Phenomic screen identifies a role for the yeast lysine acetyltransferase NuA4 in the control of Bcy1 subcellular localization, glycogen biosynthesis, and mitochondrial morphology
Autoři:
Elizabeth A. Walden aff001; Roger Y. Fong aff001; Trang T. Pham aff001; Hana Knill aff001; Sarah Jane Laframboise aff001; Sylvain Huard aff001; Mary-Ellen Harper aff001; Kristin Baetz aff001
Působiště autorů:
Department of Biochemistry, Microbiology and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Canada
aff001; Ottawa Institute of Systems Biology, Ottawa, Canada
aff002
Vyšlo v časopise:
Phenomic screen identifies a role for the yeast lysine acetyltransferase NuA4 in the control of Bcy1 subcellular localization, glycogen biosynthesis, and mitochondrial morphology. PLoS Genet 16(11): e1009220. doi:10.1371/journal.pgen.1009220
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1009220
Souhrn
Cellular metabolism is tightly regulated by many signaling pathways and processes, including lysine acetylation of proteins. While lysine acetylation of metabolic enzymes can directly influence enzyme activity, there is growing evidence that lysine acetylation can also impact protein localization. As the Saccharomyces cerevisiae lysine acetyltransferase complex NuA4 has been implicated in a variety of metabolic processes, we have explored whether NuA4 controls the localization and/or protein levels of metabolic proteins. We performed a high-throughput microscopy screen of over 360 GFP-tagged metabolic proteins and identified 23 proteins whose localization and/or abundance changed upon deletion of the NuA4 scaffolding subunit, EAF1. Within this, three proteins were required for glycogen synthesis and 14 proteins were associated with the mitochondria. We determined that in eaf1Δ cells the transcription of glycogen biosynthesis genes is upregulated resulting in increased proteins and glycogen production. Further, in the absence of EAF1, mitochondria are highly fused, increasing in volume approximately 3-fold, and are chaotically distributed but remain functional. Both the increased glycogen synthesis and mitochondrial elongation in eaf1Δ cells are dependent on Bcy1, the yeast regulatory subunit of PKA. Surprisingly, in the absence of EAF1, Bcy1 localization changes from being nuclear to cytoplasmic and PKA activity is altered. We found that NuA4-dependent localization of Bcy1 is dependent on a lysine residue at position 313 of Bcy1. However, the glycogen accumulation and mitochondrial elongation phenotypes of eaf1Δ, while dependent on Bcy1, were not fully dependent on Bcy1-K313 acetylation state and subcellular localization of Bcy1. As NuA4 is highly conserved with the human Tip60 complex, our work may inform human disease biology, revealing new avenues to investigate the role of Tip60 in metabolic diseases.
Klíčová slova:
Mitochondria – Acetylation – Biosynthesis – Glucose – Glycogens – Lysine – Protein metabolism – Yeast
Zdroje
1. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine Acetylation Targets Protein Complexes and Co-Regulates Major Cellular Functions. Science (80) [Internet]. 2009;325[5942]:834–40. Available from: doi: 10.1126/science.1175371 19608861
2. Mitchell L, Huard S, Cotrut M, Pourhanifeh-Lemeri R, Steunou A-L, Hamza A, et al. mChIP-KAT-MS, a method to map protein interactions and acetylation sites for lysine acetyltransferases. Proc Natl Acad Sci. 2013;110[17]:E1641–50. doi: 10.1073/pnas.1218515110 23572591
3. Downey M, Johnson JR, Davey NE, Newton BW, Johnson TL, Galaang S, et al. Acetylome profiling reveals overlap in the regulation of diverse processes by sirtuins, Gcn5, and esa1. Mol Cell Proteomics. 2015;14[1]:162–76. doi: 10.1074/mcp.M114.043141 25381059
