Autophagy compensates for defects in mitochondrial dynamics


Autoři: Simon Haeussler aff001;  Fabian Köhler aff001;  Michael Witting aff002;  Madeleine F. Premm aff001;  Stéphane G. Rolland aff001;  Christian Fischer aff001;  Laetitia Chauve aff005;  Olivia Casanueva aff005;  Barbara Conradt aff001
Působiště autorů: Faculty of Biology, Ludwig-Maximilians-University Munich, Munich, Germany aff001;  Research Unit Analytical BioGeoChemistry, Helmholtz Zentrum München, Neuherberg, Germany aff002;  Chair of Analytical Food Chemistry, Technische Universität München, Freising, Germany aff003;  Center for Integrated Protein Science, Ludwig-Maximilians-University Munich, Planegg-Martinsried, Germany aff004;  Epigenetics Programme, The Babraham Institute, Cambridge, United Kingdom aff005;  Department of Cell and Developmental Biology, Division of Biosciences, University College London, London, United Kingdom aff006
Vyšlo v časopise: Autophagy compensates for defects in mitochondrial dynamics. PLoS Genet 16(3): e32767. doi:10.1371/journal.pgen.1008638
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008638

Souhrn

Compromising mitochondrial fusion or fission disrupts cellular homeostasis; however, the underlying mechanism(s) are not fully understood. The loss of C. elegans fzo-1MFN results in mitochondrial fragmentation, decreased mitochondrial membrane potential and the induction of the mitochondrial unfolded protein response (UPRmt). We performed a genome-wide RNAi screen for genes that when knocked-down suppress fzo-1MFN(lf)-induced UPRmt. Of the 299 genes identified, 143 encode negative regulators of autophagy, many of which have previously not been implicated in this cellular quality control mechanism. We present evidence that increased autophagic flux suppresses fzo-1MFN(lf)-induced UPRmt by increasing mitochondrial membrane potential rather than restoring mitochondrial morphology. Furthermore, we demonstrate that increased autophagic flux also suppresses UPRmt induction in response to a block in mitochondrial fission, but not in response to the loss of spg-7AFG3L2, which encodes a mitochondrial metalloprotease. Finally, we found that blocking mitochondrial fusion or fission leads to increased levels of certain types of triacylglycerols and that this is at least partially reverted by the induction of autophagy. We propose that the breakdown of these triacylglycerols through autophagy leads to elevated metabolic activity, thereby increasing mitochondrial membrane potential and restoring mitochondrial and cellular homeostasis.

Klíčová slova:

Autophagic cell death – Fluorescence imaging – Larvae – Lipids – Membrane potential – Mitochondria – Mitochondrial membrane – RNA interference


Zdroje

1. Youle RJ, van der Bliek AM. Mitochondrial fission, fusion, and stress. Science (New York, NY). 2012;337(6098):1062–5.

2. van der Bliek AM, Shen Q, Kawajiri S. Mechanisms of Mitochondrial Fission and Fusion. Cold Spring Harbor Perspectives in Biology. 2013;5(6).

3. Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM. C. elegans Dynamin-Related Protein DRP-1 Controls Severing of the Mitochondrial Outer Membrane. Molecular cell. 1999;4(5):815–26. doi: 10.1016/s1097-2765(00)80391-3 10619028

4. Ingerman E, Perkins EM, Marino M, Mears JA, McCaffery JM, Hinshaw JE, et al. Dnm1 forms spirals that are structurally tailored to fit mitochondria. The Journal of cell biology. 2005;170(7):1021–7. doi: 10.1083/jcb.200506078 16186251

5. 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. The Journal of Biochemistry. 2008;143(4):449–54. doi: 10.1093/jb/mvm245 18174190

6. Kanazawa T, Zappaterra MD, Hasegawa A, Wright AP, Newman-Smith ED, Buttle KF, et al. The C. elegans Opa1 Homologue EAT-3 Is Essential for Resistance to Free Radicals. PLoS genetics. 2008;4(2):e1000022. doi: 10.1371/journal.pgen.1000022 18454199

