Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation

eLife

Volumn 2014, Issue 3, 2014, Pages

  Petrovska, Ivana ^a   Nüske, Elisabeth ^a   Munder, Matthias C ^a   Kulasegaran, Gayathrie ^a   Malinovska, Liliana ^a   Kroschwald, Sonja ^a   Richter, Doris ^a   Fahmy, Karim ^b   Gibson, Kimberley ^a   Verbavatz, Jean Marc ^a   Alberti, Simon ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^b INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE AMMONIA LIGASE; PROTEIN; PROTEIN GLN1; UNCLASSIFIED DRUG;

ACIDIFICATION; AGAR GEL ELECTROPHORESIS; ARTICLE; CELL FUNCTION; CELL METABOLISM; CELL SURVIVAL; CELLULAR STARVATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCULAR DICHROISM; CYTOSOL; ELECTRON MICROSCOPY; ENZYME ACTIVITY; FLUORESCENCE MICROSCOPY; LIGHT SCATTERING; MACROMOLECULAR CROWDING; MUTATION; NONHUMAN; PH; POINT MUTATION; PROTEIN PURIFICATION; STARVATION; THIN FILAMENT; TRANSMISSION ELECTRON MICROSCOPY; YEAST; YEAST CELL;

EID: 84899657388     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02409     Document Type: Article

References (54)