4. Henriksen P, Wagner SA, Weinert BT, Sharma S, Bačinskaja G, Rehman M, et al. Proteome-wide Analysis of Lysine Acetylation Suggests its Broad Regulatory Scope in Saccharomyces cerevisiae. Mol Cell Proteomics [Internet]. 2012;11[11]:1510–22. Available from: doi: 10.1074/mcp.M112.017251 22865919
5. Kaluarachchi Duffy S, Friesen H, Baryshnikova A, Lambert J-P, Chong YT, Figeys D, et al. Exploring the Yeast Acetylome Using Functional Genomics. Cell. 2012;149[4]:936–48. doi: 10.1016/j.cell.2012.02.064 22579291
6. Singh BN, Zhang G, Hwa YL, Li J, Dowdy SC, Jiang S. Nonhistone protein acetylation as cancer therapy targets. Expert Rev Anticancer Ther. 2010;10[6]:935–54. doi: 10.1586/era.10.62 20553216
7. Iyer A, Fairlie DP, Brown L. Lysine acetylation in obesity, diabetes and metabolic disease. Immunol Cell Biol [Internet]. 2012;90[1]:39–46. Available from: doi: 10.1038/icb.2011.99 22083525
8. Zhang Y, Zhou F, Bai M, Liu Y, Zhang L, Zhu Q, et al. The pivotal role of protein acetylation in linking glucose and fatty acid metabolism to β-cell function. Cell Death Dis [Internet]. 2019;10[2]. Available from: doi: 10.1038/s41419-019-1349-z 30683850
9. Yamada HY. Human Tip60 (NuA4) Complex and Cancer. Color Cancer Biol—From Genes to Tumor. 2012;60:217–40.
10. Di Martile M, Del Bufalo D, Trisciuoglio D. The multifaceted role of lysine acetylation in cancer: Prognostic biomarker and therapeutic target. Oncotarget. 2016;7[34]:55789–810. doi: 10.18632/oncotarget.10048 27322556
11. Doyon Y, Selleck W, Lane WS, Tan S, Côté J. Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol [Internet]. 2004;24[5]:1884–96. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=350560&tool=pmcentrez&rendertype=abstract. doi: 10.1128/mcb.24.5.1884-1896.2004 14966270
12. Sapountzi V, Logan IR, Robson CN. Cellular functions of TIP60. Int J Biochem Cell Biol. 2006;38[9]:1496–509. doi: 10.1016/j.biocel.2006.03.003 16698308
13. Gehrking KM, Andresen JM, Duvick L, Lough J, Zoghbi HY, Orr HT. Partial loss of Tip60 slows mid-stage neurodegeneration in a spinocerebellar ataxia type 1 (SCA1) mouse model. Hum Mol Genet. 2011;20[11]:2204–12. doi: 10.1093/hmg/ddr108 21427130
14. Panikker P, Xu SJ, Zhang H, Sarthi J, Beaver M, Sheth A, et al. Restoring Tip60 HAT/HDAC2 balance in the neurodegenerative brain relieves epigenetic transcriptional repression and reinstates cognition. J Neurosci. 2018;38[19]:4569–83. doi: 10.1523/JNEUROSCI.2840-17.2018 29654189
15. Yang P, Xu C, Reece EA, Chen X, Zhong J, Zhan M, et al. Tip60- and sirtuin 2-regulated MARCKS acetylation and phosphorylation are required for diabetic embryopathy. Nat Commun [Internet]. 2019;10[1]:1–15. Available from: doi: 10.1038/s41467-018-08268-6 30655546
16. Auger A, Galarneau L, Altaf M, Nourani A, Doyon Y, Utley RT, et al. Eaf1 Is the Platform for NuA4 Molecular Assembly That Evolutionarily Links Chromatin Acetylation to ATP-Dependent Exchange of Histone H2A Variants. Mol Cell Biol [Internet]. 2008;28[7]:2257–70. Available from: doi: 10.1128/MCB.01755-07 18212047
17. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, et al. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 1999;18[18]:5108–19. doi: 10.1093/emboj/18.18.5108 10487762
18. Cheng X, Auger A, Altaf M, Drouin S, Paquet E, Utley RT, et al. Eaf1 links the NuA4 histone acetyltransferase complex to Htz1 incorporation and regulation of purine biosynthesis. Eukaryot Cell. 2015;14[6]:535–44. doi: 10.1128/EC.00004-15 25841019
19. Chittuluru J, Chaban Y, Monnet-Saksouk J, Carrozza M, Sapountzi V, Selleck W, et al. Structure and nucleosome interaction of the yeast NuA4 and Piccolo-NuA4 histone acetyltransferase complexes. Nat Struct Mol Bio. 2012;18[11]:1196–203.