7. Kim S, Sieburth D. Sphingosine Kinase Activates the Mitochondrial Unfolded Protein Response and Is Targeted to Mitochondria by Stress. Cell reports. 2018;24(11):2932–45.e4. doi: 10.1016/j.celrep.2018.08.037 30208318

8. Zhang Q, Wu X, Chen P, Liu L, Xin N, Tian Y, et al. The Mitochondrial Unfolded Protein Response Is Mediated Cell-Non-autonomously by Retromer-Dependent Wnt Signaling. Cell. 2018;174(4):870–83.e17. doi: 10.1016/j.cell.2018.06.029 30057120

9. Haynes CM, Yang Y, Blais SP, Neubert TA, Ron D. The matrix peptide exporter HAF-1 signals a mitochondrial UPR by activating the transcription factor ZC376.7 in C. elegans. Molecular cell. 2010;37(4):529–40. doi: 10.1016/j.molcel.2010.01.015 20188671

10. Rolland SG, Schneid S, Schwarz M, Rackles E, Fischer C, Haeussler S, et al. Compromised Mitochondrial Protein Import Acts as a Signal for UPRmt. Cell reports. 2019;28(7):1659–69.e5. doi: 10.1016/j.celrep.2019.07.049 31412237

11. Nargund AM, Pellegrino MW, Fiorese CJ, Baker BM, Haynes CM. Mitochondrial import efficiency of ATFS-1 regulates mitochondrial UPR activation. Science (New York, NY). 2012;337(6094):587–90. doi: 10.1126/science.1223560 22700657

12. Benedetti C, Haynes CM, Yang Y, Harding HP, Ron D. Ubiquitin-like protein 5 positively regulates chaperone gene expression in the mitochondrial unfolded protein response. Genetics. 2006;174(1):229–39. doi: 10.1534/genetics.106.061580 16816413

13. Haynes CM, Petrova K, Benedetti C, Yang Y, Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Developmental cell. 2007;13(4):467–80. doi: 10.1016/j.devcel.2007.07.016 17925224

14. Yoneda T, Benedetti C, Urano F, Clark SG, Harding HP, Ron D. Compartment-specific perturbation of protein handling activates genes encoding mitochondrial chaperones. Journal of cell science. 2004;117(Pt 18):4055–66.

15. Levine B, Klionsky DJ. Development by Self-Digestion. Developmental cell. 2004;6(4):463–77. doi: 10.1016/s1534-5807(04)00099-1 15068787

16. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21(22):2861–73. doi: 10.1101/gad.1599207 18006683

17. Feng Y, He D, Yao Z, Klionsky DJ. The machinery of macroautophagy. Cell Res. 2014;24(1):24–41. doi: 10.1038/cr.2013.168 24366339

18. Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nature reviews Molecular cell biology. 2009;10(7):458–67. doi: 10.1038/nrm2708 19491929

19. Long X, Spycher C, Han ZS, Rose AM, Müller F, Avruch J. TOR Deficiency in C. elegans Causes Developmental Arrest and Intestinal Atrophy by Inhibition of mRNA Translation. Current Biology. 2002;12(17):1448–61. doi: 10.1016/s0960-9822(02)01091-6 12225660

20. Hansen M, Chandra A, Mitic LL, Onken B, Driscoll M, Kenyon C. A role for autophagy in the extension of lifespan by dietary restriction in C. elegans. PLoS genetics. 2008;4(2):e24. doi: 10.1371/journal.pgen.0040024 18282106

21. Jia K, Chen D, Riddle DL. The TOR pathway interacts with the insulin signaling pathway to regulate C. elegans larval development, metabolism and life span. Development. 2004;131(16):3897–906. doi: 10.1242/dev.01255 15253933

22. Kuroyanagi H, Yan J, Seki N, Yamanouchi Y, Suzuki Y, Takano T, et al. Human ULK1, a novel serine/threonine kinase related to UNC-51 kinase of Caenorhabditis elegans: cDNA cloning, expression, and chromosomal assignment. Genomics. 1998;51(1):76–85. doi: 10.1006/geno.1998.5340 9693035

23. Ogura K, Wicky C, Magnenat L, Tobler H, Mori I, Müller F, et al. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/threonine kinase. Genes & Development. 1994;8(20):2389–400.

