Functional equivalence of HMGA- and histone H1-like domains in a bacterial transcriptional factor
- 11 August 2009
- journal article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 106 (32), 13546-13551
- https://doi.org/10.1073/pnas.0902233106
Abstract
Histone H1 and high-mobility group A (HMGA) proteins compete dynamically to modulate chromatin structure and regulate DNA transactions in eukaryotes. In prokaryotes, HMGA-like domains are known only in Myxococcus xanthus CarD and its Stigmatella aurantiaca ortholog. These have an N-terminal module absent in HMGA that interacts with CarG (a zinc-associated factor that does not bind DNA) to form a stable complex essential in regulating multicellular development, light-induced carotenogenesis, and other cellular processes. An analogous pair, CarD(Ad) and CarG(Ad), exists in another myxobacterium, Anaeromyxobacter dehalogenans. Intriguingly, the CarD(Ad) C terminus lacks the hallmark HMGA DNA-binding AT-hooks and instead resembles the C-terminal region (CTR) of histone H1. We find that CarD(Ad) alone could not replace CarD in M. xanthus. By contrast, when introduced with CarG(Ad), CarD(Ad) functionally replaced CarD in regulating not just 1 but 3 distinct processes in M. xanthus, despite the lower DNA-binding affinity of CarD(Ad) versus CarD in vitro. The ability of the cognate CarD(Ad)-CarG(Ad) pair to interact, but not the noncognate CarD(Ad)-CarG, rationalizes these data. Thus, in chimeras that conserve CarD-CarG interactions, the H1-like CTR of CarD(Ad) could replace the CarD HMGA AT-hooks with no loss of function in vivo. More tellingly, even chimeras with the CarD AT-hook region substituted by human histone H1 CTR or full-length H1 functioned in M. xanthus. Our domain-swap analyses showing functional equivalence of HMGA AT-hooks and H1 CTR in prokaryotic transcriptional regulation provide molecular insights into possible modes of action underlying their biological roles.Keywords
This publication has 45 references indexed in Scilit:
- The Mosaic Genome of Anaeromyxobacter dehalogenans Strain 2CP-C Suggests an Aerobic Common Ancestor to the Delta-ProteobacteriaPLOS ONE, 2008
- Evolution of sensory complexity recorded in a myxobacterial genomeProceedings of the National Academy of Sciences of the United States of America, 2006
- Intrinsic Protein Disorder, Amino Acid Composition, and Histone Terminal DomainsJournal of Biological Chemistry, 2006
- Energetics of Binding the Mammalian High Mobility Group Protein HMGA2 to poly(dA-dT)2 and poly(dA)-poly(dT)Journal of Molecular Biology, 2005
- Intrinsically unstructured proteins and their functionsNature Reviews Molecular Cell Biology, 2005
- The High-Mobility Group A-Type Protein CarD of the Bacterium Myxococcus xanthus as a Transcription Factor for Several Distinct Vegetative GenesSequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AJ505751, AJ505752, AJ505753, and AJ505849.Genetics, 2004
- Domain Architecture of a High Mobility Group A-type Bacterial Transcriptional FactorPublished by Elsevier BV ,2001
- Genetic Engineering of Single-Chain Gonadotropins and Hormone–Receptor Fusion ProteinsMethods, 2000
- A genetic link between light response and multicellular development in the bacterium Myxococcus xanthus.Genes & Development, 1994
- Close encounters: why unstructured, polymeric domains can increase rates of specific macromolecular associationTrends in Biochemical Sciences, 1993