Compartmentation is essential for the localization of biological processes within a cell. In 2010, three groups independently reported that cytidine triphosphate synthase (CTPS), a metabolic enzyme for de novo synthesis of the nucleotide CTP, is compartmentalized in cytoophidia (Greek for “cellular snakes”) in bacteria, yeast, and fruit flies. Subsequent studies demonstrate that CTPS can also form filaments in human cells. Thus, the cytoophidium represents a new type of intracellular compartment that is strikingly conserved across prokaryotes and eukaryotes. Multiple lines of evidence have recently suggested that polymerization of metabolic enzymes such as CTPS and inosine monophosphate dehydrogenase into filamentous cytoophidia modulates enzymatic activity. With many more metabolic enzymes found to form the cytoophidium and its kind, compartmentation via filamentation may serve as a general mechanism for the regulation of metabolism.


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Literature Cited

  1. An S, Kumar R, Sheets ED, Benkovic SJ. 2008. Reversible compartmentalization of de novo purine biosynthetic complexes in living cells. Science 320:103–6 [Google Scholar]
  2. Anderson PM. 1983. CTP synthetase from Escherichia coli: an improved purification procedure and characterization of hysteretic and enzyme concentration effects on kinetic properties. Biochemistry 22:3285–92 [Google Scholar]
  3. Aronow B, Ullman B. 1987. In situ regulation of mammalian CTP synthetase by allosteric inhibition. J. Biol. Chem. 262:5106–12 [Google Scholar]
  4. Aughey GN, Grice SJ, Liu JL. 2016. The interplay between Myc and CTP synthase in Drosophila. PLOS Genet. 12:e1005867 [Google Scholar]
  5. Aughey GN, Grice SJ, Shen QJ, Xu Y, Chang CC. et al. 2014. Nucleotide synthesis is regulated by cytoophidium formation during neurodevelopment and adaptive metabolism. Biol. Open 3:1045–56 [Google Scholar]
  6. Azzam G, Liu JL. 2013. Only one isoform of Drosophila melanogaster CTP synthase forms the cytoophidium. PLOS Genet. 9:e1003256 [Google Scholar]
  7. Barry RM, Bitbol AF, Lorestani A, Charles EJ, Habrian CH. et al. 2014. Large-scale filament formation inhibits the activity of CTP synthetase. eLife 3:e03638 [Google Scholar]
  8. Bateman A. 1997. The structure of a domain common to archaebacteria and the homocystinuria disease protein. Trends Biochem. Sci. 22:12–13 [Google Scholar]
  9. Bearne SL, Hekmat O, Macdonnell JE. 2001. Inhibition of Escherichia coli CTP synthase by glutamate gamma-semialdehyde and the role of the allosteric effector GTP in glutamine hydrolysis. Biochem. J. 356:223–32 [Google Scholar]
  10. Bilgen T. 2004. Metabolic evolution and the origin of life. Functional Metabolism: Regulation and Adaptation KB Storey 557–82 Hoboken, NJ: Wiley-Liss [Google Scholar]
  11. Bowne SJ, Sullivan LS, Blanton SH, Cepko CL, Blackshaw S. et al. 2002. Mutations in the inosine monophosphate dehydrogenase 1 gene (IMPDH1) cause the RP10 form of autosomal dominant retinitis pigmentosa. Hum. Mol. Genet. 11:559–68 [Google Scholar]
  12. Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C. et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–32 [Google Scholar]
  13. Buszczak M, Paterno S, Lighthouse D, Bachman J, Planck J. et al. 2007. The Carnegie protein trap library: a versatile tool for Drosophila developmental studies. Genetics 175:1505–31 [Google Scholar]
  14. Calise SJ, Keppeke GD, Andrade LE, Chan EK. 2015. Anti-rods/rings: a human model of drug-induced autoantibody generation. Front. Immunol. 6:41 [Google Scholar]