24. Wullschleger S, Loewith R, Hall MN. TOR signaling in growth and metabolism. Cell. 2006;124(3):471–84. doi: 10.1016/j.cell.2006.01.016 16469695

25. Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Letters. 1993;333(1–2):169–74. doi: 10.1016/0014-5793(93)80398-e 8224160

26. Sato M, Sato K. Degradation of Paternal Mitochondria by Fertilization-Triggered Autophagy in C. elegans Embryos. Science (New York, NY). 2011;334(6059):1141–4.

27. Christ L, Raiborg C, Wenzel EM, Campsteijn C, Stenmark H. Cellular Functions and Molecular Mechanisms of the ESCRT Membrane-Scission Machinery. Trends in biochemical sciences. 2017;42(1):42–56. doi: 10.1016/j.tibs.2016.08.016 27669649

28. Katzmann DJ, Babst M, Emr SD. Ubiquitin-Dependent Sorting into the Multivesicular Body Pathway Requires the Function of a Conserved Endosomal Protein Sorting Complex, ESCRT-I. Cell. 2001;106(2):145–55. doi: 10.1016/s0092-8674(01)00434-2 11511343

29. Raiborg C, Bache KG, Gillooly DJ, Madshus IH, Stang E, Stenmark H. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nature cell biology. 2002;4(5):394–8. doi: 10.1038/ncb791 11988743

30. Sachse M, Urbe S, Oorschot V, Strous GJ, Klumperman J. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell. 2002;13(4):1313–28. doi: 10.1091/mbc.01-10-0525 11950941

31. Amit I, Yakir L, Katz M, Zwang Y, Marmor MD, Citri A, et al. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 2004;18(14):1737–52. doi: 10.1101/gad.294904 15256501

32. Carlton JG, Martin-Serrano J. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery. Science (New York, NY). 2007;316(5833):1908–12.

33. Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerod L, Fisher EM, et al. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. The Journal of cell biology. 2007;179(3):485–500. doi: 10.1083/jcb.200702115 17984323

34. Lee JA, Beigneux A, Ahmad ST, Young SG, Gao FB. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr Biol. 2007;17(18):1561–7. doi: 10.1016/j.cub.2007.07.029 17683935

35. Rusten TE, Vaccari T, Lindmo K, Rodahl LM, Nezis IP, Sem-Jacobsen C, et al. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr Biol. 2007;17(20):1817–25. doi: 10.1016/j.cub.2007.09.032 17935992

36. Tamai K, Tanaka N, Nara A, Yamamoto A, Nakagawa I, Yoshimori T, et al. Role of Hrs in maturation of autophagosomes in mammalian cells. Biochem Biophys Res Commun. 2007;360(4):721–7. doi: 10.1016/j.bbrc.2007.06.105 17624298

37. Takahashi Y, He H, Tang Z, Hattori T, Liu Y, Young MM, et al. An autophagy assay reveals the ESCRT-III component CHMP2A as a regulator of phagophore closure. Nature communications. 2018;9(1):2855. doi: 10.1038/s41467-018-05254-w 30030437

38. Zhou F, Wu Z, Zhao M, Murtazina R, Cai J, Zhang A, et al. Rab5-dependent autophagosome closure by ESCRT. The Journal of cell biology. 2019;218(6):1908–27. doi: 10.1083/jcb.201811173 31010855

39. Djeddi A, Michelet X, Culetto E, Alberti A, Barois N, Legouis R. Induction of autophagy in ESCRT mutants is an adaptive response for cell survival in C. elegans. Journal of cell science. 2012;125(3):685–94.