20. Mitchell L, Lambert J-P, Gerdes M, Al-Madhoun AS, Skerjanc IS, Figeys D, et al. Functional Dissection of the NuA4 Histone Acetyltransferase Reveals Its Role as a Genetic Hub and that Eaf1 Is Essential for Complex Integrity. Mol Cell Biol [Internet]. 2008;28[7]:2244–56. Available from: doi: 10.1128/MCB.01653-07 18212056
21. Dacquay L, Flint A, Butcher J, Salem D, Kennedy M, Kaern M, et al. NuA4 lysine acetyltransferase complex contributes to phospholipid homeostasis in Saccharomyces cerevisiae. G3 Genes, Genomes, Genet. 2017;7[6]:1799–809. doi: 10.1534/g3.117.041053 28455416
22. Clarke AS, Lowell JE, Jacobson SJ, Pillus L. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol [Internet]. 1999;19[4]:2515–26. Available from: http://www.ncbi.nlm.nih.gov/cgi-bin/Entrez/referer?http://mcb.asm.org/cgi/content/full/19/4/2515. doi: 10.1128/mcb.19.4.2515 10082517
23. Lin YY, Qi Y, Lu JY, Pan X, Yuan DS, Zhao Y, et al. A comprehensive synthetic genetic interaction network governing yeast histone acetylation and deacetylation. Genes Dev. 2008;22[15]:2062–74. doi: 10.1101/gad.1679508 18676811
24. Valdes-Hevia MD, de la Guerra R, Gancedo C. Isolation and characterization of the gene encoding 2,3-oxidosqualene-lanosterol cyclase from Saccharomyces cerevisiae. Proc Natl Acad Sci. 1989;258[2]:313–6.
25. Lin Y, Lu J, Zhang J, Walter W, Dang W, Tao S, et al. Protein Acetylation Microarray Reveals NuA4 Controls Key Metabolic Target Regulating Gluconeogenesis. Cell. 2010;136[6]:1073–84.
26. Lu J, Lin Y, Sheu J, Wu J, Lee F, Chen Y, et al. Acetylation of yeast AMP-Activated Protein Kinase Controls Intrinsic Aging Independently of Caloric Restriction. Cell. 2011;146[6]:969–79. doi: 10.1016/j.cell.2011.07.044 21906795
27. Hedbacker K, Carlson M. SNF1/AMPK pathways in yeast. Front Biosci. 2008;13[7]:2408–20. doi: 10.2741/2854 17981722
28. Ashrafi K, Lin SS, Manchester JK, Gordon JI. Sip2p and its partner Snf1p kinase affect aging in S. cerevisiae. Genes Dev. 2000;14[15]:1872–85. 10921902
29. Stapleton D, Gao G, Michell BJ, Widmerq J, House M, Wittersq LA. Protein Kinase Non-catalytic Subunits Are Homologs of Snfl Protein Kinase. J Biol Chem. 1994;269[47]:29343–6. 7961907
30. Carlson M, Osmond BC, Botstein D. Mutants of yeast defective in sucrose utilization. Genetics. 1981;98[1]:25–40. 7040163
31. Filteau M, Diss G, Torres-Quiroz F, Dubé AK, Schraffl A, Bachmann VA, et al. Systematic identification of signal integration by protein kinase A. Proc Natl Acad Sci [Internet]. 2015;112[14]:4501–6. Available from: http://www.pnas.org/lookup/doi/10.1073/pnas.1409938112. 25831502
32. Chevtzoff C, Vallortigara J, Avéret N, Rigoulet M, Devin A. The yeast cAMP protein kinase Tpk3p is involved in the regulation of mitochondrial enzymatic content during growth. Biochim Biophys Acta—Bioenerg. 2005. doi: 10.1016/j.bbabio.2004.10.001 15620372
33. Chang-Rung C, Blackstone C, Chang CR, Blackstone C. Cyclic AMP-dependent protein kinase phosphorylation of Drp1 regulates its GTPase activity and mitochondrial morphology. J Biol Chem. 2007;282[30]:21583–7. doi: 10.1074/jbc.C700083200 17553808
