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Regulation of Protein Phosphatase 4 by a MAP Kinase Cascade Controls Chemotaxis

ABSTRACT: Classical genetics in model organisms has defined many signaling pathways that control cell movement and multicellular morphogenesis. However,these approaches have not succeeded in placing some established chemotaxis regulators, such as the MAP kinase kinase MEK1, in activator/effector pathways. Here, we combined morphological measurements with epistasis analysis of transcriptional phenotypes and found that the protein phosphatase 4 (PP4) signaling pathway controls Dictyostelium chemotaxis and development. PP4 is a phosphatase that regulates recovery from DNA damage. We show that Dictyostelium SMEK functions as the PP4R3 regulatory subunit and may regulate the subcellular localization of PP4 catalytic subunit PP4C. SMEK binds PP4C and the complex functions downstream of MEK1 to regulate chemotaxis and morphogenesis. Microarray analysis of gene expression in mutant strains indicated that PP4 controls leading edge formation and cellular responses to stress. Thus, the MEKPP4C/SMEK pathway has a direct role in regulating chemotaxis, in addition to regulating the DNA repair checkpoint. Keywords: Developmental time course series from 1 Dictyostelium wildtype and 5 chemotaxis mutants to determine epistatic relationship

ORGANISM(S): Dictyostelium discoideum

PROVIDER: GSE5597 | GEO | 2006/08/25

SECONDARY ACCESSION(S): PRJNA96885

REPOSITORIES: GEO

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Project description:Chemotaxis is used by free-living motile bacteria to swim towards nutrient sources or away from repellents, and to navigate the environment to locate niches optimal for growth and survival. Multiple chemotaxis systems have been identified in different bacterial species, including Azospirillum brasilense. In A. brasilense, chemotaxis is mediated by two distinct chemotaxis pathways, named Che1 and Che4, that physically interact to form mixed chemotaxis signaling arrays. Signaling from the Che1 and Che4 pathways control transient increases in swimming speed and swimming reversals, respectively, during chemotaxis. In A. brasilense, chemotaxis is tightly linked to energy metabolism with this coupling occurring through the sensory input of several energy-sensing chemoreceptors and through the control of chemoreceptor activity by the c-di-GMP second messenger. Previous work has demonstrated that chemotaxis in A. brasilense also affects unrelated cellular functions including cell-to-cell clumping and flocculation. However, the molecular mechanism for these effects is not known. Here, we identify additional effects of mutations abolishing Che1 (cheA1 mutant), Che4 (cheA4 mutant) or both Che1 and Che4 (cheA1/cheA4 mutant) function on nitrogen and carbon metabolism and use whole cell proteome and metabolome mass spectrometry to further characterize the interplay between chemotaxis and metabolism. We found that CheA1 mediates most changes in chemoreceptor arrays composition and also affects small molecules signaling while a mutant lacking CheA4 displays changes in nitrogen metabolism, including nitrate assimilation and nitrogen fixation. In contrast, the mutant lacking both CheA1 and CheA4, which lacks chemotaxis and does not form chemotaxis signaling arrays, displays distinct and non-overlapping changes that suggest the assembly of chemotaxis signaling arrays modulates energy and carbon metabolism. Together, the results suggest distinct roles for CheA1, CheA4 and chemotaxis signaling arrays in modulating chemotaxis and metabolism, likely through control of distinct global regulatory networks.

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Regulation of Protein Phosphatase 4 by a MAP Kinase Cascade Controls Chemotaxis

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