40. Guo B, Huang X, Zhang P, Qi L, Liang Q, Zhang X, et al. Genome‐wide screen identifies signaling pathways that regulate autophagy during Caenorhabditis elegans development. EMBO reports. 2014;15(6):705–13. doi: 10.1002/embr.201338310 24764321

41. Zubovych IO, Straud S, Roth MG, Newmeyer DD. Mitochondrial Dysfunction Confers Resistance to Multiple Drugs in Caenorhabditis elegans. Molecular Biology of the Cell. 2010;21(6):956–69. doi: 10.1091/mbc.E09-08-0673 20089839

42. Köhler F, Müller-Rischart AK, Conradt B, Rolland SG. The loss of LRPPRC function induces the mitochondrial unfolded protein response. Aging. 2015;7(9):701–12. doi: 10.18632/aging.100812 26412102

43. Liu Y, Samuel BS, Breen PC, Ruvkun G. Caenorhabditis elegans pathways that surveil and defend mitochondria. Nature. 2014;508(7496):406–10. doi: 10.1038/nature13204 24695221

44. Runkel ED, Liu S, Baumeister R, Schulze E. Surveillance-activated defenses block the ROS-induced mitochondrial unfolded protein response. PLoS genetics. 2013;9(3):e1003346. doi: 10.1371/journal.pgen.1003346 23516373

45. Kamath RS, Ahringer J. Genome-wide RNAi screening in Caenorhabditis elegans. Methods (San Diego, Calif). 2003;30(4):313–21.

46. Rolland SG, Motori E, Memar N, Hench J, Frank S, Winklhofer KF, et al. Impaired complex IV activity in response to loss of LRPPRC function can be compensated by mitochondrial hyperfusion. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(32):E2967–76. doi: 10.1073/pnas.1303872110 23878239

47. Loew LM, Tuft RA, Carrington W, Fay FS. Imaging in five dimensions: time-dependent membrane potentials in individual mitochondria. Biophysical Journal. 1993;65(6):2396–407. doi: 10.1016/S0006-3495(93)81318-3 8312478

48. Chen Y, Scarcelli V, Legouis R. Approaches for Studying Autophagy in Caenorhabditis elegans. Cells. 2017;6(3).

49. Jenzer C, Simionato E, Legouis R. Tools and methods to analyze autophagy in C. elegans. Methods (San Diego, Calif). 2015;75:162–71.

50. Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12(1):1–222. doi: 10.1080/15548627.2015.1100356 26799652

51. Tian Y, Li Z, Hu W, Ren H, Tian E, Zhao Y, et al. C. elegans Screen Identifies Autophagy Genes Specific to Multicellular Organisms. Cell. 2010;141(6):1042–55. doi: 10.1016/j.cell.2010.04.034 20550938

52. Zhang H, Chang JT, Guo B, Hansen M, Jia K, Kovacs AL, et al. Guidelines for monitoring autophagy in Caenorhabditis elegans. Autophagy. 2015;11(1):9–27. doi: 10.1080/15548627.2014.1003478 25569839

53. Chapin HC, Okada M, Merz AJ, Miller DL. Tissue-specific autophagy responses to aging and stress in C. elegans. Aging (Albany NY). 2015;7(6):419–34.

54. Mizushima N, Yoshimori T, Levine B. Methods in Mammalian Autophagy Research. Cell. 2010;140(3):313–26. doi: 10.1016/j.cell.2010.01.028 20144757

55. Homma K, Suzuki K, Sugawara H. The Autophagy Database: an all-inclusive information resource on autophagy that provides nourishment for research. Nucleic Acids Research. 2011;39(suppl_1):D986–D90.

56. Lipinski MM, Hoffman G, Ng A, Zhou W, Py BF, Hsu E, et al. A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Developmental cell. 2010;18(6):1041–52. doi: 10.1016/j.devcel.2010.05.005 20627085

57. Strohecker AM, Joshi S, Possemato R, Abraham RT, Sabatini DM, White E. Identification of 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase as a novel autophagy regulator by high content shRNA screening. Oncogene. 2015;34(45):5662–76. doi: 10.1038/onc.2015.23 25772235

