Interspecies Variation in the Functional Consequences of Mutation of Cytochrome c
The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by dysregulation of platelet production. The molecular basis of the platelet production defect is unknown. Despite high conservation of cytochrome...
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Published in | PloS one Vol. 10; no. 6; p. e0130292 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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18.06.2015
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Abstract | The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by dysregulation of platelet production. The molecular basis of the platelet production defect is unknown. Despite high conservation of cytochrome c between human and mouse (91.4% identity), introducing the G41S mutation into mouse cytochrome c in a knockin mouse (CycsG41S/G41S) did not recapitulate the low platelet phenotype of Thrombocytopenia Cargeeg. While investigating the cause of this disparity we found a lack of conservation of the functional impact of cytochrome c mutations on caspase activation across species. Mutation of cytochrome c at residue 41 has distinct effects on the ability of cytochrome c to activate caspases depending on the species of both the cytochrome c and its binding partner Apaf-1. In contrast to our previous results showing the G41S mutation increases the ability of human cytochrome c to activate caspases, here we find this activity is decreased in mouse G41S cytochrome c. Additionally unlike wildtype human cytochrome c, G41S cytochrome c is unable to activate caspases in Xenopus embryo extracts. Taken together these results demonstrate a previously unreported species-specific component to the interaction of cytochrome c with Apaf-1. This suggests that the electrostatic interaction between cytochrome c and Apaf-1 is not the sole determinant of binding, with additional factors controlling binding specificity and affinity. These results have important implications for studies of the effects of cytochrome c mutations on the intrinsic apoptosis pathway. |
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AbstractList | The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by dysregulation of platelet production. The molecular basis of the platelet production defect is unknown. Despite high conservation of cytochrome c between human and mouse (91.4% identity), introducing the G41S mutation into mouse cytochrome c in a knockin mouse (CycsG41S/G41S) did not recapitulate the low platelet phenotype of Thrombocytopenia Cargeeg. While investigating the cause of this disparity we found a lack of conservation of the functional impact of cytochrome c mutations on caspase activation across species. Mutation of cytochrome c at residue 41 has distinct effects on the ability of cytochrome c to activate caspases depending on the species of both the cytochrome c and its binding partner Apaf-1. In contrast to our previous results showing the G41S mutation increases the ability of human cytochrome c to activate caspases, here we find this activity is decreased in mouse G41S cytochrome c. Additionally unlike wildtype human cytochrome c, G41S cytochrome c is unable to activate caspases in Xenopus embryo extracts. Taken together these results demonstrate a previously unreported species-specific component to the interaction of cytochrome c with Apaf-1. This suggests that the electrostatic interaction between cytochrome c and Apaf-1 is not the sole determinant of binding, with additional factors controlling binding specificity and affinity. These results have important implications for studies of the effects of cytochrome c mutations on the intrinsic apoptosis pathway. The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by dysregulation of platelet production. The molecular basis of the platelet production defect is unknown. Despite high conservation of cytochrome c between human and mouse (91.4% identity), introducing the G41S mutation into mouse cytochrome c in a knockin mouse ( Cycs G41S/G41S ) did not recapitulate the low platelet phenotype of Thrombocytopenia Cargeeg. While investigating the cause of this disparity we found a lack of conservation of the functional impact of cytochrome c mutations on caspase activation across species. Mutation of cytochrome c at residue 41 has distinct effects on the ability of cytochrome c to activate caspases depending on the species of both the cytochrome c and its binding partner Apaf-1. In contrast to our previous results showing the G41S mutation increases the ability of human cytochrome c to activate caspases, here we find this activity is decreased in mouse G41S cytochrome c . Additionally unlike wildtype human cytochrome c , G41S cytochrome c is unable to activate caspases in Xenopus embryo extracts. Taken together these results demonstrate a previously unreported species-specific component to the interaction of cytochrome c with Apaf-1. This suggests that the electrostatic interaction between cytochrome c and Apaf-1 is not the sole determinant