HAM-5 Functions As a MAP Kinase Scaffold during Cell Fusion in

English version České info

Cell fusion between genetically identical cells of the fungus Neurospora crassa occurs when germinating asexual cells (conidia) sense each other's proximity and redirect their growth. Chemotropic growth is dependent upon the assembly of a MAPK cascade (NRC-1/MEK-2/MAK-2) at the cell cortex (conidial anastomosis tubes; CATs), followed by disassembly over an ∼8 min cycle. A second protein required for fusion, SO, also assembles and disassembles at CAT tips during chemotropic growth, but with perfectly opposite dynamics to the MAK-2 complex. This process of germling chemotropism, oscillation and cell fusion is regulated by many genes and is poorly understood. Via a phosphoproteomics approach, we identify HAM-5, which functions as a scaffold for the MAK-2 signal transduction complex. HAM-5 is required for assembly/disassembly and oscillation of the MAK-2 complex during chemotropic growth. Our data supports a model whereby regulated modification of HAM-5 controls the disassembly of the MAK-2 MAPK complex and is essential for modulating the tempo of oscillation during chemotropic interactions.

Vyšlo v časopise: HAM-5 Functions As a MAP Kinase Scaffold during Cell Fusion in. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004783
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004783

Souhrn

Zdroje

1. AguilarPS, BayliesMK, FleissnerA, HelmingL, InoueN, et al. (2013) Genetic basis of cell-cell fusion mechanisms. Trends Genet 29: 427–437.

2. ChenEH, OlsonEN (2005) Unveiling the mechanisms of cell-cell fusion. Science 308: 369–373.

3. Fricker MD, Boddy L, Bebber D (2007) Network organization of filamentous fungi. In: Howard, R and Gow, N. A R, Eds. Biology of the Fungal Cell. Berlin: Springer-Verlag. pp.309-330.

4. Rayner ADM (1996) Interconnectedness and individualism in fungal mycelia; Sutton BC, editor. Cambridge: Cambridge University Press. pp.193-232.

5. GlassNL, RasmussenC, RocaMG, ReadND (2004) Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12: 135–141.

6. Roca GM, Read ND, Wheals AE (2005) Conidial anastomosis tubes in filamentous fungi. FEMS Microbio Letts 249: : 191-198.

7. Read ND, Fleißner A, Roca MG, Glass NL (2010) Hyphal Fusion. In: Borkovich, K.A and Ebbole, D., Eds. Cellular and Molecular Biology of Filamentous Fungi. Washington, D.C. ASM Press. pp.260-273.

8. PandeyA, RocaMG, ReadND, GlassNL (2004) Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3: 348–358.

9. SimoninA, Palma-GuerreroJ, FrickerM, GlassNL (2012) Physiological significance of network organization in fungi. Eukaryot Cell 11: 1345–1352.

10. RoperM, SimoninA, HickeyPC, LeederA, GlassNL (2013) Nuclear dynamics in a fungal chimera. Proc Natl Acad Sci U S 110: 12875–12880.

11. RichardF, GlassNL, PringleA (2012) Cooperation among germinating spores facilitates the growth of the fungus, Neurospora crassa. Biol Lett 8: 419–422.

12. CharltonND, ShojiJY, GhimireSR, NakashimaJ, CravenKD (2012) Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte Epichloe festucae and the host plant. Eukaryot Cell 11: 1463–1471.

13. TanakaA, CartwrightGM, SaikiaS, KayanoY, TakemotoD, et al. (2013) ProA, a transcriptional regulator of fungal fruiting body development, regulates leaf hyphal network development in the Epichloe festucae-Lolium perenne symbiosis. Mol Microbiol 90: 551–568.

14. RocaM, ArltJ, JeffreeC, ReadN (2005) Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4: 911–919.

15. ReadND, LichiusA, ShojiJY, GoryachevAB (2009) Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12: 608–615.

16. IshikawaFH, SouzaEA, ShojiJY, ConnollyL, FreitagM, et al. (2012) Heterokaryon incompatibility is suppressed following conidial anastomosis tube fusion in a fungal plant pathogen. PLoS One 7: e31175.

17. FleissnerA, SimoninAR, GlassNL (2008) Cell fusion in the filamentous fungus, Neurospora crassa. Methods Mol Biol 475: 21–38.

18. DettmannA, IllgenJ, MarzS, SchurgT, FleissnerA, et al. (2012) The NDR kinase scaffold HYM1/MO25 is essential for MAK-2 map kinase signaling in Neurospora crassa. PLoS Genet 8: e1002950.

19. FleissnerA, LeederAC, RocaMG, ReadND, GlassNL (2009) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci USA 106: 19387–19392.

20. FleissnerA, GlassNL (2007) SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6: 84–94.

21. GoryachevAB, LichiusA, WrightGD, ReadND (2012) Excitable behavior can explain the "ping-pong" mode of communication between cells using the same chemoattractant. Bioessays 34: 259–266.

22. TeichertI, SteffensEK, SchnabN, FranzelB, KrispC, et al. (2014) PRO40 is a scaffold protein of the cell wall integrity pathway, linking the MAP kinase module to the upstream activator protein kinase C. PLoS Genet 10: e1004582.

23. FuC, IyerP, HerkalA, AbdullahJ, StoutA, et al. (2011) Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10: 1100–1109.

24. LeederAC, JonkersW, LiJ, GlassNL (2013) Germination and early colony establishment in Neurospora crassa requires a MAP kinase regulatory network. Genetics 195: 883–898.

25. KosakoH, NaganoK (2011) Quantitative phosphoproteomics strategies for understanding protein kinase-mediated signal transduction pathways. Expert Rev Proteomics 8: 81–94.

26. WangY, DingSJ, WangW, JacobsJM, QianWJ, et al. (2007) Profiling signaling polarity in chemotactic cells. Proc Natl Acad Sci USA 104: 8328–8333.

27. KirkpatrickDS, BustosDJ, DoganT, ChanJ, PhuL, et al. (2013) Phosphoproteomic characterization of DNA damage response in melanoma cells following MEK/PI3K dual inhibition. Proc Natl Acad Sci USA 110: 19426–19431.

28. MertinsP, YangF, LiuT, ManiDR, PetyukVA, et al. (2014) Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol Cell Proteomics 13: 1690–1704.

29. AldabbousMS, RocaMG, StoutA, HuangIC, ReadND, et al. (2010) The ham-5, rcm-1 and rco-1 genes regulate hyphal fusion in Neurospora crassa. Microbiol 156: 2621–2629.

30. RueppA, ZollnerA, MaierD, AlbermannK, HaniJ, et al. (2004) The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucl Acids Res 32: 5539–5545.

31. MaerzS, ZivC, VogtN, HelmstaedtK, CohenN, et al. (2008) The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK-1 and MAK-2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179: 1313–1325.

32. ZhangY, LammR, PillonelC, LamS, XuJR (2002) Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Appl Environ Microbiol 68: 532–538.

33. YoussarL, SchmidhauserTJ, AvalosJ (2005) The Neurospora crassa gene responsible for the cut and ovc phenotypes encodes a protein of the haloacid dehalogenase family. Mol Microbiol 55: 828–838.

34. FujimuraM, OchiaiN, OshimaM, MotoyamaT, IchiishiA, et al. (2003) Putative homologs of SSK22 MAPKK kinase and PBS2 MAPK kinase of Saccharomyces cerevisiae encoded by os-4 and os-5 genes for osmotic sensitivity and fungicide resistance in Neurospora crassa. Biosci Biotechnol Biochem 67: 186–191.

35. YamashitaK, ShiozawaA, WatanabeS, FukumoriF, KimuraM, et al. (2008) ATF-1 transcription factor regulates the expression of ccg-1 and cat-1 genes in response to fludioxonil under OS-2 MAP kinase in Neurospora crassa. Fungal Genet Biol 45: 1562–1569.

36. MokJ, KimPM, LamHY, PiccirilloS, ZhouX, et al. (2010) Deciphering protein kinase specificity through large-scale analysis of yeast phosphorylation site motifs. Science Signaling 3: ra12.

37. ParnellSC, MarottiLAJr, KiangL, TorresMP, BorchersCH, et al. (2005) Phosphorylation of the RGS protein Sst2 by the MAP kinase Fus3 and use of Sst2 as a model to analyze determinants of substrate sequence specificity. Biochem 44: 8159–8166.

38. LiD, BobrowiczP, WilkinsonHH, EbboleDJ (2005) A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170: 1091–1104.

39. RemenyiA, GoodMC, BhattacharyyaRP, LimWA (2005) The role of docking interactions in mediating signaling input, output, and discrimination in the yeast MAPK network. Mol Cell 20: 951–962.

40. XiongY, CoradettiST, LiX, GritsenkoMA, ClaussT, et al. (2014) The proteome and phosphoproteome of Neurospora crassa in response to cellulose, sucrose and carbon starvation. Fungal Genet Biol S1087-1845(14)00083-8.

41. XuC, MinJ (2011) Structure and function of WD40 domain proteins. Protein & Cell 2: 202–214.

42. GoodMC, ZalatanJG, LimWA (2011) Scaffold proteins: hubs for controlling the flow of cellular information. Science 332: 680–686.

43. MaddiA, DettmanA, FuC, SeilerS, FreeSJ (2012) WSC-1 and HAM-7 are MAK-1 MAP kinase pathway sensors required for cell wall integrity and hyphal fusion in Neurospora crassa. PLoS ONE 7: e42374.

44. LeederAC, Palma-GuerreroJ, GlassNL (2011) The social network: deciphering fungal language. Nat Rev Microbiol 9: 440–451.

45. HickeyPC, JacobsonD, ReadND, Louise GlassNL (2002) Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet Biol 37: 109–119.

46. DettmannA, HeiligY, ValeriusO, LudwigS, SeilerS (2014) Fungal communication requires the MAK-2 pathway elements STE-20, RAS-2, the NRC-1 adapter STE-50 and the MAP kinase scaffold HAM-5. PLoS Genet 10: e1004762.

47. HouZ, XueC, PengY, KatanT, KistlerHC, et al. (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15: 1119–1127.

48. Di PietroA, Garcia-MacEiraFI, MegleczE, RonceroMIG (2001) A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol Microbiol 39: 1140–1152.

49. BayramO, BayramOS, AhmedYL, MaruyamaJ, ValeriusO, et al. (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8: e1002816.

50. Ruiz-RoldanMC, KohliM, RonceroMI, PhilippsenP, Di PietroA, et al. (2010) Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum. Eukaryot Cell 9: 1216–1224.

51. Jamet-ViernyC, DebuchyR, PrigentM, SilarP (2007) IDC1, a pezizomycotina-specific gene that belongs to the PaMpk1 MAP kinase transduction cascade of the filamentous fungus Podospora anserina. Fungal Genet Biol 44: 1219–1230.

52. XuJR, StaigerCJ, HamerJE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc Natl Acad Sci USA 95: 12713–12718.

53. LevS, SharonA, HadarR, MaH, HorwitzBA (1999) A mitogen-activated protein kinase of the corn leaf pathogen Cochliobolus heterostrophus is involved in conidiation, appressorium formation, and pathogenicity: diverse roles for mitogen-activated protein kinase homologs in foliar pathogens. Proc Natl Acad Sci USA 96: 13542–13547.

54. ZhengL, CampbellM, MurphyJ, LamS, XuJR (2000) The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol Plant-Microbe Interact 13: 724–732.

55. KojimaK, KikuchiT, TakanoY, OshiroE, OkunoT (2002) The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Mol Plant Microbe Interact 15: 1268–1276.

56. LengelerKB, DavidsonRC, D'SouzaC, HarashimaT, ShenW-C, et al. (2000) Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64: 746–785.

57. XuJR, HamerJE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Devel 10: 2696–2706.

58. CoyleSM, FloresJ, LimWA (2013) Exploitation of latent allostery enables the evolution of new modes of MAP kinase regulation. Cell 154: 875–887.

59. BhattacharyyaRP, RemenyiA, GoodMC, BashorCJ, FalickAM, et al. (2006) The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway. Science 311: 822–826.

60. StrickfadenSC, WintersMJ, Ben-AriG, LamsonRE, TyersM, et al. (2007) A mechanism for cell-cycle regulation of MAP kinase signaling in a yeast differentiation pathway. Cell 128: 519–531.

61. WonS, MichkovAV, KrystofovaS, GarudAV, BorkovichKA (2012) Genetic and physical interactions between Galpha subunits and components of the Gbetagamma dimer of heterotrimeric G proteins in Neurospora crassa. Eukaryot Cell 11: 1239–1248.

62. EatonCJ, CabreraIE, ServinJA, WrightSJ, CoxMP, et al. (2012) The guanine nucleotide exchange factor RIC8 regulates conidial germination through Galpha proteins in Neurospora crassa. PLoS One 7: e48026.

63. LeeuwT, Fourest-LieuvinA, WuC, ChenevertJ, ClarkK, et al. (1995) Pheromone response in yeast: association of Bem1p with proteins of the MAP kinase cascade and actin. Science 270: 1210–1213.

64. LichiusA, GoryachevAB, FrickerMD, ObaraB, Castro-LongoriaE, et al. (2014) CDC-42 and RAC-1 regulate opposite chemotropisms in Neurospora crassa. J Cell Sci 127: 1953–1965.

65. Palma-GuerreroJ, LeederAC, WelchJ, GlassNL (2014) Identification and characterization of LFD1, a novel protein involved in membrane merger during cell fusion in Neurospora crassa. Mol Microbiol 92: 164–182.

66. DettmannA, HeiligY, LudwigS, SchmittK, IllgenJ, et al. (2013) HAM-2 and HAM-3 are central for the assembly of the Neurospora STRIPAK complex at the nuclear envelope and regulate nuclear accumulation of the MAP kinase MAK-1 in a MAK-2-dependent manner. Mol Microbiol 90: 796–812.

67. VogelHJ (1956) A convenient growth medium for Neurospora. Microbiol Genet Bull 13: 42–46.

68. WestergaardM, MitchellHK (1947) Neurospora V. A synthetic medium favoring sexual reproduction. Amer J Bot 34: 573–577.

69. ColotHV, ParkG, TurnerGE, RingelbergC, CrewCM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103: 10352–10357.

70. MargolinBS, FreitagM, SelkerEU (1997) Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa by electroporation. Fungal Genet Newslett 44: 34–36.

71. FreitagM, HickeyPC, RajuNB, SelkerEU, ReadND (2004) GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet Biol 41: 897–910.

72. Castro-LongoriaE, FerryM, Bartnicki-GarciaS, HastyJ, BrodyS (2010) Circadian rhythms in Neurospora crassa: dynamics of the clock component frequency visualized using a fluorescent reporter. Fungal Genet Biol 47: 332–341.

73. PanditA, MaheshwariR (1994) A simple method of obtaining pure microconidia in Neurospora crassa. Fungal Genet Newsl 41: 64–65.

74. McCluskeyK (2003) The Fungal Genetics Stock Center: from molds to molecules. Adv Appl Microbiol 52: 245–262.

75. DunlapJC, BorkovichKA, HennMR, TurnerGE, SachsMS, et al. (2007) Enabling a community to dissect an organism: Overview of the Neurospora functional genomics project. Adv Genet 57: 49–96.

76. NguyenTH, BrechenmacherL, AldrichJT, ClaussTR, GritsenkoMA, et al. (2012) Quantitative phosphoproteomic analysis of soybean root hairs inoculated with Bradyrhizobium japonicum. Mol Cell Proteomics 11: 1140–1155.

77. EngJK, McCormackAL, YatesJR (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Amer Soc Mass Spectrometry 5: 976–989.

78. KimS, GuptaN, PevznerPA (2008) Spectral probabilities and generating functions of tandem mass spectra: a strike against decoy databases. J Proteome Res 7: 3354–3363.

79. MonroeME, ShawJL, DalyDS, AdkinsJN, SmithRD (2008) MASIC: a software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC-MS(/MS) features. Comp Biol Chem 32: 215–217.