Lipid Biosynthesis Coordinates a Mitochondrial-to-Cytosolic Stress Response

Cell

Volumn 166, Issue 6, 2016, Pages 1539-1552.e16

  Kim, Hyun Eui ^a   Grant, Ana Rodrigues ^b   Simic, Milos S ^a   Kohnz, Rebecca A ^a   Nomura, Daniel K ^a,c   Durieux, Jenni ^a   Riera, Celine E ^a   Sanchez, Melissa ^a   Kapernick, Erik ^a   Wolff, Suzanne ^a   Dillin, Andrew ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACRIDINE ORANGE; ACYL COENZYME A; CARDIOLIPIN; CERAMIDASE; CERAMIDE; CERAMIDE 1 PHOSPHATE; CHAPERONE; CHAPERONIN 60; FATTY ACID SYNTHASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 6; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; HUNTINGTIN; MITOCHONDRIAL PROTEIN; PERHEXILINE; PHOSPHATIDYLGLYCEROL; POLYGLUTAMINE; SMALL HEAT SHOCK PROTEIN; SMALL INTERFERING RNA; SPHINGOMYELIN; SPHINGOSINE; UNCLASSIFIED DRUG; LIPID;

ADULT; ARTICLE; CAENORHABDITIS ELEGANS; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOSOL; EMBRYO; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FIBROBLAST; GENE SILENCING; HEAT SHOCK RESPONSE; HEAT STRESS; HEK293 CELL LINE; HUMAN; HUMAN CELL; LIPID HOMEOSTASIS; LIPID STORAGE; LIPOGENESIS; METABOLIC REGULATION; MICROARRAY ANALYSIS; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN MISFOLDING; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; LIPID METABOLISM; METABOLISM; PHYSIOLOGY;

ANIMALS; CAENORHABDITIS ELEGANS; CELL LINE; CYTOSOL; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK PROTEINS; HEAT-SHOCK RESPONSE; HOMEOSTASIS; HUMANS; LIPID METABOLISM; LIPIDS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MOLECULAR CHAPERONES; PROTEIN FOLDING; UNFOLDED PROTEIN RESPONSE;

EID: 84986257777     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2016.08.027     Document Type: Article

References (55)

1. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., et al., The Gene Ontology Consortium. Gene ontology: tool for the unification of biology. Nat. Genet. 25 (2000), 25–29.
2. Ashrafi, K., Obesity and the regulation of fat metabolism. WormBook, 2007, 1–20.
3. Baird, N.A., Douglas, P.M., Simic, M.S., Grant, A.R., Moresco, J.J., Wolff, S.C., Yates, J.R., Manning, G., Dillin, A., HSF-1–mediated cytoskeletal integrity determines thermotolerance and life span. Science 346 (2014), 360–363.
4. Becker, T., Böttinger, L., Pfanner, N., Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem. Sci. 37 (2012), 85–91.
5. Bellyei, S., Szigeti, A., Boronkai, A., Pozsgai, E., Gomori, E., Melegh, B., Janaky, T., Bognar, Z., Hocsak, E., Sumegi, B., Gallyas, F. Jr., Inhibition of cell death by a novel 16.2 kD heat shock protein predominantly via Hsp90 mediated lipid rafts stabilization and Akt activation pathway. Apoptosis 12 (2007), 97–112.
6. Benjamin, D.I., Cozzo, A., Ji, X., Roberts, L.S., Louie, S.M., Mulvihill, M.M., Luo, K., Nomura, D.K., Ether lipid generating enzyme AGPS alters the balance of structural and signaling lipids to fuel cancer pathogenicity. Proc. Natl. Acad. Sci. USA 110 (2013), 14912–14917.
7. Benjamini, Y., Hochberg, Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57 (1995), 289–300.
8. Bukau, B., Horwich, A.L., The Hsp70 and Hsp60 chaperone machines. Cell 92 (1998), 351–366.
9. Dai, S., Tang, Z., Cao, J., Zhou, W., Li, H., Sampson, S., Dai, C., Suppression of the HSF1-mediated proteotoxic stress response by the metabolic stress sensor AMPK. EMBO J. 34 (2015), 275–293.
10. Daugaard, M., Rohde, M., Jäättelä, M., The heat shock protein 70 family: Highly homologous proteins with overlapping and distinct functions. FEBS Lett. 581 (2007), 3702–3710.
11. Duennwald, M.L., Echeverria, A., Shorter, J., Small heat shock proteins potentiate amyloid dissolution by protein disaggregases from yeast and humans. PLoS Biol., 10, 2012, e1001346.
12. El Bawab, S., Birbes, H., Roddy, P., Szulc, Z.M., Bielawska, A., Hannun, Y.A., Biochemical characterization of the reverse activity of rat brain ceramidase. A CoA-independent and fumonisin B1-insensitive ceramide synthase. J. Biol. Chem. 276 (2001), 16758–16766.
13. Fritz, V., Benfodda, Z., Henriquet, C., Hure, S., Cristol, J.-P., Michel, F., Carbonneau, M.-A., Casas, F., Fajas, L., Metabolic intervention on lipid synthesis converging pathways abrogates prostate cancer growth. Oncogene 32 (2013), 5101–5110.
14. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol., 5, 2004, R80.
15. Haynes, C.M., Ron, D., The mitochondrial UPR - protecting organelle protein homeostasis. J. Cell Sci. 123 (2010), 3849–3855.
16. Ho, H.K., Jia, Y., Coe, K.J., Gao, Q., Doneanu, C.E., Hu, Z., Bammler, T.K., Beyer, R.P., Fausto, N., Bruschi, S.A., Nelson, S.D., Cytosolic heat shock proteins and heme oxygenase-1 are preferentially induced in response to specific and localized intramitochondrial damage by tetrafluoroethylcysteine. Biochem. Pharmacol. 72 (2006), 80–90.
17. Horst, M., Oppliger, W., Rospert, S., Schönfeld, H.-J., Schatz, G., Azem, A., Sequential action of two hsp70 complexes during protein import into mitochondria. EMBO J. 16 (1997), 1842–1849.
18. Hsu, A.-L., Murphy, C.T., Kenyon, C., Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science 300 (2003), 1142–1145.
19. Hu, F., Liu, F., Mitochondrial stress: a bridge between mitochondrial dysfunction and metabolic diseases?. Cell. Signal. 23 (2011), 1528–1533.
20. Hughes, A.L., Gottschling, D.E., An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492 (2012), 261–265.
21. Ichishita, R., Tanaka, K., Sugiura, Y., Sayano, T., Mihara, K., Oka, T., An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J. Biochem. 143 (2008), 449–454.
22. Indiveri, C., Iacobazzi, V., Tonazzi, A., Giangregorio, N., Infantino, V., Convertini, P., Console, L., Palmieri, F., The mitochondrial carnitine/acylcarnitine carrier: function, structure and physiopathology. Mol. Aspects Med. 32 (2011), 223–233.
23. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., Speed, T.P., Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res., 31, 2003, e15.
24. Jovaisaite, V., Mouchiroud, L., Auwerx, J., The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J. Exp. Biol. 217 (2014), 137–143.
25. Kennedy, J.A., Unger, S.A., Horowitz, J.D., Inhibition of carnitine palmitoyltransferase-1 in rat heart and liver by perhexiline and amiodarone. Biochem. Pharmacol. 52 (1996), 273–280.
26. Kim, D., Ouyang, H., Li, G.C., Heat shock protein hsp70 accelerates the recovery of heat-shocked mammalian cells through its modulation of heat shock transcription factor HSF1. Proc. Natl. Acad. Sci. USA 92 (1995), 2126–2130.
27. Kirstein-Miles, J., Morimoto, R.I., Caenorhabditis elegans as a model system to study intercompartmental proteostasis: Interrelation of mitochondrial function, longevity, and neurodegenerative diseases. Dev. Dyn. 239 (2010), 1529–1538.