1. Adams, S.R., Campbell, R.E., Gross, L.A., Martin, B.R., Walkup, G.K., Yao, Y., Llopis, J., and Tsien, R.Y. (2002). New biarsenical ligands and tetracysteine motifs for protein labeling in vitro and in vivo: synthesis and biological applications. Journal of the American Chemical Society 124, 6063-6076.
2. Alberti, S., Gitler, A.D., and Lindquist, S. (2007). A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24, 913-919.
3. Alberti, S., Halfmann, R., King, O., Kapila, A., and Lindquist, S. (2009). A systematic survey identifies prions and illuminates sequence features of prionogenic proteins. Cell 137, 146-158.
4. Alberti, S., Halfmann, R., and Lindquist, S. (2010). Biochemical, cell biological, and genetic assays to analyze amyloid and prion aggregation in yeast. Methods in enzymology 470, 709-734.
5. Andresen, M., Schmitz-Salue, R., and Jakobs, S. (2004). Short tetracysteine tags to beta-tubulin demonstrate the significance of small labels for live cell imaging. Molecular biology of the cell 15, 5616-5622.
6. Barnhart, M.C., and Mcmahon, B.R. (1988). Depression of Aerobic Metabolism and Intracellular Ph by Hypercapnia in Land Snails, Otala-Lactea. J Exp Biol 138, 289-299.
7. Barry, R.M., and Gitai, Z. (2011). Self-assembling enzymes and the origins of the cytoskeleton. Current opinion in microbiology 14, 704-711.
8. Bernstein, B.W., and Bamburg, J.R. (2010). ADF/Cofilin: a functional node in cell biology. Trends in Cell Biology 20, 187-195.
9. Bernstein, B.W., Chen, H., Boyle, J.A., and Bamburg, J.R. (2006). Formation of actin-ADF/cofilin rods transiently retards decline of mitochondrial potential and ATP in stressed neurons. Am J Physiol-Cell Ph 291, C828-C839.
10. Brangwynne, C.P. (2011). Soft active aggregates: mechanics, dynamics and self-assembly of liquid-like intracellular protein bodies. Soft Matter 7, 3052-3059.
11. Brangwynne, C.P., Eckmann, C.R., Courson, D.S., Rybarska, A., Hoege, C., Gharakhani, J., Julicher, F., and Hyman, A.A. (2009). Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science New York, NY 324, 1729-1732.
12. Brangwynne, C.P., Mitchison, T.J., and Hyman, A.A. (2011). Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proceedings of the National Academy of Sciences of the United States of America 108, 4334-4339.
13. Brett, C.L., Tukaye, D.N., Mukherjee, S., and Rao, R. (2005). The yeast endosomal Na+K+/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Molecular biology of the cell 16, 1396-1405.
14. Busa, W.B., and Crowe, J.H. (1983). Intracellular pH Regulates Transitions Between Dormancy and Development of Brine Shrimp (Artemia salina) Embryos. Science New York, NY 221, 366-368.
15. Busa, W.B., and Nuccitelli, R. (1984). Metabolic regulation via intracellular pH. Am J Physiol 246, R409-438.
16. Chapman, M.R., Robinson, L.S., Pinkner, J.S., Roth, R., Heuser, J., Hammar, M., Normark, S., and Hultgren, S.J. (2002). Role of Escherichia coli curli operons in directing amyloid fiber formation. Science New York, NY 295, 851-855.
17. Dechant, R., Binda, M., Lee, S.S., Pelet, S., Winderickx, J., and Peter, M. (2010). Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. The EMBO journal 29, 2515-2526.
18. Fowler, D.M., Koulov, A.V., Alory-Jost, C., Marks, M.S., Balch, W.E., and Kelly, J.W. (2006). Functional amyloid formation within mammalian tissue. PLoS Biol 4, 6.
19. Gross, J.D., Bradbury, J., Kay, R.R., and Peacey, M.J. (1983). Intracellular pH and the control of cell differentiation in Dictyostelium discoideum. Nature 303, 244-245.
20. Gueldener, U., Heinisch, J., Koehler, G.J., Voss, D., and Hegemann, J.H. (2002). A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic acids research 30, 23.
21. Hand, S.C., Menze, M.A., Borcar, A., Patil, Y., Covi, J.A., Reynolds, J.A., and Toner, M. (2011). Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. J Insect Physiol 57, 584-594.
22. He, Y.X., Gui, L., Liu, Y.Z., Du, Y., Zhou, Y., Li, P., and Zhou, C.Z. (2009). Crystal structure of Saccharomyces cerevisiae glutamine synthetase Gln1 suggests a nanotube-like supramolecular assembly. Proteins 76, 249-254.
23. Hyman, A.A., and Simons, K. (2012). Cell biology. Beyond oil and water-phase transitions in cells. Science New York, NY 337, 1047-1049.
24. Ingerson-Mahar, M., Briegel, A., Werner, J.N., Jensen, G.J., and Gitai, Z. (2010). The metabolic enzyme CTP synthase forms cytoskeletal filaments. Nature cell biology 12, 739-746.
25. Isom, D.G., Sridharan, V., Baker, R., Clement, S.T., Smalley, D.M., and Dohlman, H.G. (2013). Protons as second messenger regulators of G protein signaling. Mol Cell 51, 531-538.
26. Klosinska, M.M., Crutchfield, C.A., Bradley, P.H., Rabinowitz, J.D., and Broach, J.R. (2011). Yeast cells can access distinct quiescent states. Genes Dev 25, 336-349.
27. Kronqvist, N., Otikovs, M., Chmyrov, V., Chen, G., Andersson, M., Nordling, K., Landreh, M., Sarr, M., Jornvall, H., Wennmalm, S., et al. (2014). Sequential pH-driven dimerization and stabilization of the N-terminal domain enables rapid spider silk formation. Nat Commun 5, 3254.
