Genetic relationships between the RACK1 homolog cpc-2 and heterotrimeric G protein subunit genes in Neurospora crassa

English version

Autoři: Amruta Garud ^aff001; Alexander J. Carrillo ^aff001; Logan A. Collier ^aff001; Arit Ghosh ^aff001; James D. Kim ^aff001; Berenise Lopez-Lopez ^aff001; Shouqiang Ouyang ^aff001; Katherine A. Borkovich ^aff001
Působiště autorů: Department of Microbiology and Plant Pathology, University of California, Riverside, California, United States of America ^aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0223334

Souhrn

Receptor for Activated C Kinase-1 (RACK1) is a multifunctional eukaryotic scaffolding protein with a seven WD repeat structure. Among their many cellular roles, RACK1 homologs have been shown to serve as alternative Gβ subunits during heterotrimeric G protein signaling in many systems. We investigated genetic interactions between the RACK1 homolog cpc-2, the previously characterized Gβ subunit gnb-1 and other G protein signaling components in the multicellular filamentous fungus Neurospora crassa. Results from cell fractionation studies and from fluorescent microscopy of a strain expressing a CPC-2-GFP fusion protein revealed that CPC-2 is a cytoplasmic protein. Genetic epistasis experiments between cpc-2, the three Gα genes (gna-1, gna-2 and gna-3) and gnb-1 demonstrated that cpc-2 is epistatic to gna-2 with regards to basal hyphae growth rate and aerial hyphae height, while deletion of cpc-2 mitigates the increased macroconidiation on solid medium observed in Δgnb-1 mutants. Δcpc-2 mutants inappropriately produce conidiophores during growth in submerged culture and mutational activation of gna-3 alleviates this defect. Δcpc-2 mutants are female-sterile and fertility could not be restored by mutational activation of any of the three Gα genes. With the exception of macroconidiation on solid medium, double mutants lacking cpc-2 and gnb-1 exhibited more severe defects for all phenotypic traits, supporting a largely synergistic relationship between GNB-1 and CPC-2 in N. crassa.

Klíčová slova:

Cell membranes – Fungal genetics – Gel electrophoresis – Membrane proteins – Particulates – Phenotypes – Protein extraction – Neurospora crassa

Zdroje

1. Bock A, Kostenis E, Trankle C, Lohse MJ, Mohr K. Pilot the pulse: controlling the multiplicity of receptor dynamics. Trends Pharmacol Sci. 2014;35(12):630–8. doi: 10.1016/j.tips.2014.10.002 25455830.

2. Chini B, Parenti M, Poyner DR, Wheatley M. G-protein-coupled receptors: from structural insights to functional mechanisms. Biochem Soc Trans. 2013;41(1):135–6. doi: 10.1042/BST20120344 23356272.

3. Tesmer JJ. The quest to understand heterotrimeric G protein signaling. Nat Struct Mol Biol. 2010;17(6):650–2. doi: 10.1038/nsmb0610-650 20520658.

4. Selker EU. Neurospora. Curr Biol. 2011;21(4):R139–40. Epub 2011/02/22. doi: 10.1016/j.cub.2011.01.006 21334288.

5. Borkovich KA, Alex LA, Yarden O, Freitag M, Turner GE, Read ND, et al. Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev. 2004;68(1):1–108. doi: 10.1128/MMBR.68.1.1-108.2004 15007097.

6. Cabrera IE, Pacentine IV, Lim A, Guerrero N, Krystofova S, Li L, et al. Global Analysis of Predicted G Protein-Coupled Receptor Genes in the Filamentous Fungus, Neurospora crassa. G3 (Bethesda). 2015;5(12):2729–43. doi: 10.1534/g3.115.020974 26464358.

7. Li L, Wright SJ, Krystofova S, Park G, Borkovich KA. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol. 2007;61:423–52. doi: 10.1146/annurev.micro.61.080706.093432 17506673.