58. Dayalan Naidu S, Dikovskaya D, Gaurilcikaite E, Knatko EV, Healy ZR, Mohan H, et al. Transcription factors NRF2 and HSF1 have opposing functions in autophagy. Sci Rep. 2017;7(1):11023. doi: 10.1038/s41598-017-11262-5 28887499

59. Demishtein A, Fraiberg M, Berko D, Tirosh B, Elazar Z, Navon A. SQSTM1/p62-mediated autophagy compensates for loss of proteasome polyubiquitin recruiting capacity. Autophagy. 2017;13(10):1697–708. doi: 10.1080/15548627.2017.1356549 28792301

60. Dokladny K, Zuhl MN, Mandell M, Bhattacharya D, Schneider S, Deretic V, et al. Regulatory coordination between two major intracellular homeostatic systems: heat shock response and autophagy. The Journal of biological chemistry. 2013;288(21):14959–72. doi: 10.1074/jbc.M113.462408 23576438

61. Hu G, McQuiston T, Bernard A, Park YD, Qiu J, Vural A, et al. A conserved mechanism of TOR-dependent RCK-mediated mRNA degradation regulates autophagy. Nature cell biology. 2015;17(7):930–42. doi: 10.1038/ncb3189 26098573

62. Hwang DW, So KS, Kim SC, Park KM, Lee YJ, Kim SW, et al. Autophagy Induced by CX-4945, a Casein Kinase 2 Inhibitor, Enhances Apoptosis in Pancreatic Cancer Cell Lines. Pancreas. 2017;46(4):575–81. doi: 10.1097/MPA.0000000000000780 28196025

63. Keith SA, Maddux SK, Zhong Y, Chinchankar MN, Ferguson AA, Ghazi A, et al. Graded Proteasome Dysfunction in Caenorhabditis elegans Activates an Adaptive Response Involving the Conserved SKN-1 and ELT-2 Transcription Factors and the Autophagy-Lysosome Pathway. PLoS genetics. 2016;12(2):e1005823. doi: 10.1371/journal.pgen.1005823 26828939

64. Kumsta C, Chang JT, Schmalz J, Hansen M. Hormetic heat stress and HSF-1 induce autophagy to improve survival and proteostasis in C. elegans. Nature communications. 2017;8:14337. doi: 10.1038/ncomms14337 28198373

65. Lee SW, Song YS, Lee SY, Yoon YG, Lee SH, Park BS, et al. Downregulation of protein kinase CK2 activity facilitates tumor necrosis factor-alpha-mediated chondrocyte death through apoptosis and autophagy. PloS one. 2011;6(4):e19163. doi: 10.1371/journal.pone.0019163 21559479

66. Meléndez A, Tallóczy Z, Seaman M, Eskelinen E-L, Hall DH, Levine B. Autophagy Genes Are Essential for Dauer Development and Life-Span Extension in C. elegans. Science (New York, NY). 2003;301(5638):1387–91.

67. Menzies FM, Garcia-Arencibia M, Imarisio S, O'Sullivan NC, Ricketts T, Kent BA, et al. Calpain inhibition mediates autophagy-dependent protection against polyglutamine toxicity. Cell death and differentiation. 2015;22(3):433–44. doi: 10.1038/cdd.2014.151 25257175

68. Murphy CT, McCarroll SA, Bargmann CI, Fraser A, Kamath RS, Ahringer J, et al. Genes that act downstream of DAF-16 to influence the lifespan of Caenorhabditis elegans. Nature. 2003;424:277. doi: 10.1038/nature01789 12845331

69. Pierce SB, Costa M, Wisotzkey R, Devadhar S, Homburger SA, Buchman AR, et al. Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family. Genes & Development. 2001;15(6):672–86.