of binding, with additional factors controlling binding specificity and affinity. These results have important implications for studies of the effects of cytochrome c mutations on the intrinsic apoptosis pathway. The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by dysregulation of platelet production. The molecular basis of the platelet production defect is unknown. Despite high conservation of cytochrome c between human and mouse (91.4% identity), introducing the G41S mutation into mouse cytochrome c in a knockin mouse (Cycs.sup.G41S/G41S) did not recapitulate the low platelet phenotype of Thrombocytopenia Cargeeg. While investigating the cause of this disparity we found a lack of conservation of the functional impact of cytochrome c mutations on caspase activation across species. Mutation of cytochrome c at residue 41 has distinct effects on the ability of cytochrome c to activate caspases depending on the species of both the cytochrome c and its binding partner Apaf-1. In contrast to our previous results showing the G41S mutation increases the ability of human cytochrome c to activate caspases, here we find this activity is decreased in mouse G41S cytochrome c. Additionally unlike wildtype human cytochrome c, G41S cytochrome c is unable to activate caspases in Xenopus embryo extracts. Taken together these results demonstrate a previously unreported species-specific component to the interaction of cytochrome c with Apaf-1. This suggests that the electrostatic interaction between cytochrome c and Apaf-1 is not the sole determinant of binding, with additional factors controlling binding specificity and affinity. These results have important implications for studies of the effects of cytochrome c mutations on the intrinsic apoptosis pathway. |
Audience | Academic |
Author | Ledgerwood, Elizabeth C Ong, Lily Hibbs, Moira E Josephs, Tracy M Morison, Ian M |
AuthorAffiliation | 2 Department of Pathology, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand The University of Texas MD Anderson Cancer Center, UNITED STATES 1 Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand |
AuthorAffiliation_xml | – name: 1 Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand – name: The University of Texas MD Anderson Cancer Center, UNITED STATES – name: 2 Department of Pathology, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand |
Author_xml | – sequence: 1 givenname: Tracy M surname: Josephs fullname: Josephs, Tracy M organization: Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand – sequence: 2 givenname: Moira E surname: Hibbs fullname: Hibbs, Moira E organization: Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand – sequence: 3 givenname: Lily surname: Ong fullname: Ong, Lily organization: Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand – sequence: 4 givenname: Ian M surname: Morison fullname: Morison, Ian M organization: Department of Pathology, Dunedin School of Medicine, University of Otago, Dunedin, New Zealand – sequence: 5 givenname: Elizabeth C surname: Ledgerwood fullname: Ledgerwood, Elizabeth C organization: Department of Biochemistry, Otago School of Medical Sciences, University of Otago, Dunedin, New Zealand |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26086723$$D View this record in MEDLINE/PubMed |
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CitedBy_id | crossref_primary_10_1016_j_bbadis_2024_167134 crossref_primary_10_1021_acs_chemrev_7b00257 crossref_primary_10_1038_srep30447 crossref_primary_10_1042_BCJ20200793 crossref_primary_10_1080_09537104_2018_1543866 crossref_primary_10_3390_biom13081233 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Current address: Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia Competing Interests: The authors have declared that no competing interests exist. Conceived and designed the experiments: TMJ IMM ECL. Performed the experiments: TMJ MEH LO. Analyzed the data: TMJ IMM ECL. Wrote the paper: TMJ MEH LO IMM ECL. |
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Snippet | The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by... The naturally occurring human cytochrome c variant (G41S) is associated with a mild autosomal dominant thrombocytopenia (Thrombocytopenia Cargeeg) caused by... |
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SubjectTerms | Amino Acid Sequence Amphibians Animals Apaf-1 protein Apoptosis Binding Biochemistry Blood platelets Bone marrow Caspase Caspases - metabolism Conservation Cytochrome Cytochrome c Cytochromes c - genetics Cytochromes c - metabolism Electrostatic properties Enzyme Activation Gene Knock-In Techniques Genetic aspects Hematology Hematopoiesis Human performance Humans Mice, Inbred C57BL Mice, Transgenic Mitochondrial DNA Molecular chains Molecular Sequence Data Mutation Phenotypes Platelet Count Platelets Proteins Species Species Specificity Thrombocytopenia |
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Title | Interspecies Variation in the Functional Consequences of Mutation of Cytochrome c |
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