  15. Carcamo WC, Calise SJ, Von Muhlen CA, Satoh M, Chan EK. 2014. Molecular cell biology and immunobiology of mammalian rod/ring structures. Int. Rev. Cell Mol. Biol. 308:35–74 [Google Scholar]
  16. Carcamo WC, Satoh M, Kasahara H, Terada N, Hamazaki T. et al. 2011. Induction of cytoplasmic rods and rings structures by inhibition of the CTP and GTP synthetic pathway in mammalian cells. PLOS ONE 6:e29690 [Google Scholar]
  17. Chakraborty KP, Hurlbert RB. 1961. Role of glutamine in the biosynthesis of cytidine nucleotides in Escherichia coli. Biochim. Biophys. Acta 47:607–9 [Google Scholar]
  18. Chang CC, Lin WC, Pai LM, Lee HS, Wu SC. et al. 2015. Cytoophidium assembly reflects upregulation of IMPDH activity. J. Cell Sci. 128:3550–55 [Google Scholar]
  19. Chen K, Zhang J, Tastan OY, Deussen ZA, Siswick MY, Liu JL. 2011. Glutamine analogs promote cytoophidium assembly in human and Drosophila cells. J. Genet. Genom. 38:391–402 [Google Scholar]
  20. Climent J, Morandeira F, Castellote J, Xiol J, Niubo J. et al. 2016. Clinical correlates of the “rods and rings” antinuclear antibody pattern. Autoimmunity 49:102–8 [Google Scholar]
  21. De Clercq E. 2001. Vaccinia virus inhibitors as a paradigm for the chemotherapy of poxvirus infections. Clin. Microbiol. Rev. 14:382–97 [Google Scholar]
  22. Dyson F. 1999. Origins of Life Cambridge, UK: Cambridge Univ. Press
  23. Ellims PH, Gan TE, Medley G. 1983. Cytidine triphosphate synthetase activity in lymphoproliferative disorders. Cancer Res. 43:1432–35 [Google Scholar]
  24. Endrizzi JA, Kim H, Anderson PM, Baldwin EP. 2004. Crystal structure of Escherichia coli cytidine triphosphate synthetase, a nucleotide-regulated glutamine amidotransferase/ATP-dependent amidoligase fusion protein and homologue of anticancer and antiparasitic drug targets. Biochemistry 43:6447–63 [Google Scholar]
  25. Endrizzi JA, Kim H, Anderson PM, Baldwin EP. 2005. Mechanisms of product feedback regulation and drug resistance in cytidine triphosphate synthetases from the structure of a CTP-inhibited complex. Biochemistry 44:13491–99 [Google Scholar]
  26. Fijolek A, Hofer A, Thelander L. 2007. Expression, purification, characterization, and in vivo targeting of trypanosome CTP synthetase for treatment of African sleeping sickness. J. Biol. Chem. 282:11858–65 [Google Scholar]
  27. Gall JG. 2000. Cajal bodies: the first 100 years. Annu. Rev. Cell Dev. Biol. 16:273–300 [Google Scholar]
  28. Genchev DD, Mandel P. 1976. Changes of CTP synthetase activity during postnatal rat brain development. J. Neurosci. Res. 2:413–18 [Google Scholar]
  29. Gilbert W. 1986. The RNA world. Nature 319:618 [Google Scholar]
  30. Goto M, Omi R, Nakagawa N, Miyahara I, Hirotsu K. 2004. Crystal structures of CTP synthetase reveal ATP, UTP, and glutamine binding sites. Structure 12:1413–23 [Google Scholar]
  31. Gou KM, Chang CC, Shen QJ, Sung LY, Liu JL. 2014. CTP synthase forms cytoophidia in the cytoplasm and nucleus. Exp. Cell Res. 323:242–53 [Google Scholar]
  32. Hedstrom L. 2009. IMP dehydrogenase: structure, mechanism, and inhibition. Chem. Rev. 109:2903–28 [Google Scholar]
  33. Hendriks EF, O'Sullivan WJ, Stewart TS. 1998. Molecular cloning and characterization of the Plasmodium falciparum cytidine triphosphate synthetase gene. Biochim. Biophys. Acta 1399:213–18 [Google Scholar]
  34. Higgins MJ, Loiselle D, Haystead TA, Graves LM. 2008. Human cytidine triphosphate synthetase 1 interacting proteins. Nucleosides Nucleotides Nucleic Acids 27:850–57 [Google Scholar]
