E3 Ubiquitin Ligase CHIP and NBR1-Mediated Selective Autophagy Protect Additively against Proteotoxicity in Plant Stress Responses

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Plant stress responses require both protective measures that reduce or restore stress-inflicted damage to cellular structures and mechanisms that efficiently remove damaged and toxic macromolecules, such as misfolded and damaged proteins. We have recently reported that NBR1, the first identified plant autophagy adaptor with a ubiquitin-association domain, plays a critical role in plant stress tolerance by targeting stress-induced, ubiquitinated protein aggregates for degradation by autophagy. Here we report a comprehensive genetic analysis of CHIP, a chaperone-associated E3 ubiquitin ligase from Arabidopsis thaliana implicated in mediating degradation of nonnative proteins by 26S proteasomes. We isolated two chip knockout mutants and discovered that they had the same phenotypes as the nbr1 mutants with compromised tolerance to heat, oxidative and salt stresses and increased accumulation of insoluble proteins under heat stress. To determine their functional interactions, we generated chip nbr1 double mutants and found them to be further compromised in stress tolerance and in clearance of stress-induced protein aggregates, indicating additive roles of CHIP and NBR1. Furthermore, stress-induced protein aggregates were still ubiquitinated in the chip mutants. Through proteomic profiling, we systemically identified heat-induced protein aggregates in the chip and nbr1 single and double mutants. These experiments revealed that highly aggregate-prone proteins such as Rubisco activase and catalases preferentially accumulated in the nbr1 mutant while a number of light-harvesting complex proteins accumulated at high levels in the chip mutant after a relatively short period of heat stress. With extended heat stress, aggregates for a large number of intracellular proteins accumulated in both chip and nbr1 mutants and, to a greater extent, in the chip nbr1 double mutant. Based on these results, we propose that CHIP and NBR1 mediate two distinct but complementary anti-proteotoxic pathways and protein's propensity to aggregate under stress conditions is one of the critical factors for pathway selection of protein degradation.

Vyšlo v časopise: E3 Ubiquitin Ligase CHIP and NBR1-Mediated Selective Autophagy Protect Additively against Proteotoxicity in Plant Stress Responses. PLoS Genet 10(1): e32767. doi:10.1371/journal.pgen.1004116
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004116

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Zdroje

1. ShaidS, BrandtsCH, ServeH, DikicI (2013) Ubiquitination and selective autophagy. Cell Death Differ 20 : 21–30.

2. LyzengaWJ, StoneSL (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63 : 599–616.

3. ChristensenAH, SharrockRA, QuailPH (1992) Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promoter activity following transfer to protoplasts by electroporation. Plant Mol Biol 18 : 675–689.

4. GenschikP, ParmentierY, DurrA, MarbachJ, CriquiMC, et al. (1992) Ubiquitin genes are differentially regulated in protoplast-derived cultures of Nicotiana sylvestris and in response to various stresses. Plant Mol Biol 20 : 897–910.

5. SunCW, CallisJ (1997) Independent modulation of Arabidopsis thaliana polyubiquitin mRNAs in different organs and in response to environmental changes. Plant J 11 : 1017–1027.

6. GuoQF, ZhangJ, GaoQ, XingSC, LiF, et al. (2008) Drought tolerance through overexpression of monoubiquitin in transgenic tobacco. Journal of Plant Physiology 165 : 1745–1755.

7. KurepaJ, KarangwaC, DukeLS, SmalleJA (2010) Arabidopsis sensitivity to protein synthesis inhibitors depends on 26S proteasome activity. Plant Cell Rep 29 : 249–259.

8. WangSH, KurepaJ, SmalleJA (2009) The Arabidopsis 26S proteasome subunit RPN1a is required for optimal plant growth and stress responses. Plant and Cell Physiology 50 : 1721–1725.

9. KurepaJ, WangS, LiY, ZaitlinD, PierceAJ, et al. (2009) Loss of 26S proteasome function leads to increased cell size and decreased cell number in Arabidopsis shoot organs. Plant Physiol 150 : 178–189.

10. KurepaJ, Toh-eA, SmalleJA (2008) 26S proteasome regulatory particle mutants have increased oxidative stress tolerance. Plant Journal 53 : 102–114.

11. SmalleJ, KurepaJ, YangPZ, EmborgTJ, BabiychukE, et al. (2003) The pleiotropic role of the 26S proteasome subunit RPN10 in Arabidopsis growth and development supports a substrate-specific function in abscisic acid signaling. Plant Cell 15 : 965–980.

12. BarralJM, BroadleySA, SchaffarG, HartlFU (2004) Roles of molecular chaperones in protein misfolding diseases. Seminars in cell & developmental biology 15 : 17–29.

13. RossCA, PoirierMA (2005) Opinion: What is the role of protein aggregation in neurodegeneration? Nature reviews Molecular cell biology 6 : 891–898.