34. Griffioen G, Anghileri P, Imre E, Baroni MD, Ruis H. Nutritional control of nucleocytoplasmic localization of cAMP-dependent protein kinase catalytic and regulatory subunits in Saccharomyces cerevisiae. J Biol Chem. 2000;275[2]:1449–56. doi: 10.1074/jbc.275.2.1449 10625697
35. Ould Amer Y, Hebert-Chatelain E. Mitochondrial cAMP-PKA signaling: What do we really know? Biochim Biophys Acta—Bioenerg [Internet]. 2018;1859[9]:868–77. Available from: doi: 10.1016/j.bbabio.2018.04.005 29694829
36. Toda T, Cameron S, Sass P, Zoller M, Wigler M. Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase. Cell. 1987;50[2]:277–87. doi: 10.1016/0092-8674(87)90223-6 3036373
37. Toda T, Cameron S, Sass P, Zoller M, Scott JD, McMullen B, et al. Cloning and characterization of BCY1, a locus encoding a regulatory subunit of the cyclic AMP-dependent protein kinase in Saccharomyces cerevisiae. Mol Cell Biol. 1987;7[4]:1371–7. doi: 10.1128/mcb.7.4.1371 3037314
38. Canaves JM, Taylor SS. Classification and phylogenetic analysis of the cAMP-dependent protein kinase regulatory subunit family. J Mol Evol. 2002;54[1]:17–29. doi: 10.1007/s00239-001-0013-1 11734894
39. Griffioen G, Thevelein JM. Molecular mechanisms controlling the localisation of protein kinase A. Curr Genet. 2002;41[4]:199–207. doi: 10.1007/s00294-002-0308-9 12172960
40. Zhang F, Zhang L, Qi Y, Xu H. Mitochondrial cAMP signaling. Cell Mol Life Sci. 2016;73[24]:4577–90. doi: 10.1007/s00018-016-2282-2 27233501
41. Griffioen G, Branduardi P, Ballarini A, Anghileri P, Norbeck J, Baroni MD, et al. Nucleocytoplasmic Distribution of Budding Yeast Protein Kinase A Regulatory Subunit Bcy1 Requires Zds1 and Is Regulated by Yak1-Dependent Phosphorylation of Its Targeting Domain. Mol Cell Biol [Internet]. 2001;21[2]:511–23. Available from: doi: 10.1128/MCB.21.2.511-523.2001 11134339
42. Tudisca V, Recouvreux V, Moreno S, Boy-Marcotte E, Jacquet M, Portela P. Differential localization to cytoplasm, nucleus or P-bodies of yeast PKA subunits under different growth conditions. Eur J Cell Biol [Internet]. 2010;89:339–48. Available from: doi: 10.1016/j.ejcb.2009.08.005 19804918
43. Estruch F, Carlson M. Two homologous zinc finger genes identified by multicopy suppression in a SNF1 protein kinase mutant of Saccharomyces cerevisiae. Mol Cell Biol. 1993;13[7]:3872–81. doi: 10.1128/mcb.13.7.3872 8321194
44. Gorner W, Durchschlag E, Martinez-Pastor MT, Estruch F, Ammerer G, Hamilton B, et al. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 1997;12:586–97.
45. Rajvanshi PK, Arya M, Rajasekharan R. The stress-regulatory transcription factors Msn2 and Msn4 regulate fatty acid oxidation in budding yeast. J Biol Chem. 2017;292[45]:18628–43. doi: 10.1074/jbc.M117.801704 28924051
46. Kuang Z, Pinglay S, Ji H, Boeke JD. Msn2/4 regulate expression of glycolytic enzymes and control transition from quiescence to growth. Elife. 2017;6:1–16.
47. Martínez-Pastor MT, Marchler G, Schüller C, Marchler-Bauer A, Ruis H, Estruch F. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J [Internet]. 1996;15[9]:2227–35. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=450147&tool=pmcentrez&rendertype=abstract.