70. Putker M, Madl T, Vos Harmjan R, de Ruiter H, Visscher M, van den Berg Maaike CW, et al. Redox-Dependent Control of FOXO/DAF-16 by Transportin-1. Molecular cell. 2013;49(4):730–42. doi: 10.1016/j.molcel.2012.12.014 23333309

71. Sheaffer KL, Updike DL, Mango SE. The Target of Rapamycin pathway antagonizes pha-4/FoxA to control development and aging. Curr Biol. 2008;18(18):1355–64. doi: 10.1016/j.cub.2008.07.097 18804378

72. Tang L, Fares H, Zhao X, Du W, Liu BF. Different endocytic functions of AGEF-1 in C. elegans coelomocytes. Biochimica et biophysica acta. 2012;1820(7):829–40. doi: 10.1016/j.bbagen.2012.03.004 22446376

73. Yang D, Li L, Liu H, Wu L, Luo Z, Li H, et al. Induction of autophagy and senescence by knockdown of ROC1 E3 ubiquitin ligase to suppress the growth of liver cancer cells. Cell death and differentiation. 2013;20(2):235–47. doi: 10.1038/cdd.2012.113 22935614

74. Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, et al. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nature cell biology. 2010;12:665. doi: 10.1038/ncb2069 20543840

75. Nawa M, Kage-Nakadai E, Aiso S, Okamoto K, Mitani S, Matsuoka M. Reduced expression of BTBD10, an Akt activator, leads to motor neuron death. Cell Death & Differentiation. 2012;19(8):1398–407.

76. Nawa M, Matsuoka M. The Method of the Body Bending Assay Using Caenorhabditis elegans. Bio Protoc. 2012;2(17):e253.

77. Johnson D, Nehrke K. Mitochondrial Fragmentation Leads to Intracellular Acidification in Caenorhabditis elegans and Mammalian Cells. Molecular Biology of the Cell. 2010;21(13):2191–201. doi: 10.1091/mbc.E09-10-0874 20444981

78. Lim Y, Rubio-Peña K, Sobraske PJ, Molina PA, Brookes PS, Galy V, et al. Fndc-1 contributes to paternal mitochondria elimination in C. elegans. Developmental Biology. 2019;454(1):15–20. doi: 10.1016/j.ydbio.2019.06.016 31233739

79. Palikaras K, Lionaki E, Tavernarakis N. Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans. Nature. 2015.

80. Rauthan M, Ranji P, Aguilera Pradenas N, Pitot C, Pilon M. The mitochondrial unfolded protein response activator ATFS-1 protects cells from inhibition of the mevalonate pathway. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(15):5981–6. doi: 10.1073/pnas.1218778110 23530189

81. Bennett CF, Vander Wende H, Simko M, Klum S, Barfield S, Choi H, et al. Activation of the mitochondrial unfolded protein response does not predict longevity in Caenorhabditis elegans. Nature communications. 2014;5:3483. doi: 10.1038/ncomms4483 24662282

82. Buis A, Bellemin S, Goudeau J, Monnier L, Loiseau N, Guillou H, et al. Coelomocytes Regulate Starvation-Induced Fat Catabolism and Lifespan Extension through the Lipase LIPL-5 in Caenorhabditis elegans. Cell reports. 2019;28(4):1041–9.e4. doi: 10.1016/j.celrep.2019.06.064 31340142

83. Harvald EB, Sprenger RR, Dall KB, Ejsing CS, Nielsen R, Mandrup S, et al. Multi-omics Analyses of Starvation Responses Reveal a Central Role for Lipoprotein Metabolism in Acute Starvation Survival in C.elegans. Cell Systems. 2017;5(1):38–52.e4. doi: 10.1016/j.cels.2017.06.004 28734827

84. Vrablik TL, Petyuk VA, Larson EM, Smith RD, Watts JL. Lipidomic and proteomic analysis of Caenorhabditis elegans lipid droplets and identification of ACS-4 as a lipid droplet-associated protein. Biochimica et Biophysica Acta (BBA)—Molecular and Cell Biology of Lipids. 2015;1851(10):1337–45.