  35. Hofer A, Steverding D, Chabes A, Brun R, Thelander L. 2001. Trypanosoma brucei CTP synthetase: a target for the treatment of African sleeping sickness. PNAS 98:6412–16 [Google Scholar]
  36. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW. et al. 2003. Global analysis of protein localization in budding yeast. Nature 425:686–91 [Google Scholar]
  37. Hung V, Zou P, Rhee HW, Udeshi ND, Cracan V. et al. 2014. Proteomic mapping of the human mitochondrial intermembrane space in live cells via ratiometric APEX tagging. Mol. Cell 55:332–41 [Google Scholar]
  38. Hyman AA, Weber CA, Julicher F. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58 [Google Scholar]
  39. Ingerson-Mahar M, Briegel A, Werner JN, Jensen GJ, Gitai Z. 2010. The metabolic enzyme CTP synthase forms cytoskeletal filaments. Nat. Cell Biol. 12:739–46 [Google Scholar]
  40. Ji Y, Gu J, Makhov AM, Griffith JD, Mitchell BS. 2006. Regulation of the interaction of inosine monophosphate dehydrogenase with mycophenolic acid by GTP. J. Biol. Chem. 281:206–12 [Google Scholar]
  41. Joyce GF. 2002. The antiquity of RNA-based evolution. Nature 418:214–21 [Google Scholar]
  42. Kammen HO, Hurlbert RB. 1958. Amination of uridine nucleotides to cytidine nucleotides by soluble mammalian enzymes; role of glutamine and guanosine nucleotides. Biochim. Biophys. Acta 30:195–96 [Google Scholar]
  43. Kammen HO, Hurlbert RB. 1959. The formation of cytidine nucleotides and RNA cytosine from orotic acid by the Novikoff tumor in vitro. Cancer Res. 19:654–63 [Google Scholar]
  44. Keppeke GD, Calise SJ, Chan EK, Andrade LE. 2015. Assembly of IMPDH2-based, CTPS-based, and mixed rod/ring structures is dependent on cell type and conditions of induction. J. Genet. Genom. 42:287–99 [Google Scholar]
  45. Keppeke GD, Nunes E, Ferraz ML, Silva EA, Granato C. et al. 2012. Longitudinal study of a human drug-induced model of autoantibody to cytoplasmic rods/rings following HCV therapy with ribavirin and interferon-alpha. PLOS ONE 7:e45392 [Google Scholar]
  46. Keppeke GD, Satoh M, Ferraz ML, Chan EK, Andrade LE. 2014. Temporal evolution of human autoantibody response to cytoplasmic rods and rings structure during anti-HCV therapy with ribavirin and interferon-alpha. Immunol. Res. 60:38–49 [Google Scholar]
  47. Kizaki H, Ohsaka F, Sakurada T. 1985. CTP synthetase from Ehrlich ascites tumor cells. Subunit stoichiometry and regulation of activity. Biochim. Biophys. Acta 829:34–43 [Google Scholar]
  48. Kizaki H, Williams JC, Morris HP, Weber G. 1980. Increased cytidine 5′-triphosphate synthetase activity in rat and human tumors. Cancer Res. 40:3921–27 [Google Scholar]
  49. Kozhevnikova EN, Van Der Knaap JA, Pindyurin AV, Ozgur Z, Van Ijcken WF. et al. 2012. Metabolic enzyme IMPDH is also a transcription factor regulated by cellular state. Mol. Cell 47:133–39 [Google Scholar]
  50. Labesse G, Alexandre T, Vaupre L, Salard-Arnaud I, Him JL. et al. 2013. MgATP regulates allostery and fiber formation in IMPDHs. Structure 21:975–85 [Google Scholar]
  51. Lam SS, Martell JD, Kamer KJ, Deerinck TJ, Ellisman MH. et al. 2015. Directed evolution of APEX2 for electron microscopy and proximity labeling. Nat. Methods 12:51–54 [Google Scholar]
  52. Lee L, Davies SE, Liu JL. 2009. The spinal muscular atrophy protein SMN affects Drosophila germline nuclear organization through the U body–P body pathway. Dev. Biol. 332:142–55 [Google Scholar]
  53. Levitzki A, Koshland DE Jr. 1969. Negative cooperativity in regulatory enzymes. PNAS 62:1121–28 [Google Scholar]
  54. Levitzki A, Koshland DE Jr. 1970. Ligand-induced association-dissociation as a means for enzyme purification. Biochim. Biophys. Acta 206:473–75 [Google Scholar]