48. Huang J, Mousley CJ, Dacquay L, Maitra N, Drin G, He C, et al. A Lipid Transfer Protein Signaling Axis Exerts Dual Control of Cell-Cycle and Membrane Trafficking Systems. Dev Cell [Internet]. 2018;44[3]:378–391.e5. Available from: doi: 10.1016/j.devcel.2017.12.026 29396115
49. Li TY, Song L, Sun Y, Li J, Yi C, Lam SM, et al. Tip60-mediated lipin 1 acetylation and ER translocation determine triacylglycerol synthesis rate. Nat Commun [Internet]. 2018;9[1]. Available from: doi: 10.1038/s41467-018-04363-w 29765047
50. Chong YT, Koh JLY, Boone C, Andrews BJ. Yeast Proteome Dynamics from Single Cell Imaging and Automated Analysis Resource Yeast Proteome Dynamics from Single Cell Imaging and Automated Analysis. Cell [Internet]. 2015;161[6]:1413–24. Available from: http://dx.doi.org/10.1016/j.cell.2015.04.051.
51. Rollins M, Huard S, Morettin A, Takuski J, Pham TT, Fullerton MD, et al. Lysine acetyltransferase NuA4 and acetyl-CoA regulate glucose-deprived stress granule formation in Saccharomyces cerevisiae. PLoS Genet. 2017;13[2]:1–27. doi: 10.1371/journal.pgen.1006626 28231279
52. Tong AHY, Boone C. Synthetic Genetic Array Analysis in Saccharomyces cerevisiae. Methods Mol Biol. 313[1]:171–91.
53. Tong AHY, Lesage G, Bader GD, Ding H, Xu H, Xin X, et al. Global mapping of the yeast genetic interaction network. Science (80-). 2004;303:808–14. doi: 10.1126/science.1091317 14764870
54. Huh W-KK, Falvo J V, Gerke LC, Carroll AS, Howson RW, Weissman JS, et al. Global analysis of protein localization in budding yeast. Nature. 2003;425[6959]:686–91. doi: 10.1038/nature02026 14562095
55. Wayne AW, Peter JR, Manuel M, Edurne B-F, Francisco José M, Gustavo E, et al. Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol Rev [Internet]. 2010;34[6]:952–85. Available from: http://dx.doi.org/10.1111/j.1574-6976.2010.00220.x.
56. Roach PJ, Cao Y, Corbeti CA, Farkas I, Fiol CJ, Flotow H, et al. Glycogen metabolism and signal transduction in mammals and yeast. Adv Enzyme Regul. 1991;31:101–20. doi: 10.1016/0065-2571(91)90011-a 1652188
57. Adeva-andany MM, González-lucán M, Donapetry-garcía C, Fernández-fernández C, Ameneiros-rodríguez E. Glycogen metabolism in humans. BBA Clin [Internet]. 2016;5:85–100. Available from: http://dx.doi.org/10.1016/j.bbacli.2016.02.001.
58. Quain DE, Tubb RS. A rapid, simple, adaptable and widely applicable procedure for the determination of glycogen in yeast. J Inst Brew. 1983;89:38–40.
59. Enjalbert B, Parrou JL, Teste MA, Francois J. Combinatorial control by the protein kinases PKA, PHO85 and SNF1 of transcriptional induction of the Saccharomyces cerevisiae GSY2 gene at the diauxic shift. Mol Genet Genomics [Internet]. 2004;271[6]:697–708. Available from: doi: 10.1007/s00438-004-1014-8 15221454
60. Unnikrishnan I, Miller S, Meinke M, LaPorte DC. Multiple positive and negative elements involved in the regulation of expression of GSY1 in Saccharomyces cerevisiae. J Biol Chem. 2003;278[29]:26450–7. doi: 10.1074/jbc.M211808200 12697770
61. Moskvina E, Schüller C, Maurer CTC, Mager WH, Ruis H. A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast. 1998;14[11]:1041–50. doi: 10.1002/(SICI)1097-0061(199808)14:11<1041::AID-YEA296>3.0.CO;2-4 9730283
62. Farkas I, Hardy TA, Goeblt MG, Roach PJ. Two Glycogen Synthase Isoforms in Saccharomyces are coded in distict genes that are differentially controlled. J Biol Chem. 1991;[19]:15602–7.