8. Wright SJ, Inchausti R, Eaton CJ, Krystofova S, Borkovich KA. RIC8 is a guanine-nucleotide exchange factor for Galpha subunits that regulates growth and development in Neurospora crassa. Genetics. 2011;189(1):165–76. doi: 10.1534/genetics.111.129270 21750256.

9. Li L, Borkovich KA. GPR-4 Is a Predicted G-Protein-Coupled Receptor Required for Carbon Source-Dependent Asexual Growth and Development in Neurospora crassa. Eukaryot Cell. 2006;5(8):1287–300. doi: 10.1128/EC.00109-06 16896213

10. Kim H, Wright SJ, Park G, Ouyang S, Krystofova S, Borkovich KA. Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics. 2012;190(4):1389–404. doi: 10.1534/genetics.111.136358 22298702.

11. Krystofova S, Borkovich KA. The predicted G-protein-coupled receptor GPR-1 is required for female sexual development in the multicellular fungus Neurospora crassa. Eukaryotic Cell. 2006;5(9):1503–16. doi: 10.1128/EC.00124-06 16963633

12. Li L, Wright SJ, Krystofova S, Park G, Borkovich KA. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol. 2007;61:423–52. doi: 10.1146/annurev.micro.61.080706.093432 17506673

13. Turner GE, Borkovich KA. Identification of a G protein alpha subunit from Neurospora crassa that is a member of the Gi family. J Biol Chem. 1993;268(20):14805–11. Epub 1993/07/15. 8325859.

14. Kays AM, Rowley PS, Baasiri RA, Borkovich KA. Regulation of conidiation and adenylyl cyclase levels by the G-alpha protein GNA-3 in Neurospora crassa. Mol Cell Biol. 2000;20(20):7693–705. doi: 10.1128/mcb.20.20.7693-7705.2000 11003665

15. Adams DR, Ron D, Kiely PA. RACK1, A multifaceted scaffolding protein: Structure and function. Cell Commun Signal. 2011;9:22. doi: 10.1186/1478-811X-9-22 21978545.

16. Adams DR, Ron D, Kiely PA. RACK1, A multifaceted scaffolding protein: Structure and function. Cell Commun Signal. 2011;9. Artn 22

17. Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D. Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc Natl Acad Sci U S A. 1994;91(3):839–43. doi: 10.1073/pnas.91.3.839 8302854.

18. Lopez-Bergami P, Habelhah H, Bhoumik A, Zhang W, Wang LH, Ronai Z. RACK1 mediates activation of JNK by protein kinase C [corrected]. Mol Cell. 2005;19(3):309–20. doi: 10.1016/j.molcel.2005.06.025 16061178.

19. Chen S, Dell EJ, Lin F, Sai J, Hamm HE. RACK1 regulates specific functions of Gbetagamma. J Biol Chem. 2004;279(17):17861–8. doi: 10.1074/jbc.M313727200 14963031.

20. Sengupta J, Nilsson J, Gursky R, Spahn CM, Nissen P, Frank J. Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat Struct Mol Biol. 2004;11(10):957–62. doi: 10.1038/nsmb822 15334071.

21. Zeller CE, Parnell SC, Dohlman HG. The RACK1 ortholog Asc1 functions as a G-protein beta subunit coupled to glucose responsiveness in yeast. J Biol Chem. 2007;282(34):25168–76. Epub 2007/06/27. doi: 10.1074/jbc.M702569200 17591772.

22. Palmer DA, Thompson JK, Li L, Prat A, Wang P. Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem. 2006;281(43):32596–605. Epub 2006/09/05. doi: 10.1074/jbc.M602768200 16950773.

23. Zeller CE, Parnell SC, Dohlman HG. The RACK1 ortholog Asc1 functions as a G-protein beta subunit coupled to glucose responsiveness in yeast. J Biol Chem. 2007;282(34):25168–76. doi: 10.1074/jbc.M702569200 17591772.

24. Palmer DA, Thompson JK, Li L, Prat A, Wang P. Gib2, a novel Gbeta-like/RACK1 homolog, functions as a Gbeta subunit in cAMP signaling and is essential in Cryptococcus neoformans. J Biol Chem. 2006;281(43):32596–605. doi: 10.1074/jbc.M602768200 16950773.

