasu KT. A technique for ultracryotomy of cell suspensions and tissues. J Cell Bio. 1973;57(2):551–65. doi: 10.1083/jcb.57.2.551 4121290

66. Kushnirov VV. Rapid and reliable protein extraction from yeast. Yeast. 2000;16(9):857–60. doi: 10.1002/1097-0061(20000630)16:9<857::AID-YEA561>3.0.CO;2-B 10861908

67. Mruk DD, Cheng CY. Enhanced chemiluminescence (ECL) for routine immunoblotting: An inexpensive alternative to commercially available kits. Spermatogenesis. 2011;1(2):121–2. doi: 10.4161/spmg.1.2.16606 22319660

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2019 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Svět praktické medicíny 3/2024 (znalostní test z časopisu)
nový kurz

Kardiologické projevy hypereozinofilií
Autoři: prof. MUDr. Petr Němec, Ph.D.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Aktuální možnosti diagnostiky a léčby litiáz
Autoři: MUDr. Tomáš Ürge, PhD.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Všechny kurzy
Kurzy Podcasty Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#