63. Teste MA, Enjalbert B, Parrou JL, François JM. The Saccharomyces cerevisiae YPR184w gene encodes the glycogen debranching enzyme. FEMS Microbiol Lett. 2000;193[1]:105–10. doi: 10.1111/j.1574-6968.2000.tb09410.x 11094287
64. François J, Parrou JL. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev. 2001;25[1]:125–45. doi: 10.1111/j.1574-6976.2001.tb00574.x 11152943
65. Vowinckel J, Hartl J, Butler R, Ralser M. MitoLoc: A method for the simultaneous quantification of mi tochondrial network morphology and membrane potential in single cells. Mitochondrion [Internet]. 2015;24:77–86. Available from: http://dx.doi.org/10.1016/j.mito.2015.07.001.
66. Giacomello M, Pyakurel A, Glytsou C, Scorrano L. The cell biology of mitochondrial membrane dynamics. Nat Rev Mol Cell Biol [Internet]. 2020;1–21. Available from: http://www.nature.com/articles/s41580-020-0210-7. doi: 10.1038/s41580-020-0210-7 32071438
67. Hanekamp T, Thorsness MK, Rebbapragada I, Fisher EM, Seebart C, Darland MR, et al. Maintenance of mitochondrial morphology is linked to maintenance of the mitochondrial genome in Saccharomyces cerevisiae. Genetics. 2002;162[3]:1147–56. 12454062
68. Bolotin-Fukuhara M. Thirty years of the HAP2/3/4/5 complex. Biochimica et Biophysica Acta—Gene Regulatory Mechanisms. 2017. doi: 10.1016/j.bbagrm.2016.10.011 27989936
69. Chowanadisai W, Bauerly KA, Tchaparian E, Wong A, Cortopassi GA, Rucker RB. Pyrroloquinoline quinone stimulates mitochondrial biogenesis through cAMP response element-binding protein phosphorylation and increased PGC-1α expression. J Biol Chem. 2010;285[1]:142–52. doi: 10.1074/jbc.M109.030130 19861415
70. Vlahakis A, Lopez Muniozguren N, Powers T. Stress-response transcription factors Msn2 and Msn4 couple TORC2-Ypk1 signaling and mitochondrial respiration to ATG8 gene expression and autophagy. Autophagy [Internet]. 2017;13[11]:1804–12. Available from: doi: 10.1080/15548627.2017.1356949 29198169
71. Dai C, Miao D, Li H, Yi C, Huang Y, Li N, et al. Formation of a Snf1-Mec1-Atg1 Module on Mitochondria Governs Energy Deprivation-Induced Autophagy by Regulating Mitochondrial Respiration. Dev Cell. 2017;41[1]:59–71.e4. doi: 10.1016/j.devcel.2017.03.007 28399401
72. Martinez-Ortiz C, Carrillo-Garmendia A, Correa-Romero BF, Canizal-García M, González-Hernández JC, Regalado-Gonzalez C, et al. SNF1 controls the glycolytic flux and mitochondrial respiration. Yeast [Internet]. 2019;36:487–94. Available from: doi: 10.1002/yea.3399 31074533
73. Herzig D, Eser P, Radtke T, Wenger A, Rusterholz T, Wilhelm M, et al. Relation of heart rate and its variability during sleep with age, physical activity, and body composition in young children. Front Physiol. 2017;8:1–12. doi: 10.3389/fphys.2017.00001 28154536
74. Suhm T, Kaimal JM, Dawitz H, Peselj C, Masser AE, Hanzén S, et al. Mitochondrial Translation Efficiency Controls Cytoplasmic Protein Homeostasis. Cell Metab. 2018;27[6]:1309–1322.e6. doi: 10.1016/j.cmet.2018.04.011 29754951
75. Zhou W, Chen KH, Cao W, Zeng J, Liao H, Zhao L, et al. Mutation of the protein kinase A phosphorylation site influences the anti-proliferative activity of mitofusin 2. Atherosclerosis [Internet]. 2010;211[1]:216–23. Available from: doi: 10.1016/j.atherosclerosis.2010.02.012 20303493