85. Benador IY, Veliova M, Mahdaviani K, Petcherski A, Wikstrom JD, Assali EA, et al. Mitochondria Bound to Lipid Droplets Have Unique Bioenergetics, Composition, and Dynamics that Support Lipid Droplet Expansion. Cell metabolism. 2018;27(4):869–85.e6. doi: 10.1016/j.cmet.2018.03.003 29617645

86. Rambold Angelika S, Cohen S, Lippincott-Schwartz J. Fatty Acid Trafficking in Starved Cells: Regulation by Lipid Droplet Lipolysis, Autophagy, and Mitochondrial Fusion Dynamics. Developmental cell. 2015;32(6):678–92. doi: 10.1016/j.devcel.2015.01.029 25752962

87. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, et al. Autophagy regulates lipid metabolism. Nature. 2009;458:1131. doi: 10.1038/nature07976 19339967

88. Saito T, Kuma A, Sugiura Y, Ichimura Y, Obata M, Kitamura H, et al. Autophagy regulates lipid metabolism through selective turnover of NCoR1. Nature communications. 2019;10(1):1567. doi: 10.1038/s41467-019-08829-3 30952864

89. Pellegrino MW, Nargund AM, Haynes CM. Signaling the mitochondrial unfolded protein response. Biochimica et Biophysica Acta (BBA)—Molecular Cell Research. 2013;1833(2):410–6.

90. Honjoh S, Yamamoto T, Uno M, Nishida E. Signalling through RHEB-1 mediates intermittent fasting-induced longevity in C. elegans. Nature. 2008;457:726. doi: 10.1038/nature07583 19079239

91. Cooper JF, Machiela E, Dues DJ, Spielbauer KK, Senchuk MM, Van Raamsdonk JM. Activation of the mitochondrial unfolded protein response promotes longevity and dopamine neuron survival in Parkinson’s disease models. Scientific Reports. 2017;7(1):16441. doi: 10.1038/s41598-017-16637-2 29180793

92. Kim KH, Lee M-S. Autophagy—a key player in cellular and body metabolism. Nature Reviews Endocrinology. 2014;10:322. doi: 10.1038/nrendo.2014.35 24663220

93. Rabinowitz JD, White E. Autophagy and Metabolism. Science (New York, NY). 2010;330(6009):1344–8.

94. Lin Y-F, Haynes CM. Metabolism and the UPRmt. Molecular cell. 2016;61(5):677–82. doi: 10.1016/j.molcel.2016.02.004 26942672

95. Mouysset J, Kähler C, Hoppe T. A conserved role of Caenorhabditis elegans CDC-48 in ER-associated protein degradation. Journal of Structural Biology. 2006;156(1):41–9. doi: 10.1016/j.jsb.2006.02.015 16647269

96. Takahashi M, Iwasaki H, Inoue H, Takahashi K. Reverse Genetic Analysis of the Caenorhabditis elegans 26S Proteasome Subunits by RNA Interference. Biological Chemistry2002. p. 1263. doi: 10.1515/BC.2002.140 12437114

97. Baker BM, Nargund AM, Sun T, Haynes CM. Protective coupling of mitochondrial function and protein synthesis via the eIF2alpha kinase GCN-2. PLoS genetics. 2012;8(6):e1002760. doi: 10.1371/journal.pgen.1002760 22719267

98. Brenner S. The Genetics of Caenorhabditis Elegans. Genetics. 1974;77(1):71–94. 4366476

99. Simmer F, Tijsterman M, Parrish S, Koushika SP, Nonet ML, Fire A, et al. Loss of the Putative RNA-Directed RNA Polymerase RRF-3 Makes C. elegans Hypersensitive to RNAi. Current Biology. 2002;12(15):1317–9. doi: 10.1016/s0960-9822(02)01041-2 12176360

100. Springer W, Hoppe T, Schmidt E, Baumeister R. A Caenorhabditis elegans Parkin mutant with altered solubility couples α-synuclein aggregation to proteotoxic stress. Human Molecular Genetics. 2005;14(22):3407–23. doi: 10.1093/hmg/ddi371 16204351

101. Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, Goncharov A, et al. Distinct Innate Immune Responses to Infection and Wounding in the C. elegans Epidermis. Current Biology. 2008;18(7):481–9. doi: 10.1016/j.cub.2008.02.079 18394898

102. Kang C, You Y-j, Avery L. Dual roles of autophagy in the survival of Caenorhabditis elegans during starvation. Genes & Development. 2007;21(17):2161–71.