25. Li G, Zhang X, Tian H, Choi YE, Tao WA, Xu JR. MST50 is involved in multiple MAP kinase signaling pathways in Magnaporthe oryzae. Environ Microbiol. 2017;19(5):1959–74. doi: 10.1111/1462-2920.13710 28244240.

26. Yin Z, Zhang X, Wang J, Yang L, Feng W, Chen C, et al. MoMip11, a MoRgs7-interacting protein, functions as a scaffolding protein to regulate cAMP signaling and pathogenicity in the rice blast fungus Magnaporthe oryzae. Environ Microbiol. 2018;20(9):3168–85. doi: 10.1111/1462-2920.14102 29727050.

27. Nunez A, Franco A, Madrid M, Soto T, Vicente J, Gacto M, et al. Role for RACK1 orthologue Cpc2 in the modulation of stress response in fission yeast. Mol Biol Cell. 2009;20(18):3996–4009. doi: 10.1091/mbc.E09-05-0388 19625445.

28. Hoffmann B, Wanke C, Lapaglia SK, Braus GH. c-Jun and RACK1 homologues regulate a control point for sexual development in Aspergillus nidulans. Mol Microbiol. 2000;37(1):28–41. doi: 10.1046/j.1365-2958.2000.01954.x 10931303.

29. Cai ZD, Chai YF, Zhang CY, Qiao WR, Sang H, Lu L. The Gbeta-like protein CpcB is required for hyphal growth, conidiophore morphology and pathogenicity in Aspergillus fumigatus. Fungal Genet Biol. 2015;81:120–31. doi: 10.1016/j.fgb.2015.04.007 25892048.

30. Wang L, Berndt P, Xia X, Kahnt J, Kahmann R. A seven-WD40 protein related to human RACK1 regulates mating and virulence in Ustilago maydis. Mol Microbiol. 2011;81(6):1484–98. doi: 10.1111/j.1365-2958.2011.07783.x 21815950.

31. Kruger D, Koch J, Barthelmess IB. cpc-2, a new locus involved in general control of amino acid synthetic enzymes in Neurospora crassa. Curr Genet. 1990;18(3):211–5. doi: 10.1007/bf00318383 2147403.

32. Barthelmess IB, Kolanus J. The range of amino acids whose limitation activates general amino-acid control in Neurospora crassa. Genet Res. 1990;55(1):7–12. Epub 1990/02/01. doi: 10.1017/s0016672300025131 2138581.

33. Muller F, Kruger D, Sattlegger E, Hoffmann B, Ballario P, Kanaan M, et al. The cpc-2 gene of Neurospora crassa encodes a protein entirely composed of WD-repeat segments that is involved in general amino acid control and female fertility. Mol Gen Genet. 1995;248(2):162–73. doi: 10.1007/bf02190797 7651339.

34. Paluh JL, Orbach MJ, Legerton TL, Yanofsky C. The cross-pathway control gene of Neurospora crassa, cpc-1, encodes a protein similar to GCN4 of yeast and the DNA-binding domain of the oncogene v-jun-encoded protein. Proc Natl Acad Sci U S A. 1988;85(11):3728–32. doi: 10.1073/pnas.85.11.3728 2967496.

35. Sattlegger E, Hinnebusch AG, Barthelmess IB. cpc-3, the Neurospora crassa homologue of yeast GCN2, encodes a polypeptide with juxtaposed eIF2alpha kinase and histidyl-tRNA synthetase-related domains required for general amino acid control. J Biol Chem. 1998;273(32):20404–16. doi: 10.1074/jbc.273.32.20404 9685394.

36. McCluskey K, Wiest A, Plamann M. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J Biosci. 2010;35(1):119–26. doi: 10.1007/s12038-010-0014-6 20413916.