76. Pidoux G, Witczak O, Jarnss E, Myrvold L, Urlaub H, Stokka AJ, et al. Optic atrophy 1 is an A-kinase anchoring protein on lipid droplets that mediates adrenergic control of lipolysis. EMBO J. 2011;30[21]:4371–86. doi: 10.1038/emboj.2011.365 21983901
77. Cribbs JT, Strack S. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Rep. 2007;8[10]:939–44. doi: 10.1038/sj.embor.7401062 17721437
78. Schmidt O, Harbauer AB, Rao S, Eyrich B, Zahedi RP, Stojanovski D, et al. Regulation of mitochondrial protein import by cytosolic kinases. Cell. 2011;144[2]:227–39. doi: 10.1016/j.cell.2010.12.015 21215441
79. Gerbeth C, Schmidt O, Rao S, Harbauer AB, Mikropoulou D, Opalinska M, et al. Glucose-induced regulation of protein import receptor tom22 by cytosolic and mitochondria-bound kinases. Cell Metab. 2013;18[4]:578–87. doi: 10.1016/j.cmet.2013.09.006 24093680
80. Lark DS, Reese LR, Ryan TE, Torres MJ, Smith CD, Lin C Te, et al. Protein kinase A governs oxidative phosphorylation kinetics and oxidant emitting potential at complex I. Front Physiol. 2015;6:1–11. doi: 10.3389/fphys.2015.00001 25688210
81. Xie K, Zhu M, Xiang P, Chen X, Kasimumali A, Lu R, et al. Protein Kinase A/CREB Signaling Prevents Adriamycin-Induced Podocyte Apoptosis via Upregulation of Mitochondrial Respiratory Chain Complexes. Mol Cell Biol. 2018;38[1]:1–16. doi: 10.1128/MCB.00181-17 29038164
82. Kamieniarz K, Schneider R. Tools to Tackle Protein Acetylation. Vol. 16, Chemistry and Biology. 2009. p. 1027–9. doi: 10.1016/j.chembiol.2009.10.002 19875076
83. Brust H, Orzechowski S, Fettke J. Starch and Glycogen Analyses: Methods and Techniques. Biomolecules. 2020;10[7]. doi: 10.3390/biom10071020 32660096
84. Bodvard K, Peeters K, Roger F, Romanov N, Igbaria A, Welkenhuysen N, et al. Light-sensing via hydrogen peroxide and a peroxiredoxin. Nat Commun. 2017;8. doi: 10.1038/s41467-017-00021-9 28364116
85. Budhwar R, Lu A, Hirsch JP. Nutrient Control of Yeast PKA Activity Involves Opposing Effects on Phosphorylation of the Bcy1 Regulatory Subunit. Lew DJ, editor. Mol Biol Cell [Internet]. 2010 Nov;21[21]:3749–58. Available from: https://www.molbiolcell.org/doi/10.1091/mbc.e10-05-0388.
86. Li Y, Wang Y. Ras protein/cAMP-dependent protein kinase signaling is negatively regulated by a deubiquitinating enzyme, Ubp3, in yeast. J Biol Chem. 2013;288[16]:11358–65. doi: 10.1074/jbc.M112.449751 23476013
87. Lindstrom KC, Vary JC, Parthun MR, Delrow J, Tsukiyama T. Isw1 Functions in Parallel with the NuA4 and Swr1 Complexes in Stress-Induced Gene Repression. Mol Cell Biol [Internet]. 2006;26[16]:6117–29. Available from: http://mcb.asm.org/cgi/doi/10.1128/MCB.00642-06. 16880522
88. Yu R, Liu T, Ning C, Tan F, Jin SB, Lendahl U, et al. The phosphorylation status of Ser-637 in dynamin-related protein 1 (Drp1) does not determine Drp1 recruitment to mitochondria. J Biol Chem. 2019;294[46]:17262–77. doi: 10.1074/jbc.RA119.008202 31533986
89. Kim YY, Um JH, Yoon JH, Lee DY, Lee YJ, Kim DH, et al. p53 regulates mitochondrial dynamics by inhibiting Drp1 translocation into mitochondria during cellular senescence. FASEB J. 2020;34[2]:2451–64. doi: 10.1096/fj.201901747RR 31908078
90. Akabane S, Uno M, Tani N, Shimazaki S, Ebara N, Kato H, et al. PKA Regulates PINK1 Stability and Parkin Recruitment to Damaged Mitochondria through Phosphorylation of MIC60. Mol Cell [Internet]. 2016;62[3]:371–84. Available from: doi: 10.1016/j.molcel.2016.03.037 27153535
