Evolution of an ancient protein function involved in organized multicellularity in animals
| Autor: | William Campodonico-Burnett, Joseph W. Thornton, Nicole King, Douglas P Anderson, Brian F. Volkman, Kenneth E. Prehoda, Dustin S. Whitney, Victor Hanson-Smith, Arielle Woznica |
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| Jazyk: | angličtina |
| Rok vydání: | 2016 |
| Předmět: |
0301 basic medicine
Models Molecular Cell Cycle Proteins evolutionary biochemistry Salpingea rosetta Models cell biology Biology (General) Genetics General Neuroscience Cell Cycle General Medicine Cell biology Genomics and Evolutionary Biology mitotic spindle Medicine Protein Binding Research Article QH301-705.5 Evolution Science 1.1 Normal biological development and functioning evolutionary cell biology Spindle Apparatus Biology General Biochemistry Genetics and Molecular Biology Motor protein Evolution Molecular 03 medical and health sciences Microtubule Underpinning research Cell cortex genomics Animals Cell Cycle Protein protein evolution Mitosis General Immunology and Microbiology ancestral protein reconstruction evolutionary biology Correction Molecular Cell Biology Spindle apparatus Multicellular organism 030104 developmental biology Generic health relevance Biochemistry and Cell Biology Other Protein Multimerization Guanylate Kinases Function (biology) |
| Zdroj: | eLife eLife, vol 5, iss JANUARY2016 eLife, Vol 5 (2016) |
| ISSN: | 2050-084X |
| Popis: | To form and maintain organized tissues, multicellular organisms orient their mitotic spindles relative to neighboring cells. A molecular complex scaffolded by the GK protein-interaction domain (GKPID) mediates spindle orientation in diverse animal taxa by linking microtubule motor proteins to a marker protein on the cell cortex localized by external cues. Here we illuminate how this complex evolved and commandeered control of spindle orientation from a more ancient mechanism. The complex was assembled through a series of molecular exploitation events, one of which – the evolution of GKPID’s capacity to bind the cortical marker protein – can be recapitulated by reintroducing a single historical substitution into the reconstructed ancestral GKPID. This change revealed and repurposed an ancient molecular surface that previously had a radically different function. We show how the physical simplicity of this binding interface enabled the evolution of a new protein function now essential to the biological complexity of many animals. DOI: http://dx.doi.org/10.7554/eLife.10147.001 eLife digest For billions of years, life on Earth was made up of single cells. In the lineage that led to animals – and independently in those that led to plants and to fungi – multicellular organisms evolved as cells began to specialize and arrange themselves into tissues and organs. Although the evolution of multicellularity is one of the most important events in the history of animal life, very little is known about the molecular mechanisms by which it took place. To form and maintain organized tissues, cells must coordinate how they divide relative to the position of their neighbours. One important aspect of this process is orientation of the mitotic spindle, a structure inside the dividing cell that distributes the chromosomes —and the genetic material they carry — between the daughter cells. When the spindle is not oriented properly, malformed tissues and cancer can result. In a diverse range of animals, the orientation of the spindle is controlled by an ancient scaffolding protein that links the spindle to “marker” proteins on the edge of the cell. Anderson et al. have now used a technique called ancestral protein reconstruction to investigate how this molecular complex evolved its ability to position the spindle. First, the amino acid sequences of the scaffolding protein’s ancient progenitors, which existed before the origin of the most primitive animals on Earth, were determined. Anderson et al. did this by computationally retracing the evolution of large numbers of present-day scaffolding protein sequences down the tree of life, into the deep past. Living cells were then made to produce the ancient proteins, allowing their properties to be experimentally examined. By experimentally dissecting successive ancestral versions of the scaffolding protein, Anderson et al. deduced how the molecular complex that it anchors came to control spindle orientation. This new ability evolved by a number of “molecular exploitation” events, which repurposed parts of the protein for new roles. The progenitor of the scaffolding protein was actually an enzyme, but the evolution of its spindle-orienting ability can be recapitulated by introducing a single amino acid change that happened many hundreds of millions of years ago. How could a single mutation have conferred such a dramatically new function? Anderson et al. found that the ancient scaffolding protein uses the same part of its surface to bind to the spindle-orienting molecular marker as the ancient enzyme used to bind to its target substrate molecule, and the two partner molecules happen to share certain key chemical properties. This fortuitous resemblance between two unrelated molecules thus set the stage for the simple evolution of a function that is now essential to the complexity of multicellular animals. DOI: http://dx.doi.org/10.7554/eLife.10147.002 |
| Databáze: | OpenAIRE |
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