37. Vogel HJ. Distribution of lysine pathways among fungi: Evolutionary implications. Am Nat. 1964;98:435–46.

38. Westergaard M, Mitchell HK. Neurospora V. A synthetic medium favoring sexual reproduction. Amer J Bot. 1947;34:573–7.

39. Davis RH, deSerres FJ. Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol. 1970;71A:79–143.

40. Spatafora JW, Aime MC, Grigoriev IV, Martin F, Stajich JE, Blackwell M. The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies. Microbiol Spectr. 2017;5(5). doi: 10.1128/microbiolspec.FUNK-0053-2016 28917057.

41. Stajich JE, Harris T, Brunk BP, Brestelli J, Fischer S, Harb OS, et al. FungiDB: an integrated functional genomics database for fungi. Nucleic Acids Res. 2012;40(Database issue):D675–81. doi: 10.1093/nar/gkr918 22064857.

42. Lemoine F, Correia D, Lefort V, Doppelt-Azeroual O, Mareuil F, Cohen-Boulakia S, et al. NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res. 2019;47(W1):W260–W5. doi: 10.1093/nar/gkz303 31028399.

43. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80. doi: 10.1093/molbev/mst010 23329690.

44. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10:210. doi: 10.1186/1471-2148-10-210 20626897.

45. Lefort V, Desper R, Gascuel O. FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program. Mol Biol Evol. 2015;32(10):2798–800. doi: 10.1093/molbev/msv150 26130081.

46. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47(W1):W256–W9. doi: 10.1093/nar/gkz239 30931475.

47. Ghosh A, Servin JA, Park G, Borkovich KA. Global analysis of serine/threonine and tyrosine protein phosphatase catalytic subunit genes in Neurospora crassa reveals interplay between phosphatases and the p38 mitogen-activated protein kinase. G3 (Bethesda). 2014;4(2):349–65. doi: 10.1534/g3.113.008813 24347630.

48. Avalos J, Geever RF, Case ME. Bialaphos resistance as a dominant selectable marker in Neurospora crassa. Curr Genet. 1989;16(5–6):369–72. doi: 10.1007/bf00340716 2532965.

49. Pall M. The use of Ignite (basta; glufosinate; phosphinothricin) to select transformants of bar-containing plasmids in Neurospora crassa. Fungal Genet Newsl. 1993;40:57.

50. Perkins D. Advantages of using the inactive-mating-type am1 strain as a helper component in heterokaryons. Neurospora Newslett. 1985;31:41–2.

51. Kuck U, Hoff B. Application of the nourseothricin acetyltransferase gene (nat1) as dominant marker for the transformation of filamentous fungi. Fungal Genet Newsl. 2006;53:9–11.

52. Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P. Multifunctional yeast high-copy-number shuttle vectors. Gene. 1992;110(1):119–22. doi: 10.1016/0378-1119(92)90454-w 1544568.

53. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, et al. A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A. 2006;103(27):10352–7. Epub 2006/06/28. doi: 10.1073/pnas.0601456103 16801547.

54. Winston F, Dollard C, Ricupero-Hovasse SL. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast. 1995;11(1):53–5. doi: 10.1002/yea.320110107 7762301.

55. Won S, Michkov AV, Krystofova S, Garud AV, Borkovich KA. Genetic and physical interactions between Galpha subunits and components of the Gbetagamma dimer of heterotrimeric G proteins in Neurospora crassa. Eukaryot Cell. 2012;11(10):1239–48. doi: 10.1128/EC.00151-12 22903975.

56. Ivey FD, Hodge PN, Turner GE, Borkovich KA. The G alpha i homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Mol Biol Cell. 1996;7(8):1283–97. doi: 10.1091/mbc.7.8.1283 8856670.

57. Ebbole DJ, Sachs MS. A rapid and simple method for isolation of Neurospora crassa homokaryons using microconidia. Fungal Genet Newsl. 1990;37:17–8.

58. Ouyang S, Beecher CN, Wang K, Larive CK, Borkovich KA. Metabolic Impacts of Using Nitrogen and Copper-Regulated Promoters to Regulate Gene Expression in Neurospora crassa. G3 (Bethesda). 2015;5(9):1899–908.