91. Bouchez C, Devin A. Mitochondrial Biogenesis and Mitochondrial Reactive Oxygen Species (ROS): A Complex Relationship Regulated by the cAMP/PKA Signaling Pathway. Cells. 2019;8[4]:287. doi: 10.3390/cells8040287 30934711
92. Fernandez-Marcos PJ, Auwerx J. Regulation of PGC-1α, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr [Internet]. 2011 Apr 1;93[4]:884S–890S. Available from: https://academic.oup.com/ajcn/article/93/4/884S/4597813 doi: 10.3945/ajcn.110.001917 21289221
93. Moujalled D, Weston R, Anderton H, Ninnis R, Goel P, Coley A, et al. Cyclic-AMP-dependent protein kinase A regulates apoptosis by stabilizing the BH3-only protein Bim. EMBO Rep. 2011;12[1]:77–83. doi: 10.1038/embor.2010.190 21151042
94. Lizcano JM, Morrice N, Cohen P. Regulation of BAD by cAMP-dependent protein kinase is mediated via phosphorylation of a novel site, Ser155. Biochem J. 2000;349[2]:547–57. doi: 10.1042/0264-6021:3490547 10880354
95. Harada H, Becknell B, Wilm M, Mann M, Jun-shen Huang L, Taylor SS, et al. Phosphorylation and Inactivation of BAD by Mitochondria-Anchored Protein Kinase A tissues and the maintenance of normal tissue homeosta- sis. In order for cells to avoid a suicidal fate, they must receive cues from their extracellular environment (Raff. Mol Cell. 1999;3:413–22. doi: 10.1016/s1097-2765(00)80469-4 10230394
96. Langeberg LK, Scott JD. A-kinase-anchoring proteins. J Cell Sci. 2005;118[15]:3217–20. doi: 10.1242/jcs.02416 16079273
97. Galello F, Moreno S, Rossi S. Interacting proteins of protein kinase A regulatory subunit in Saccharomyces cerevisiae. J Proteomics [Internet]. 2014;109:261–75. Available from: doi: 10.1016/j.jprot.2014.07.008 25065647
98. Fang X, Lu G, Ha K, Lin H, Du Y, Zuo Q, et al. Acetylation of TIP60 at K104 is essential for metabolic stress-induced apoptosis in cells of hepatocellular cancer. Exp Cell Res. 2017;362[2]:279–86. doi: 10.1016/j.yexcr.2017.11.028 29174981
99. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 1998;14[10]:953–61. doi: 10.1002/(SICI)1097-0061(199807)14:10<953::AID-YEA293>3.0.CO;2-U 9717241
100. Koh JLY, Chong YT, Friesen H, Moses A, Boone C, Andrews BJ, et al. CYCLoPs: A comprehensive database constructed from automated analysis of protein abundance and subcellular localization patterns in Saccharomyces cerevisiae. G3 Genes, Genomes, Genet. 2015;5[6]:1223–32. doi: 10.1534/g3.115.017830 26048563
101. Romanauska A, Köhler A. The Inner Nuclear Membrane Is a Metabolically Active Territory that Generates Nuclear Lipid Droplets. Cell. 2018;174[3]:700–715.e18. doi: 10.1016/j.cell.2018.05.047 29937227
102. Hardy TA, Roach PJ. Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation. J Biol Chem. 1993;268[32]:23799–805. 8226915
103. Mollica JP, Oakhill JS, Lamb GD, Murphy RM. Are genuine changes in protein expression being overlooked? Reassessing Western blotting. Anal Biochem. 2009;386[2]:270–5. doi: 10.1016/j.ab.2008.12.029 19161968
104. Yao W, King DA, Beckwith SL, Gowans GJ, Yen K, Zhou C, et al. The INO80 Complex Requires the Arp5-Ies6 Subcomplex for Chromatin-Remodeling and Metabolic Regulation. Mol Cell Biol. 2016;36[6]:979–91. doi: 10.1128/MCB.00801-15 26755556
105. Dicarlo JE, Norville JE, Mali P, Rios X, Aach J, Church GM. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 2013;41[7]:4336–43. doi: 10.1093/nar/gkt135 23460208
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