14. KlionskyDJ (2005) Autophagy. Curr Biol 15: R282–283.

15. BasshamDC (2007) Plant autophagy-more than a starvation response. Current Opinion in Plant Biology 10 : 587–593.

16. BasshamDC, LaporteM, MartyF, MoriyasuY, OhsumiY, et al. (2006) Autophagy in development and stress responses of plants. Autophagy 2 : 2–11.

17. FloydBE, MorrissSC, MacintoshGC, BasshamDC (2012) What to eat: evidence for selective autophagy in plants. Journal of integrative plant biology 54 : 907–920.

18. JohansenT, LamarkT (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7 : 279–296.

19. SvenningS, LamarkT, KrauseK, JohansenT (2011) Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7 : 993–1010.

20. ZhouJ, WangJ, ChengY, ChiYJ, FanB, et al. (2013) NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet 9: e1003196.

21. ArndtV, RogonC, HohfeldJ (2007) To be, or not to be -⁠ molecular chaperones in protein degradation. Cellular and Molecular Life Sciences 64 : 2525–2541.

22. HohfeldJ, CyrDM, PattersonC (2001) From the cradle to the grave: molecular chaperones that may choose between folding and degradation. EMBO reports 2 : 885–890.

23. BallingerCA, ConnellP, WuYX, HuZY, ThompsonLJ, et al. (1999) Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Molecular and Cellular Biology 19 : 4535–4545.

24. KaliaLV, KaliaSK, ChauH, LozanoAM, HymanBT, et al. (2011) Ubiquitinylation of alpha-Synuclein by Carboxyl Terminus Hsp70-Interacting Protein (CHIP) Is Regulated by Bcl-2-Associated Athanogene 5 (BAG5). Plos One 6: e14695.

25. TetzlaffJE, PutchaP, OuteiroTF, IvanovA, BerezovskaO, et al. (2008) CHIP targets toxic alpha-synuclein oligomers for degradation. Journal of Biological Chemistry 283 : 17962–17968.

26. ShinYG, KluckenJ, PattersonC, HymanBT, McLeanPJ (2005) The co-chaperone carboxyl terminus of Hsp70-interacting protein (CHIP) mediates alpha-synuclein degradation decisions between proteasomal and lysosomal pathways. Journal of Biological Chemistry 280 : 23727–23734.

27. DickeyCA, PattersonC, DicksonD, PetrucelliL (2007) Brain CHIP: removing the culprits in neurodegenerative disease. Trends in molecular medicine 13 : 32–38.

28. SaharaN, MurayamaM, MizorokiT, UrushitaniM, ImaiY, et al. (2005) In vivo evidence of CHIP up-regulation attenuating tau aggregation. Journal of Neurochemistry 94 : 1254–1263.

29. ImaiY, SodaM, HatakeyamaS, AkagiT, HashikawaT, et al. (2002) CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Molecular Cell 10 : 55–67.

30. DaiQ, ZhangCL, WuYX, McDonoughH, WhaleyRA, et al. (2003) CHIP activates HSF1 and confers protection against apoptosis and cellular stress. Embo Journal 22 : 5446–5458.

31. MinJN, WhaleyRA, SharplessNE, LockyerP, PortburyAL, et al. (2008) CHIP deficiency decreases longevity, with accelerated aging phenotypes accompanied by altered protein quality control. Molecular and cellular biology 28 : 4018–4025.

32. YanJQ, WangJ, LiQT, HwangJR, PattersonC, et al. (2003) AtCHIP, a U-box-containing E3 ubiquitin ligase, plays a critical role in temperature stress tolerance in Arabidopsis. Plant Physiology 132 : 861–869.

33. LeeS, LeeDW, LeeY, MayerU, StierhofYD, et al. (2009) Heat Shock Protein Cognate 70-4 and an E3 Ubiquitin Ligase, CHIP, Mediate Plastid-Destined Precursor Degradation through the Ubiquitin-26S Proteasome System in Arabidopsis. Plant Cell 21 : 3984–4001.

34. ShenGX, YanJQ, PasapulaV, LuoJH, HeCX, et al. (2007) The chloroplast protease subunit ClpP4 is a substrate of the E3 ligase AtCHIP and plays an important role in chloroplast function. Plant Journal 49 : 228–237.

35. LuoJH, ShenGX, YanJQ, HeCX, ZhangH (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant Journal 46 : 649–657.

36. ShenGX, AdamZ, ZhangH (2007) The E3 ligase AtCHIP ubiquitylates FtsH1, a component of the chloroplast FtsH protease, and affects protein degradation in chloroplasts. Plant Journal 52 : 309–321.

37. StankowskiJN, ZeigerSLH, CohenEL, DeFrancoDB, CaiJY, et al. (2011) C-Terminus of Heat Shock Cognate 70 Interacting Protein Increases Following Stroke and Impairs Survival Against Acute Oxidative Stress. Antioxidants & Redox Signaling 14 : 1787–1801.