59. Freitag M, Hickey PC, Raju NB, Selker EU, Read ND. GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet Biol. 2004;41(10):897–910. Epub 2004/09/03. doi: 10.1016/j.fgb.2004.06.008 15341912.

60. Park G, Servin JA, Turner GE, Altamirano L, Colot HV, Collopy P, et al. Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryotic cell. 2011;10(11):1553–64. Epub 2011/10/04. doi: 10.1128/EC.05140-11 21965514.

61. Krystofova S, Borkovich KA. The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gbetagamma dimer required for normal female fertility, asexual development, and galpha protein levels in Neurospora crassa. Eukaryot Cell. 2005;4(2):365–78. doi: 10.1128/EC.4.2.365-378.2005 15701799.

62. Turner GE, Borkovich KA. Identification of a G protein alpha subunit from Neurospora crassa that is a member of the Gi family. J Biol Chem. 1993;268(20):14805–11. 8325859.

63. Baasiri RA, Lu X, Rowley PS, Turner GE, Borkovich KA. Overlapping functions for two G protein alpha subunits in Neurospora crassa. Genetics. 1997;147(1):137–45. Epub 1997/09/01. 9286674.

64. Yang Q, Poole SI, Borkovich KA. A G-protein beta subunit required for sexual and vegetative development and maintenance of normal G alpha protein levels in Neurospora crassa. Eukaryot Cell. 2002;1(3):378–90. Epub 2002/11/29. doi: 10.1128/EC.1.3.378-390.2002 12455986.

65. Turner GE. Phenotypic analysis of Neurospora crassa gene deletion strains. Methods Mol Biol. 2011;722:191–8. doi: 10.1007/978-1-61779-040-9_14 21590422.

66. Eaton CJ, Cabrera IE, Servin JA, Wright SJ, Cox MP, Borkovich KA. The guanine nucleotide exchange factor RIC8 regulates conidial germination through Galpha proteins in Neurospora crassa. PLoS One. 2012;7(10):e48026. doi: 10.1371/journal.pone.0048026 23118921.

67. Borkovich KA, Weiss RL. Purification and characterization of arginase from Neurospora crassa. J Biol Chem. 1987;262(15):7081–6. 2953715.

68. Hager KM, Mandala SM, Davenport JW, Speicher DW, Benz EJ Jr., Slayman CW. Amino acid sequence of the plasma membrane ATPase of Neurospora crassa: deduction from genomic and cDNA sequences. Proc Natl Acad Sci U S A. 1986;83(20):7693–7. doi: 10.1073/pnas.83.20.7693 2876429.

69. Kays AM, Rowley PS, Baasiri RA, Borkovich KA. Regulation of conidiation and adenylyl cyclase levels by the Galpha protein GNA-3 in Neurospora crassa. Mol Cell Biol. 2000;20(20):7693–705. Epub 2000/09/26. doi: 10.1128/mcb.20.20.7693-7705.2000 11003665.

70. Corrochano LM, Kuo A, Marcet-Houben M, Polaino S, Salamov A, Villalobos-Escobedo JM, et al. Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication. Curr Biol. 2016;26(12):1577–84. doi: 10.1016/j.cub.2016.04.038 27238284.

71. Kim H, Borkovich KA. A pheromone receptor gene, pre-1, is essential for mating type-specific directional growth and fusion of trichogynes and female fertility in Neurospora crassa. Mol Microbiol. 2004;52(6):1781–98. doi: 10.1111/j.1365-2958.2004.04096.x 15186425.

72. Kays AM, Borkovich KA. Severe impairment of growth and differentiation in a Neurospora crassa mutant lacking all heterotrimeric G alpha proteins. Genetics. 2004;166(3):1229–40. 15082543.

73. Li L, Borkovich KA. GPR-4 is a predicted G-protein-coupled receptor required for carbon source-dependent asexual growth and development in Neurospora crassa. Eukaryot Cell. 2006;5(8):1287–300. doi: 10.1128/EC.00109-06 16896213.

