The NDR kinase scaffold HYM1/MO25 is essential for MAK2 map kinase signaling in Neurospora crassa
Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete...
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Published in | PLoS genetics Vol. 8; no. 9; p. e1002950 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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01.09.2012
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Abstract | Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete Neurospora crassa, germinating spores mutually attract each other and subsequently fuse. During these tropic interactions, the two communicating cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. The MAK2 MAP kinase cascade mediates cell-cell signaling. Here, we show that the conserved scaffolding protein HYM1/MO25 controls the cell shape-regulating NDR kinase module as well as the signal-receiving MAP kinase cascade. HYM1 functions as an integral part of the COT1 NDR kinase complex to regulate the interaction with its upstream kinase POD6 and thereby COT1 activity. In addition, HYM1 interacts with NRC1, MEK2, and MAK2, the three kinases of the MAK2 MAP kinase cascade, and co-localizes with MAK2 at the apex of growing cells. During cell fusion, the three kinases of the MAP kinase module as well as HYM1 are recruited to the point of cell-cell contact. hym-1 mutants phenocopy all defects observed for MAK2 pathway mutants by abolishing MAK2 activity. An NRC1-MEK2 fusion protein reconstitutes MAK2 signaling in hym-1, while constitutive activation of NRC1 and MEK2 does not. These data identify HYM1 as a novel regulator of the NRC1-MEK2-MAK2 pathway, which may coordinate NDR and MAP kinase signaling during cell polarity and intercellular communication. |
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AbstractList | Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete Neurospora crassa, germinating spores mutually attract each other and subsequently fuse. During these tropic interactions, the two communicating cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. The MAK2 MAP kinase cascade mediates cell-cell signaling. Here, we show that the conserved scaffolding protein HYM1/MO25 controls the cell shape-regulating NDR kinase module as well as the signal-receiving MAP kinase cascade. HYM1 functions as an integral part of the COT1 NDR kinase complex to regulate the interaction with its upstream kinase POD6 and thereby COT1 activity. In addition, HYM1 interacts with NRC1, MEK2, and MAK2, the three kinases of the MAK2 MAP kinase cascade, and co-localizes with MAK2 at the apex of growing cells. During cell fusion, the three kinases of the MAP kinase module as well as HYM1 are recruited to the point of cell-cell contact. hym-1 mutants phenocopy all defects observed for MAK2 pathway mutants by abolishing MAK2 activity. An NRC1-MEK2 fusion protein reconstitutes MAK2 signaling in hym-1, while constitutive activation of NRC1 and MEK2 does not. These data identify HYM1 as a novel regulator of the NRC1-MEK2-MAK2 pathway, which may coordinate NDR and MAP kinase signaling during cell polarity and intercellular communication. Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete Neurospora crassa , germinating spores mutually attract each other and subsequently fuse. During these tropic interactions, the two communicating cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. The MAK2 MAP kinase cascade mediates cell–cell signaling. Here, we show that the conserved scaffolding protein HYM1/MO25 controls the cell shape-regulating NDR kinase module as well as the signal-receiving MAP kinase cascade. HYM1 functions as an integral part of the COT1 NDR kinase complex to regulate the interaction with its upstream kinase POD6 and thereby COT1 activity. In addition, HYM1 interacts with NRC1, MEK2, and MAK2, the three kinases of the MAK2 MAP kinase cascade, and co-localizes with MAK2 at the apex of growing cells. During cell fusion, the three kinases of the MAP kinase module as well as HYM1 are recruited to the point of cell–cell contact. hym-1 mutants phenocopy all defects observed for MAK2 pathway mutants by abolishing MAK2 activity. An NRC1-MEK2 fusion protein reconstitutes MAK2 signaling in hym-1 , while constitutive activation of NRC1 and MEK2 does not. These data identify HYM1 as a novel regulator of the NRC1-MEK2-MAK2 pathway, which may coordinate NDR and MAP kinase signaling during cell polarity and intercellular communication. Intercellular communication and cellular morphogenesis are essential for eukaryotic development. Our knowledge of molecules and mechanisms associated with these processes is, however, fragmentary. In particular, the molecular connection between signal sensing and regulation of cell polarity is poorly understood. Fungal hyphae share with neurons and pollen tubes the distinction of being amongst the most highly polarized cells in biology. The robust genetic tractability of filamentous fungi provides an unparalleled opportunity to determine common principles that underlie polarized growth and its regulation through cell communication. In Neurospora crassa , germinating spores mutually attract each other, establish physical contact through polarized tropic growth, and fuse. During this process, the cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. Here, we show that the conserved scaffolding protein HYM1/MO25 interacts with the polarity and cell shape-regulating NDR kinase complex as well as a MAP kinase module, which is essential for cell communication during the tropic interaction. We propose that this dual use of a common regulator in both molecular complexes may represent an intriguing mechanism of linking the perception of external cues with the polarization machinery to coordinate communication and tropic growth of interacting cells. Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete Neurospora crassa, germinating spores mutually attract each other and subsequently fuse. During these tropic interactions, the two communicating cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. The MAK2 MAP kinase cascade mediates cell-cell signaling. Here, we show that the conserved scaffolding protein HYM1/MO25 controls the cell shaperegulating NDR kinase module as well as the signal-receiving MAP kinase cascade. HYM1 functions as an integral part of the COT1 NDR kinase complex to regulate the interaction with its upstream kinase POD6 and thereby COT1 activity. in addition, HYM1 interacts with NRC1, MEK2, and MAK2, the three kinases of the MAK2 MAP kinase cascade, and co-localizes with MAK2 at the apex of growing cells. During cell fusion, the three kinases of the MAP kinase module as well as HYM1 are recruited to the point of cell-cell contact. hym-1 mutants phenocopy all defects observed for MAK2 pathway mutants by abolishing MAK2 activity. An NRC1-MEK2 fusion protein reconstitutes MAK2 signaling in hym-1, while constitutive activation of NRC1 and MEK2 does not. These data identify HYM1 as a novel regulator of the NRC1-MEK2-MAK2 pathway, which may coordinate NDR and MAP kinase signaling during cell polarity and intercellular communication. Cell communication is essential for eukaryotic development, but our knowledge of molecules and mechanisms required for intercellular communication is fragmentary. In particular, the connection between signal sensing and regulation of cell polarity is poorly understood. In the filamentous ascomycete Neurospora crassa, germinating spores mutually attract each other and subsequently fuse. During these tropic interactions, the two communicating cells rapidly alternate between two different physiological states, probably associated with signal delivery and response. The MAK2 MAP kinase cascade mediates cell-cell signaling. Here, we show that the conserved scaffolding protein HYM1/MO25 controls the cell shape-regulating NDR kinase module as well as the signal-receiving MAP kinase cascade. HYM1 functions as an integral part of the COT1 NDR kinase complex to regulate the interaction with its upstream kinase POD6 and thereby COT1 activity. In addition, HYM1 interacts with NRC1, MEK2, and MAK2, the three kinases of the MAK2 MAP kinase cascade, and co-localizes with MAK2 at the apex of growing cells. During cell fusion, the three kinases of the MAP kinase module as well as HYM1 are recruited to the point of cell-cell contact. hym-1 mutants phenocopy all defects observed for MAK2 pathway mutants by abolishing MAK2 activity. An NRC1-MEK2 fusion protein reconstitutes MAK2 signaling in hym-1, while constitutive activation of NRC1 and MEK2 does not. These data identify HYM1 as a novel regulator of the NRC1-MEK2-MAK2 pathway, which may coordinate NDR and MAP kinase signaling during cell polarity and intercellular communication. |
Audience | Academic |
Author | Illgen, Julia Schürg, Timo Fleissner, Andre Dettmann, Anne Seiler, Stephan März, Sabine |
AuthorAffiliation | Duke University Medical Center, United States of America 1 Institute for Microbiology and Genetics, University of Goettingen, Goettingen, Germany 2 Institute for Genetics, Technische Universität Braunschweig, Braunschweig, Germany |
AuthorAffiliation_xml | – name: 2 Institute for Genetics, Technische Universität Braunschweig, Braunschweig, Germany – name: Duke University Medical Center, United States of America – name: 1 Institute for Microbiology and Genetics, University of Goettingen, Goettingen, Germany |
Author_xml | – sequence: 1 givenname: Anne surname: Dettmann fullname: Dettmann, Anne organization: Institute for Microbiology and Genetics, University of Goettingen, Goettingen, Germany – sequence: 2 givenname: Julia surname: Illgen fullname: Illgen, Julia – sequence: 3 givenname: Sabine surname: März fullname: März, Sabine – sequence: 4 givenname: Timo surname: Schürg fullname: Schürg, Timo – sequence: 5 givenname: Andre surname: Fleissner fullname: Fleissner, Andre – sequence: 6 givenname: Stephan surname: Seiler fullname: Seiler, Stephan |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23028357$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2012 Public Library of Science Dettmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dettmann A, Illgen J, März S, Schürg T, Fleissner A, et al. (2012) The NDR Kinase Scaffold HYM1/MO25 Is Essential for MAK2 MAP Kinase Signaling in Neurospora crassa. PLoS Genet 8(9): e1002950. doi:10.1371/journal.pgen.1002950 2012 Dettmann et al 2012 Dettmann et al |
Copyright_xml | – notice: COPYRIGHT 2012 Public Library of Science – notice: Dettmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dettmann A, Illgen J, März S, Schürg T, Fleissner A, et al. (2012) The NDR Kinase Scaffold HYM1/MO25 Is Essential for MAK2 MAP Kinase Signaling in Neurospora crassa. PLoS Genet 8(9): e1002950. doi:10.1371/journal.pgen.1002950 – notice: 2012 Dettmann et al 2012 Dettmann et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: SS AF. Performed the experiments: AD JI SM TS. Analyzed the data: AD JI SM TS AF SS. Wrote the paper: AF SS. The authors have declared that no competing interests exist. |
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SubjectTerms | Amino Acid Sequence Biology Carrier Proteins - genetics Cation Transport Proteins - metabolism Cell Communication - genetics Cell Communication - physiology Cell cycle Cell Cycle Proteins - metabolism Cell interaction Cell Polarity Cell Shape Enzymes Fungal Proteins - genetics Fungal Proteins - metabolism Genetic aspects Health aspects Histidine Kinase Kinases MAP Kinase Signaling System Microbial genetics Mitogen-activated protein kinases Neurospora Neurospora crassa - genetics Neurospora crassa - metabolism Pheromones Phosphorylation Physiological aspects Plasma Protein Kinases - genetics Protein Kinases - metabolism Protein-Serine-Threonine Kinases - genetics Protein-Serine-Threonine Kinases - metabolism Protein-Serine-Threonine Kinases - physiology Proteins Spores - genetics Spores - growth & development Spores - metabolism Yeast |
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Title | The NDR kinase scaffold HYM1/MO25 is essential for MAK2 map kinase signaling in Neurospora crassa |
URI | https://www.ncbi.nlm.nih.gov/pubmed/23028357 https://www.proquest.com/docview/1313532054/abstract/ https://search.proquest.com/docview/1082405977 https://pubmed.ncbi.nlm.nih.gov/PMC3447951 https://doaj.org/article/0f612f2c6c9e4980bb47467538f17b79 http://dx.doi.org/10.1371/journal.pgen.1002950 |
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