  55. Levitzki A, Koshland DE Jr. 1971. Cytidine triphosphate synthetase. Covalent intermediates and mechanisms of action. Biochemistry 10:3365–71 [Google Scholar]
  56. Levitzki A, Koshland DE Jr. 1972a. Ligand-induced dimer-to-tetramer transformation in cytosine triphosphate synthetase. Biochemistry 11:247–53 [Google Scholar]
  57. Levitzki A, Koshland DE Jr. 1972b. Role of an allosteric effector. Guanosine triphosphate activation in cytosine triphosphate synthetase. Biochemistry 11:241–46 [Google Scholar]
  58. Levitzki A, Stallcup WB, Koshland DE Jr. 1971. Half-of-the-sites reactivity and the conformational states of cytidine triphosphate synthetase. Biochemistry 10:3371–78 [Google Scholar]
  59. Lewis DA, Villafranca JJ. 1989. Investigation of the mechanism of CTP synthetase using rapid quench and isotope partitioning methods. Biochemistry 28:8454–59 [Google Scholar]
  60. Li Y, Li G, Gorling B, Luy B, Du J, Yan J. 2015. Integrative analysis of circadian transcriptome and metabolic network reveals the role of de novo purine synthesis in circadian control of cell cycle. PLOS Comput. Biol. 11:e1004086 [Google Scholar]
  61. Li Z, Jensen GJ. 2009. Electron cryotomography: a new view into microbial ultrastructure. Curr. Opin. Microbiol. 12:333–40 [Google Scholar]
  62. Lieberman I. 1955. Enzymatic amination of uridine triphosphate to cytidine triphosphate. J. Am. Chem. Soc. 77:2661–62 [Google Scholar]
  63. Lieberman I. 1956. Enzymatic amination of uridine triphosphate to cytidine triphosphate. J. Biol. Chem. 222:765–75 [Google Scholar]
  64. Liu JL. 2010. Intracellular compartmentation of CTP synthase in Drosophila. J. Genet. Genom. 37:281–96 [Google Scholar]
  65. Liu JL. 2011. The enigmatic cytoophidium: compartmentation of CTP synthase via filament formation. BioEssays 33:159–64 [Google Scholar]
  66. Liu JL, Buszczak M, Gall JG. 2006a. Nuclear bodies in the Drosophila germinal vesicle. Chromosome Res. 14:465–75 [Google Scholar]
  67. Liu JL, Gall JG. 2007. U bodies are cytoplasmic structures that contain uridine-rich small nuclear ribonu-cleoproteins and associate with P bodies. PNAS 104:11655–59 [Google Scholar]
  68. Liu JL, Murphy C, Buszczak M, Clatterbuck S, Goodman R, Gall JG. 2006b. The Drosophila melanogaster Cajal body. J. Cell Biol. 172:875–84 [Google Scholar]
  69. Liu YC, Li F, Handler J, Huang CR, Xiang Y. et al. 2008. Global regulation of nucleotide biosynthetic genes by c-Myc. PLOS ONE 3:e2722 [Google Scholar]
  70. Long CW, Levitzki A, Koshland DE Jr. 1970. The subunit structure and subunit interactions of cytidine triphosphate synthetase. J. Biol. Chem. 245:80–87 [Google Scholar]
  71. Long CW, Pardee AB. 1967. Cytidine triphosphate synthetase of Escherichia coli B. I. Purification and kinetics. J. Biol. Chem. 242:4715–21 [Google Scholar]
  72. Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK. et al. 2012. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143–48 [Google Scholar]
  73. Martin E, Palmic N, Sanquer S, Lenoir C, Hauck F. et al. 2014. CTP synthase 1 deficiency in humans reveals its central role in lymphocyte proliferation. Nature 510:288–92 [Google Scholar]
  74. Narayanaswamy R, Levy M, Tsechansky M, Stovall GM, O'Connell JD. et al. 2009. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. PNAS 106:10147–52 [Google Scholar]
  75. Noree C, Monfort E, Shiau AK, Wilhelm JE. 2014. Common regulatory control of CTP synthase enzyme activity and filament formation. Mol. Biol. Cell 25:2282–90 [Google Scholar]
  76. Noree C, Sato BK, Broyer RM, Wilhelm JE. 2010. Identification of novel filament-forming proteins in Saccharomyces cerevisiae and Drosophila melanogaster. J. Cell Biol. 190:541–51 [Google Scholar]
  77. Novembrino C, Aghemo A, Ferraris Fusarini C, Maiavacca R, Matinato C. et al. 2014. Interferon-ribavirin therapy induces serum antibodies determining ‘rods and rings’ pattern in hepatitis C patients. J. Viral Hepat. 21:944–49 [Google Scholar]
  78. O'Connell JD, Zhao A, Ellington AD, Marcotte EM. 2012. Dynamic reorganization of metabolic enzymes into intracellular bodies. Annu. Rev. Cell Dev. Biol. 28:89–111 [Google Scholar]
  79. Ovadi J, Saks V. 2004. On the origin of intracellular compartmentation and organized metabolic systems. Mol. Cell. Biochem. 256–257:5–12 [Google Scholar]
  80. Pappas A, Yang WL, Park TS, Carman GM. 1998. Nucleotide-dependent tetramerization of CTP synthetase from Saccharomyces cerevisiae. J. Biol. Chem. 273:15954–60 [Google Scholar]
  81. Petrovska I, Nuske E, Munder MC, Kulasegaran G, Malinovska L. et al. 2014. Filament formation by metabolic enzymes is a specific adaptation to an advanced state of cellular starvation. eLife 3:e02409 [Google Scholar]
  82. Rhee HW, Zou P, Udeshi ND, Martell JD, Mootha VK. et al. 2013. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339:1328–31 [Google Scholar]
  83. Robertson JG. 1995. Determination of subunit dissociation constants in native and inactivated CTP synthetase by sedimentation equilibrium. Biochemistry 34:7533–41 [Google Scholar]
  84. Scheit KH, Linke HJ. 1982. Substrate specificity of CTP synthetase from Escherichia coli. Eur. J. Biochem. 126:57–60 [Google Scholar]
  85. Shen QJ, Kassim H, Huang Y, Li H, Zhang J. et al. 2016. Filamentation of metabolic enzymes in Saccharomyces cerevisiae. J. Genet. Genom. 43393–404
  86. Sheth U, Parker R. 2006. Targeting of aberrant mRNAs to cytoplasmic processing bodies. Cell 125:1095–109 [Google Scholar]
  87. Sitte P. 1980. General principles of cellular compartmentation. Cell Compartmentation and Metabolic Channeling L Nover, F Lynen, K Mothes 17–32 Amsterdam: Elsevier [Google Scholar]
  88. Strochlic TI, Stavrides KP, Thomas SV, Nicolas E, O'Reilly AM, Peterson JR. 2014. Ack kinase regulates CTP synthase filaments during Drosophila oogenesis. EMBO Rep. 15:1184–91 [Google Scholar]
  89. Tastan OY, Liu JL. 2015. CTP synthase is required for optic lobe homeostasis in Drosophila. J. Genet. Genom. 42:261–74 [Google Scholar]
  90. Thomas EC, Gunter JH, Webster JA, Schieber NL, Oorschot V. et al. 2012. Different characteristics and nucleotide binding properties of inosine monophosphate dehydrogenase (IMPDH) isoforms. PLOS ONE 7:e51096 [Google Scholar]
  91. Van Den Berg AA, Van Lenthe H, Busch S, De Korte D, Roos D. et al. 1993. Evidence for transformation-related increase in CTP synthetase activity in situ in human lymphoblastic leukemia. Eur. J. Biochem. 216:161–67 [Google Scholar]
  92. Van Den Berg AA, Van Lenthe H, Kipp JB, De Korte D, Van Kuilenburg AB, Van Gennip AH. 1995. Cytidine triphosphate (CTP) synthetase activity during cell cycle progression in normal and malignant T-lymphocytic cells. Eur. J. Cancer 31A:108–12 [Google Scholar]
  93. Verschuur AC, Brinkman J, Van Gennip AH, Leen R, Vet RJ. et al. 2001. Cyclopentenyl cytosine induces apoptosis and increases cytarabine-induced apoptosis in a T-lymphoblastic leukemic cell-line. Leuk. Res. 25:891–900 [Google Scholar]
  94. Verschuur AC, Van Gennip AH, Brinkman J, Voute PA, Van Kuilenburg AB. 2000a. Cyclopentenyl cytosine induces apoptosis and secondary necrosis in a T-lymphoblastic leukemic cell-line. Adv. Exp. Med. Biol. 486:319–25 [Google Scholar]