74. Park G, Colot HV, Collopy PD, Krystofova S, Crew C, Ringelberg C, et al. High-throughput production of gene replacement mutants in Neurospora crassa. Methods Mol Biol. 2011;722:179–89. doi: 10.1007/978-1-61779-040-9_13 21590421.

75. Springer ML. Genetic control of fungal differentiation: the three sporulation pathways of Neurospora crassa. Bioessays. 1993;15(6):365–74. doi: 10.1002/bies.950150602 8357339.

76. Cortat M, Turian G. Conidiation of Neurospora crassa in submerged culture without mycelial phase. Arch Mikrobiol. 1974;95(4):305–9. 4275899.

77. That TC, Turian G. Ultrastructural study of microcyclic macroconidiation in Neurospora crassa. Arch Microbiol. 1978;116(3):279–88. doi: 10.1007/bf00417852 148251.

78. Plesofsky-Vig N, Light D, Brambl R. Paedogenetic Conidiation in Neurospora crassa. Exp Mycol. 1983;7:283–6.

79. Guignard R, Grange F, Turian G. Microcycle Conidiation Induced by Partial Nitrogen Deprivation in Neurospora crassa. Can J Microbiol. 1984;30(10):1210–5.

80. Madi L, McBride SA, Bailey LA, Ebbole DJ. rco-3, a gene involved in glucose transport and conidiation in Neurospora crassa. Genetics. 1997;146(2):499–508. 9178001.

81. Ivey FD, Kays AM, Borkovich KA. Shared and independent roles for a Galpha(i) protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryot Cell. 2002;1(4):634–42. Epub 2002/11/29. doi: 10.1128/EC.1.4.634-642.2002 12456011.

82. Metzenberg RL, Glass NL. Mating type and mating strategies in Neurospora. Bioessays. 1990;12(2):53–9. doi: 10.1002/bies.950120202 2140508.

83. Randall TA, Metzenberg RL. Species-specific and mating type-specific DNA regions adjacent to mating type idiomorphs in the genus Neurospora. Genetics. 1995;141(1):119–36. 8536961.

84. Raju NB. Neurospora as a model fungus for studies in cytogenetics and sexual biology at Stanford. J Biosci. 2009;34(1):139–59. doi: 10.1007/s12038-009-0015-5 19430125.

85. Xu BE, Kurjan J. Evidence that mating by the Saccharomyces cerevisiae gpa1Val50 mutant occurs through the default mating pathway and a suggestion of a role for ubiquitin-mediated proteolysis. Mol Biol Cell. 1997;8(9):1649–64. doi: 10.1091/mbc.8.9.1649 9307963.

86. Schauber C, Chen L, Tongaonkar P, Vega I, Madura K. Sequence elements that contribute to the degradation of yeast G alpha. Genes Cells. 1998;3(5):307–19. 9685182.

87. Sattlegger E, Hinnebusch AG, Barthelmess IB. cpc-3, the Neurospora crassa homologue of yeast GCN2, encodes a polypeptide with juxtaposed eIF2 alpha kinase and histidyl-tRNA synthetase-related domains required for general amino acid control. J Biol Chem. 1998;273(32):20404–16. doi: 10.1074/jbc.273.32.20404 9685394

88. Paluh JL, Orbach MJ, Legerton TL, Yanofsky C. The Cross-Pathway Control Gene of Neurospora-Crassa, Cpc-1, Encodes a Protein Similar to Gcn4 of Yeast and the DNA-Binding Domain of the Oncogene V-Jun-Encoded Protein. Proceedings of the National Academy of Sciences of the United States of America. 1988;85(11):3728–32. doi: 10.1073/pnas.85.11.3728 2967496

Genetic relationships between the RACK1 homolog cpc-2 and heterotrimeric G protein subunit genes in Neurospora crassa

Souhrn

Klíčová slova:

Zdroje

PLOS One

INSIGHTS from European Respiratory Congress

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií