PaASK1, a mitogen-activated protein kinase kinase kinase that controls cell degeneration and cell differentiation in Podospora anserina (original) (raw)
Abstract
MAPKKK are kinases involved in cell signaling. In fungi, these kinases are known to regulate development, pathogenicity, and the sensing of external conditions. We show here that Podospora anserina strains mutated in PaASK1, a MAPKKK of the MEK family, are impaired in the development of crippled growth, a cell degeneration process caused by C, a nonconventional infectious element. They also display defects in mycelium pigmentation, differentiation of aerial hyphae, and making of fruiting bodies, three hallmarks of cell differentiation during stationary phase in P. anserina. Overexpression of PaASK1 results in exacerbation of crippled growth. PaASK1 is a large protein of 1832 amino acids with several domains, including a region rich in proline and a 60-amino-acid-long polyglutamine stretch. Deletion analysis reveals that the polyglutamine stretch is dispensable for PaASK1 activity, whereas the region that contains the prolines is essential but insufficient to promote full activity. We discuss a model based on the hysteresis of a signal transduction cascade to account for the role of PaASK1 in both cell degeneration and stationary-phase cell differentiation.
Full Text
The Full Text of this article is available as a PDF (419.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Alessi M. C., Declerck P. J., De Mol M., Nelles L., Collen D. Purification and characterization of natural and recombinant human plasminogen activator inhibitor-1 (PAI-1). Eur J Biochem. 1988 Aug 15;175(3):531–540. doi: 10.1111/j.1432-1033.1988.tb14225.x. [DOI] [PubMed] [Google Scholar]
- Bagowski C. P., Ferrell J. E., Jr Bistability in the JNK cascade. Curr Biol. 2001 Aug 7;11(15):1176–1182. doi: 10.1016/s0960-9822(01)00330-x. [DOI] [PubMed] [Google Scholar]
- Belcour L., Rossignol M., Koll F., Sellem C. H., Oldani C. Plasticity of the mitochondrial genome in Podospora. Polymorphism for 15 optional sequences: group-I, group-II introns, intronic ORFs and an intergenic region. Curr Genet. 1997 Apr;31(4):308–317. doi: 10.1007/s002940050210. [DOI] [PubMed] [Google Scholar]
- Bhalla U. S., Iyengar R. Emergent properties of networks of biological signaling pathways. Science. 1999 Jan 15;283(5400):381–387. doi: 10.1126/science.283.5400.381. [DOI] [PubMed] [Google Scholar]
- Bhalla Upinder S., Ram Prahlad T., Iyengar Ravi. MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science. 2002 Aug 9;297(5583):1018–1023. doi: 10.1126/science.1068873. [DOI] [PubMed] [Google Scholar]
- Bussink H. J., Osmani S. A. A mitogen-activated protein kinase (MPKA) is involved in polarized growth in the filamentous fungus, Aspergillus nidulans. FEMS Microbiol Lett. 1999 Apr 1;173(1):117–125. doi: 10.1111/j.1574-6968.1999.tb13492.x. [DOI] [PubMed] [Google Scholar]
- Clemons K. V., Hanson L. C., Stevens D. A. Colony phenotype switching in clinical and non-clinical isolates of Saccharomyces cerevisiae. J Med Vet Mycol. 1996 Jul-Aug;34(4):259–264. doi: 10.1080/02681219680000441. [DOI] [PubMed] [Google Scholar]
- DePace A. H., Santoso A., Hillner P., Weissman J. S. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell. 1998 Jun 26;93(7):1241–1252. doi: 10.1016/s0092-8674(00)81467-1. [DOI] [PubMed] [Google Scholar]
- Dequard-Chablat M., Coppin-Raynal E., Picard-Bennoun M., Madjar J. J. At least seven ribosomal proteins are involved in the control of translational accuracy in a eukaryotic organism. J Mol Biol. 1986 Jul 20;190(2):167–175. doi: 10.1016/0022-2836(86)90290-1. [DOI] [PubMed] [Google Scholar]
- Ferrell James E., Jr Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol. 2002 Apr;14(2):140–148. doi: 10.1016/s0955-0674(02)00314-9. [DOI] [PubMed] [Google Scholar]
- Fries Bettina C., Goldman David L., Casadevall Arturo. Phenotypic switching in Cryptococcus neoformans. Microbes Infect. 2002 Nov;4(13):1345–1352. doi: 10.1016/s1286-4579(02)00006-0. [DOI] [PubMed] [Google Scholar]
- Harrison J. C., Bardes E. S., Ohya Y., Lew D. J. A role for the Pkc1p/Mpk1p kinase cascade in the morphogenesis checkpoint. Nat Cell Biol. 2001 Apr;3(4):417–420. doi: 10.1038/35070104. [DOI] [PubMed] [Google Scholar]
- Heinisch J. J., Lorberg A., Schmitz H. P., Jacoby J. J. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol Microbiol. 1999 May;32(4):671–680. doi: 10.1046/j.1365-2958.1999.01375.x. [DOI] [PubMed] [Google Scholar]
- Hou Zhanming, Xue Chaoyang, Peng Youliang, Katan Talma, Kistler H. Corby, Xu Jin-Rong. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact. 2002 Nov;15(11):1119–1127. doi: 10.1094/MPMI.2002.15.11.1119. [DOI] [PubMed] [Google Scholar]
- Huang C. Y., Ferrell J. E., Jr Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10078–10083. doi: 10.1073/pnas.93.19.10078. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ichijo H., Nishida E., Irie K., ten Dijke P., Saitoh M., Moriguchi T., Takagi M., Matsumoto K., Miyazono K., Gotoh Y. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science. 1997 Jan 3;275(5296):90–94. doi: 10.1126/science.275.5296.90. [DOI] [PubMed] [Google Scholar]
- Kuthan Martin, Devaux Frédéric, Janderová Blanka, Slaninová Iva, Jacq Claude, Palková Zdena. Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Mol Microbiol. 2003 Feb;47(3):745–754. doi: 10.1046/j.1365-2958.2003.03332.x. [DOI] [PubMed] [Google Scholar]
- Lachke Salil A., Joly Sophie, Daniels Karla, Soll David R. Phenotypic switching and filamentation in Candida glabrata. Microbiology. 2002 Sep;148(Pt 9):2661–2674. doi: 10.1099/00221287-148-9-2661. [DOI] [PubMed] [Google Scholar]
- Lockshon Daniel. A heritable structural alteration of the yeast mitochondrion. Genetics. 2002 Aug;161(4):1425–1435. doi: 10.1093/genetics/161.4.1425. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mey Géraldine, Held Katrin, Scheffer Jan, Tenberge Klaus B., Tudzynski Paul. CPMK2, an SLT2-homologous mitogen-activated protein (MAP) kinase, is essential for pathogenesis of Claviceps purpurea on rye: evidence for a second conserved pathogenesis-related MAP kinase cascade in phytopathogenic fungi. Mol Microbiol. 2002 Oct;46(2):305–318. doi: 10.1046/j.1365-2958.2002.03133.x. [DOI] [PubMed] [Google Scholar]
- Picard-Bennoun M. Genetic evidence of ribosomal antisuppressors in Podospora anserina. Mol Gen Genet. 1976 Sep 23;147(3):299–306. doi: 10.1007/BF00582881. [DOI] [PubMed] [Google Scholar]
- Picard M. Genetic evidences for a polycistronic unit of transcription in the complex locus "14" in Podospora anserina. I. Genetic and complementation maps. Mol Gen Genet. 1971;111(1):35–50. doi: 10.1007/BF00286552. [DOI] [PubMed] [Google Scholar]
- Sha Wei, Moore Jonathan, Chen Katherine, Lassaletta Antonio D., Yi Chung-Seon, Tyson John J., Sible Jill C. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc Natl Acad Sci U S A. 2002 Dec 30;100(3):975–980. doi: 10.1073/pnas.0235349100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silar P., Daboussi M. J. Non-conventional infectious elements in filamentous fungi. Trends Genet. 1999 Apr;15(4):141–145. doi: 10.1016/s0168-9525(99)01698-4. [DOI] [PubMed] [Google Scholar]
- Silar P., Haedens V., Rossignol M., Lalucque H. Propagation of a novel cytoplasmic, infectious and deleterious determinant is controlled by translational accuracy in Podospora anserina. Genetics. 1999 Jan;151(1):87–95. doi: 10.1093/genetics/151.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silar P., Picard M. Increased longevity of EF-1 alpha high-fidelity mutants in Podospora anserina. J Mol Biol. 1994 Jan 7;235(1):231–236. doi: 10.1016/s0022-2836(05)80029-4. [DOI] [PubMed] [Google Scholar]
- Soll David R. Candida commensalism and virulence: the evolution of phenotypic plasticity. Acta Trop. 2002 Feb;81(2):101–110. doi: 10.1016/s0001-706x(01)00200-5. [DOI] [PubMed] [Google Scholar]
- True H. L., Lindquist S. L. A yeast prion provides a mechanism for genetic variation and phenotypic diversity. Nature. 2000 Sep 28;407(6803):477–483. doi: 10.1038/35035005. [DOI] [PubMed] [Google Scholar]
- Uptain Susan M., Lindquist Susan. Prions as protein-based genetic elements. Annu Rev Microbiol. 2002 Jan 30;56:703–741. doi: 10.1146/annurev.micro.56.013002.100603. [DOI] [PubMed] [Google Scholar]
- Wickner R. B. [URE3] as an altered URE2 protein: evidence for a prion analog in Saccharomyces cerevisiae. Science. 1994 Apr 22;264(5158):566–569. doi: 10.1126/science.7909170. [DOI] [PubMed] [Google Scholar]
- Widmann C., Gibson S., Jarpe M. B., Johnson G. L. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev. 1999 Jan;79(1):143–180. doi: 10.1152/physrev.1999.79.1.143. [DOI] [PubMed] [Google Scholar]
- Xu J. R., Staiger C. J., Hamer J. E. 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 U S A. 1998 Oct 13;95(21):12713–12718. doi: 10.1073/pnas.95.21.12713. [DOI] [PMC free article] [PubMed] [Google Scholar]