38. FrugoliJA, ZhongHH, NuccioML, McCourtP, McPeekMA, et al. (1996) Catalase is encoded by a multigene family in Arabidopsis thaliana (L) Heynh. Plant Physiology 112 : 327–336.

39. WangS, KurepaJ, SmalleJA (2009) The Arabidopsis 26S proteasome subunit RPN1a is required for optimal plant growth and stress responses. Plant & cell physiology 50 : 1721–1725.

40. ShanX, WangJ, ChuaL, JiangD, PengW, et al. (2011) The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant physiology 155 : 751–764.

41. LarkindaleJ, KnightMR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant physiology 128 : 682–695.

42. ContentoAL, XiongY, BasshamDC (2005) Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant Journal 42 : 598–608.

43. ThompsonAR, DoellingJH, SuttangkakulA, VierstraRD (2005) Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant physiology 138 : 2097–2110.

44. YoshimotoK, HanaokaH, SatoS, KatoT, TabataS, et al. (2004) Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16 : 2967–2983.

45. SchubertU, AntonLC, GibbsJ, NorburyCC, YewdellJW, et al. (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404 : 770–774.

46. MarquesC, GuoWM, PereiraP, TaylorA, PattersonC, et al. (2006) The triage of damaged proteins: degradation by the ubiquitin-proteasome pathway or repair by molecular chaperones. Faseb Journal 20 : 741-+.

47. MiaoY, ZentgrafU (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant Journal 63 : 179–188.

48. RaabS, DrechselG, ZarepourM, HartungW, KoshibaT, et al. (2009) Identification of a novel E3 ubiquitin ligase that is required for suppression of premature senescence in Arabidopsis. Plant Journal 59 : 39–51.

49. YoshimotoK, JikumaruY, KamiyaY, KusanoM, ConsonniC, et al. (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21 : 2914–2927.

50. LeeS, LeeDW, LeeY, MayerU, StierhofYD, et al. (2009) Heat shock protein cognate 70-4 and an E3 ubiquitin ligase, CHIP, mediate plastid-destined precursor degradation through the ubiquitin-26S proteasome system in Arabidopsis. The Plant cell 21 : 3984–4001.

51. ChenZ, RiciglianoJW, KlessigDF (1993) Purification and characterization of a soluble salicylic acid-binding protein from tobacco. Proc Natl Acad Sci U S A 90 : 9533–9537.

52. ChenZ, SilvaH, KlessigDF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262 : 1883–1886.

53. SalvucciME, OsteryoungKW, Crafts-BrandnerSJ, VierlingE (2001) Exceptional sensitivity of Rubisco activase to thermal denaturation in vitro and in vivo. Plant physiology 127 : 1053–1064.

54. NandiD, TahilianiP, KumarA, ChanduD (2006) The ubiquitin-proteasome system. Journal of biosciences 31 : 137–155.

55. RideoutHJ, Lang-RollinI, StefanisL (2004) Involvement of macroautophagy in the dissolution of neuronal inclusions. International Journal of Biochemistry & Cell Biology 36 : 2551–2562.

56. IwataA, RileyBE, JohnstonJA, KopitoRR (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated Huntingtin. Journal of Biological Chemistry 280 : 40282–40292.

57. PandeyUB, NieZP, BatleviY, McCrayBA, RitsonGP, et al. (2007) HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447 : 859–863.

58. NedelskyNB, ToddPK, TaylorJP (2008) Autophagy and the ubiquitin-proteasome system: Collaborators in neuroprotection. Biochimica Et Biophysica Acta-Molecular Basis of Disease 1782 : 691–699.

59. ShanXY, WangJX, ChuaLL, JiangDA, PengW, et al. (2011) The Role of Arabidopsis Rubisco Activase in Jasmonate-Induced Leaf Senescence. Plant Physiology 155 : 751–764.

60. KurekI, ChangTK, BertainSM, MadrigalA, LiuL, et al. (2007) Enhanced Thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19 : 3230–3241.

61. RizhskyL, Hallak-HerrE, Van BreusegemF, RachmilevitchS, BarrJE, et al. (2002) Double antisense plants lacking ascorbate peroxidase and catalase are less sensitive to oxidative stress than single antisense plants lacking ascorbate peroxidase or catalase. Plant J 32 : 329–342.

62. ZhouJ, WangJ, ChengY, ChiYJ, FanB, et al. (2013) NBR1-Mediated Selective Autophagy Targets Insoluble Ubiquitinated Protein Aggregates in Plant Stress Responses. PLoS genetics 9: e1003196.

63. ChenZ, IyerS, CaplanA, KlessigDF, FanB (1997) Differential accumulation of salicylic acid and salicylic acid-sensitive catalase in different rice tissues. Plant Physiol 114 : 193–201.

64. BradfordMM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 : 248–254.

65. XiaXJ, WangYJ, ZhouYH, TaoY, MaoWH, et al. (2009) Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol 150 : 801–814.