28. Lindquist, S., Varying patterns of protein synthesis in Drosophila during heat shock: implications for regulation. Dev. Biol. 77 (1980), 463–479.
29. Lindquist, S., Regulation of protein synthesis during heat shock. Nature 293 (1981), 311–314.
30. Liu, Y., Chang, A., Heat shock response relieves ER stress. EMBO J. 27 (2008), 1049–1059.
31. Liu, Y., Samuel, B.S., Breen, P.C., Ruvkun, G., Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature 508 (2014), 406–410.
32. Lu, Y.-W., Claypool, S.M., Disorders of phospholipid metabolism: an emerging class of mitochondrial disease due to defects in nuclear genes. Front. Genet., 6, 2015, 3.
33. Mao, J., DeMayo, F.J., Li, H., Abu-Elheiga, L., Gu, Z., Shaikenov, T.E., Kordari, P., Chirala, S.S., Heird, W.C., Wakil, S.J., Liver-specific deletion of acetyl-CoA carboxylase 1 reduces hepatic triglyceride accumulation without affecting glucose homeostasis. Proc. Natl. Acad. Sci. USA 103 (2006), 8552–8557.
34. Mao, J., Yang, T., Gu, Z., Heird, W.C., Finegold, M.J., Lee, B., Wakil, S.J., aP2-Cre-mediated inactivation of acetyl-CoA carboxylase 1 causes growth retardation and reduced lipid accumulation in adipose tissues. Proc. Natl. Acad. Sci. USA 106 (2009), 17576–17581.
35. Mayer, M.P., Bukau, B., Hsp70 chaperones: cellular functions and molecular mechanism. Cell. Mol. Life Sci. 62 (2005), 670–684.
36. Miller, M.J., Xuong, N.H., Geiduschek, E.P., A response of protein synthesis to temperature shift in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 76 (1979), 5222–5225.
37. Morley, J.F., Brignull, H.R., Weyers, J.J., Morimoto, R.I., The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99 (2002), 10417–10422.
38. Nishizawa, J., Nakai, A., Matsuda, K., Komeda, M., Ban, T., Nagata, K., Reactive oxygen species play an important role in the activation of heat shock factor 1 in ischemic-reperfused heart. Circulation 99 (1999), 934–941.
39. Okino, N., He, X., Gatt, S., Sandhoff, K., Ito, M., Schuchman, E.H., The reverse activity of human acid ceramidase. J. Biol. Chem. 278 (2003), 29948–29953.
40. Reis-Rodrigues, P., Czerwieniec, G., Peters, T.W., Evani, U.S., Alavez, S., Gaman, E.A., Vantipalli, M., Mooney, S.D., Gibson, B.W., Lithgow, G.J., Hughes, R.E., Proteomic analysis of age-dependent changes in protein solubility identifies genes that modulate lifespan. Aging Cell 11 (2012), 120–127.
41. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W., Smyth, G.K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 2015, e47.
42. Ron, D., Walter, P., Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 (2007), 519–529.
43. Sartor, M.A., Leikauf, G.D., Medvedovic, M., LRpath: a logistic regression approach for identifying enriched biological groups in gene expression data. Bioinformatics 25 (2009), 211–217.
44. Senft, D., Ronai, Z.A., UPR, autophagy, and mitochondria crosstalk underlies the ER stress response. Trends Biochem. Sci. 40 (2015), 141–148.
45. Steinkraus, K.A., Smith, E.D., Davis, C., Carr, D., Pendergrass, W.R., Sutphin, G.L., Kennedy, B.K., Kaeberlein, M., Dietary restriction suppresses proteotoxicity and enhances longevity by an hsf-1-dependent mechanism in Caenorhabditis elegans. Aging Cell 7 (2008), 394–404.
46. Supek, F., Bošnjak, M., Škunca, N., Šmuc, T., REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE, 6, 2011, e21800.
47. Tavaria, M., Gabriele, T., Kola, I., Anderson, R.L., A hitchhiker's guide to the human Hsp70 family. Cell Stress Chaperones 1 (1996), 23–28.
48. Thibault, G., Shui, G., Kim, W., McAlister, G.C., Ismail, N., Gygi, S.P., Wenk, M.R., Ng, D.T.W., The membrane stress response buffers lethal effects of lipid disequilibrium by reprogramming the protein homeostasis network. Mol. Cell 48 (2012), 16–27.
49. Vannuvel, K., Renard, P., Raes, M., Arnould, T., Functional and morphological impact of ER stress on mitochondria. J. Cell. Physiol. 228 (2013), 1802–1818.
50. Veatch, J.R., McMurray, M.A., Nelson, Z.W., Gottschling, D.E., Mitochondrial dysfunction leads to nuclear genome instability via an iron-sulfur cluster defect. Cell 137 (2009), 1247–1258.
51. Wang, M., Wey, S., Zhang, Y., Ye, R., Lee, A.S., Role of the unfolded protein response regulator GRP78/BiP in development, cancer, and neurological disorders. Antioxid. Redox Signal. 11 (2009), 2307–2316.
52. Wang, A.M., Miyata, Y., Klinedinst, S., Peng, H.-M., Chua, J.P., Komiyama, T., Li, X., Morishima, Y., Merry, D.E., Pratt, W.B., et al. Activation of Hsp70 reduces neurotoxicity by promoting polyglutamine protein degradation. Nat. Chem. Biol. 9 (2013), 112–118.
53. Westerheide, S.D., Anckar, J., Stevens, S.M. Jr., Sistonen, L., Morimoto, R.I., Stress-inducible regulation of heat shock factor 1 by the deacetylase SIRT1. Science 323 (2009), 1063–1066.
54. Wiedemann, N., Frazier, A.E., Pfanner, N., The protein import machinery of mitochondria. J. Biol. Chem. 279 (2004), 14473–14476.
55. Yang, Y., Cao, J., Shi, Y., Identification and characterization of a gene encoding human LPGAT1, an endoplasmic reticulum-associated lysophosphatidylglycerol acyltransferase. J. Biol. Chem. 279 (2004), 55866–55874.