  95. Verschuur AC, Van Gennip AH, Leen R, Meinsma R, Voute PA, Van Kuilenburg AB. 2000b. In vitro inhibition of cytidine triphosphate synthetase activity by cyclopentenyl cytosine in paediatric acute lymphocytic leukaemia. Br. J. Haematol. 110:161–69 [Google Scholar]
  96. Verschuur AC, Van Gennip AH, Leen R, Muller EJ, Elzinga L. et al. 2000c. Cyclopentenyl cytosine inhibits cytidine triphosphate synthetase in paediatric acute non-lymphocytic leukaemia: a promising target for chemotherapy. Eur. J. Cancer 36:627–35 [Google Scholar]
  97. Verschuur AC, Van Gennip AH, Leen R, Voute PA, Van Kuilenburg AB. 2000d. Cyclopentenyl cytosine increases the phosphorylation and incorporation into DNA of arabinofu-ranosyl cytosine in a myeloid leukemic cell-line. Adv. Exp. Med. Biol. 486:311–17 [Google Scholar]
  98. Verschuur AC, Van Gennip AH, Muller EJ, Voute PA, Van Kuilenburg AB. 1998. Increased activity of cytidine triphosphate synthetase in pediatric acute lymphoblastic leukemia. Adv. Exp. Med. Biol. 431:667–71 [Google Scholar]
  99. Von Der Saal W, Anderson PM, Villafranca JJ. 1985. Mechanistic investigations of Escherichia coli cytidine-5′-triphosphate synthetase. Detection of an intermediate by positional isotope exchange experiments. J. Biol. Chem. 260:14993–97 [Google Scholar]
  100. Wang PY, Lin WC, Tsai YC, Cheng ML, Lin YH. et al. 2015. Regulation of CTP synthase filament formation during DNA endoreplication in Drosophila. Genetics 201:1511–23 [Google Scholar]
  101. Weber G, Lui MS, Takeda E, Denton JE. 1980. Enzymology of human colon tumors. Life Sci. 27:793–99 [Google Scholar]
  102. Whelan J, Smith T, Phear G, Rohatiner A, Lister A, Meuth M. 1994. Resistance to cytosine arabinoside in acute leukemia: the significance of mutations in CTP synthetase. Leukemia 8:264–65 [Google Scholar]
  103. Williams JC, Kizaki H, Weber G, Morris HP. 1978. Increased CTP synthetase activity in cancer cells. Nature 271:71–73 [Google Scholar]
  104. Willoughby LF, Schlosser T, Manning SA, Parisot JP, Street IP. et al. 2013. An in vivo large-scale chemical screening platform using Drosophila for anti-cancer drug discovery. Dis. Model. Mech. 6:521–29 [Google Scholar]
  105. Wu CH, Sahoo D, Arvanitis C, Bradon N, Dill DL, Felsher DW. 2008. Combined analysis of murine and human microarrays and ChIP analysis reveals genes associated with the ability of MYC to maintain tumorigenesis. PLOS Genet. 4:e1000090 [Google Scholar]
  106. Wylie JL, Berry JD, McClarty G. 1996. Chlamydia trachomatis CTP synthetase: molecular characterization and developmental regulation of expression. Mol. Microbiol. 22:631–42 [Google Scholar]
  107. Yang WL, Bruno ME, Carman GM. 1996. Regulation of yeast CTP synthetase activity by protein kinase C. J. Biol. Chem. 271:11113–19 [Google Scholar]
  108. Yang WL, Carman GM. 1995. Phosphorylation of CTP synthetase from Saccharomyces cerevisiae by protein kinase C. J. Biol. Chem. 270:14983–88 [Google Scholar]
  109. Yang WL, Carman GM. 1996. Phosphorylation and regulation of CTP synthetase from Saccharomyces cerevisiae by protein kinase A. J. Biol. Chem. 271:28777–83 [Google Scholar]
  110. Yang WL, McDonough VM, Ozier-Kalogeropoulos O, Adeline MT, Flocco MT, Carman GM. 1994. Purification and characterization of CTP synthetase, the product of the URA7 gene in Saccharomyces cerevisiae. Biochemistry 33:10785–93 [Google Scholar]
  111. Zhang J, Hulme L, Liu JL. 2014. Asymmetric inheritance of cytoophidia in Schizosaccharomyces pombe. Biol. Open 3:1092–97 [Google Scholar]

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