28. Laporte, D., Courtout, F., Salin, B., Ceschin, J., and Sagot, I. (2013). An array of nuclear microtubules reorganizes the budding yeast nucleus during quiescence. The Journal of cell biology 203, 585-594.
29. Laporte, D., Lebaudy, A., Sahin, A., Pinson, B., Ceschin, J., Daignan-Fornier, B., and Sagot, I. (2011). Metabolic status rather than cell cycle signals control quiescence entry and exit. The Journal of cell biology 192, 949-957.
30. Laporte, D., Salin, B., Daignan-Fornier, B., and Sagot, I. (2008). Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. The Journal of cell biology 181, 737-745.
31. Li, P., Banjade, S., Cheng, H.C., Kim, S., Chen, B., Guo, L., Llaguno, M., Hollingsworth, J.V., King, D.S., Banani, S.F., et al. (2012). Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336-340.
32. Liu, I.C., Chiu, S.W., Lee, H.Y., and Leu, J.Y. (2012). The histone deacetylase Hos2 forms an Hsp42-dependent cytoplasmic granule in quiescent yeast cells. Molecular biology of the cell 23, 1231-1242.
33. Malan, A. (2014). The Evolution of Mammalian Hibernation: Lessons from Comparative Acid-Base Physiology. Integr Comp Biol. doi 10.1093/icb/icu002.
34. Marenduzzo, D., Finan, K., and Cook, P.R. (2006). The depletion attraction: an underappreciated force driving cellular organization. The Journal of cell biology 175, 681-686.
35. Minton, A.P. (2001). The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276, 10577-10580.
36. Mitchell, A.P., and Magasanik, B. (1984). Biochemical and physiological aspects of glutamine synthetase inactivation in Saccharomyces cerevisiae. J Biol Chem 259, 12054-12062.
37. Moolenaar, W.H. (1986). Effects of growth factors on intracellular pH regulation. Annu Rev Physiol 48, 363-376.
38. Narayanaswamy, R., Levy, M., Tsechansky, M., Stovall, G.M., O'Connell, J.D., Mirrielees, J., Ellington, A.D., and Marcotte, E.M. (2009). Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proceedings of the National Academy of Sciences of the United States of America 106, 10147-10152.
39. Noree, C., Sato, B.K., Broyer, R.M., and Wilhelm, J.E. (2010). Identification of novel filament-forming proteins in Saccharomyces cerevisiae and Drosophila melanogaster. The Journal of cell biology 190, 541-551.
40. O'Connell, J.D., Zhao, A., Ellington, A.D., and Marcotte, E.M. (2012). Dynamic reorganization of metabolic enzymes into intracellular bodies. Annu Rev Cell Dev Biol 28, 89-111.
41. Orij, R., Brul, S., and Smits, G.J. (2011). Intracellular pH is a tightly controlled signal in yeast. Bba-Gen Subjects 1810, 933-944.
42. Orij, R., Postmus, J., Ter Beek, A., Brul, S., and Smits, G.J. (2009). In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiol-Sgm 155, 268-278.
43. Orij, R., Urbanus, M.L., Vizeacoumar, F.J., Giaever, G., Boone, C., Nislow, C., Brul, S., and Smits, G.J. (2012). Genome-wide analysis of intracellular pH reveals quantitative control of cell division rate by pH(c) in Saccharomyces cerevisiae. Genome Biology 13:R80.
44. Parry, B.R., Surovtsev, I.V., Cabeen, M.T., O'Hern, C.S., Dufresne, E.R., and Jacobs-Wagner, C. (2014). The Bacterial Cytoplasm Has Glass-like Properties and Is Fluidized by Metabolic Activity. Cell 156, 183-194.
45. Peters, L.Z., Hazan, R., Breker, M., Schuldiner, M., and Ben-Aroya, S. (2013). Formation and dissociation of proteasome storage granules are regulated by cytosolic pH. The Journal of cell biology 201, 663-671.
46. Pintsch, T., Satre, M., Klein, G., Martin, J.B., and Schuster, S.C. (2001). Cytosolic acidification as a signal mediating hyperosmotic stress responses in Dictyostelium discoideum. BMC cell biology 2, 9.
47. Sagot, I., Pinson, B., Salin, B., and Daignan-Fornier, B. (2006). Actin bodies in yeast quiescent cells: an immediately available actin reserve? Molecular biology of the cell 17, 4645-4655.
48. Setlow, B., and Setlow, P. (1980). Measurements of the pH within dormant and germinated bacterial spores. Proceedings of the National Academy of Sciences of the United States of America 77, 2474-2476.
49. Sheff, M.A., and Thorn, K.S. (2004). Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21, 661-670.
50. Srere, P.A. (1987). Complexes of sequential metabolic enzymes. Annual review of biochemistry 56, 89-124.
51. Webb, B.A., Chimenti, M., Jacobson, M.P., and Barber, D.L. (2011). Dysregulated pH: a perfect storm for cancer progression. Nat Rev Cancer 11, 671-677.
52. Wilson, M.Z., and Gitai, Z. (2013). Beyond the cytoskeleton: mesoscale assemblies and their function in spatial organization. Current opinion in microbiology 16, 177-183.
53. Yeates, T.O., Crowley, C.S., and Tanaka, S. (2010). Bacterial microcompartment organelles: protein shell structure and evolution. Annu Rev Biophys 39, 185-205.
54. Zetterberg, A., and Engstrom, W. (1981). Mitogenic effect of alkaline pH on quiescent, serum-starved cells. Proceedings of the National Academy of Sciences of the United States of America 78, 4334-4338.