103. Urano F, Calfon M, Yoneda T, Yun C, Kiraly M, Clark SG, et al. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. The Journal of cell biology. 2002;158(4):639–46. doi: 10.1083/jcb.200203086 12186849

104. Mariol M-C, Walter L, Bellemin S, Gieseler K. A rapid protocol for integrating extrachromosomal arrays with high transmission rate into the C. elegans genome. Journal of visualized experiments: JoVE. 2013(82):e50773–e. doi: 10.3791/50773 24379027

105. Frøkjær-Jensen C, Wayne Davis M, Hopkins CE, Newman BJ, Thummel JM, Olesen S-P, et al. Single-copy insertion of transgenes in Caenorhabditis elegans. Nature Genetics. 2008;40:1375. doi: 10.1038/ng.248 18953339

106. Frøkjær-Jensen C, Davis MW, Sarov M, Taylor J, Flibotte S, LaBella M, et al. Random and targeted transgene insertion in Caenorhabditis elegans using a modified Mos1 transposon. Nature Methods. 2014;11:529. doi: 10.1038/nmeth.2889 24820376

107. Gibson DG, Young L, Chuang R-Y, Venter JC, Hutchison Iii CA, Smith HO. Enzymatic assembly of DNA molecules up to several hundred kilobases. Nature Methods. 2009;6:343. doi: 10.1038/nmeth.1318 19363495

108. Frøkjær-Jensen C, Davis MW, Ailion M, Jorgensen EM. Improved Mos1-mediated transgenesis in C. elegans. Nature Methods. 2012;9:117. doi: 10.1038/nmeth.1865 22290181

109. Jagasia R, Grote P, Westermann B, Conradt B. DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death in C. elegans. Nature. 2005;433(7027):754–60. doi: 10.1038/nature03316 15716954

110. Sternberg SR. Biomedical Image Processing. Computer. 1983;16(1):22–34.

111. Sato Y, Nakajima S, Shiraga N, Atsumi H, Yoshida S, Koller T, et al. Three-dimensional multi-scale line filter for segmentation and visualization of curvilinear structures in medical images. Medical Image Analysis. 1998;2(2):143–68. doi: 10.1016/s1361-8415(98)80009-1 10646760

112. Xiao R, Chun L, Ronan Elizabeth A, Friedman David I, Liu J, Xu XZS. RNAi Interrogation of Dietary Modulation of Development, Metabolism, Behavior, and Aging in C. elegans. Cell reports. 2015;11(7):1123–33. doi: 10.1016/j.celrep.2015.04.024 25959815

113. Löfgren L, Forsberg G-B, Ståhlman M. The BUME method: a new rapid and simple chloroform-free method for total lipid extraction of animal tissue. Scientific Reports. 2016;6(1):27688.

114. Witting M, Maier TV, Garvis S, Schmitt-Kopplin P. Optimizing a ultrahigh pressure liquid chromatography-time of flight-mass spectrometry approach using a novel sub-2μm core–shell particle for in depth lipidomic profiling of Caenorhabditis elegans. Journal of Chromatography A. 2014;1359:91–9. doi: 10.1016/j.chroma.2014.07.021 25074420

115. O’Donnell VB, Dennis EA, Wakelam MJO, Subramaniam S. LIPID MAPS: Serving the next generation of lipid researchers with tools, resources, data, and training. Science Signaling. 2019;12(563):eaaw2964. doi: 10.1126/scisignal.aaw2964 30622195

116. Kind T, Liu K-H, Lee DY, DeFelice B, Meissen JK, Fiehn O. LipidBlast in silico tandem mass spectrometry database for lipid identification. Nature Methods. 2013;10(8):755–8. doi: 10.1038/nmeth.2551 23817071

117. Mok DZL, Sternberg PW, Inoue T. Morphologically defined sub-stages of C. elegans vulval development in the fourth larval stage. BMC developmental biology. 2015;15:26–. doi: 10.1186/s12861-015-0076-7 26066484

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