Uncovering DNA-PKcs ancient phylogeny, unique sequence motifs and insights for human disease
DNA-dependent protein kinase catalytic subunit (DNA-PKcs) is a key member of the phosphatidylinositol-3 kinase-like (PIKK) family of protein kinases with critical roles in DNA-double strand break repair, transcription, metastasis, mitosis, RNA processing, and innate and adaptive immunity. The absenc...
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| Published in | Progress in biophysics and molecular biology Vol. 163; no. C; pp. 87 - 108 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
Elsevier Ltd
01.08.2021
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | DNA-dependent protein kinase catalytic subunit (DNA-PKcs) is a key member of the phosphatidylinositol-3 kinase-like (PIKK) family of protein kinases with critical roles in DNA-double strand break repair, transcription, metastasis, mitosis, RNA processing, and innate and adaptive immunity. The absence of DNA-PKcs from many model organisms has led to the assumption that DNA-PKcs is a vertebrate-specific PIKK. Here, we find that DNA-PKcs is widely distributed in invertebrates, fungi, plants, and protists, and that threonines 2609, 2638, and 2647 of the ABCDE cluster of phosphorylation sites are highly conserved amongst most Eukaryotes. Furthermore, we identify highly conserved amino acid sequence motifs and domains that are characteristic of DNA-PKcs relative to other PIKKs. These include residues in the Forehead domain and a novel motif we have termed YRPD, located in an α helix C-terminal to the ABCDE phosphorylation site loop. Combining sequence with biochemistry plus structural data on human DNA-PKcs unveils conserved sequence and conformational features with functional insights and implications. The defined generally progressive DNA-PKcs sequence diversification uncovers conserved functionality supported by Evolutionary Trace analysis, suggesting that for many organisms both functional sites and evolutionary pressures remain identical due to fundamental cell biology. The mining of cancer genomic data and germline mutations causing human inherited disease reveal that robust DNA-PKcs activity in tumors is detrimental to patient survival, whereas germline mutations compromising function are linked to severe immunodeficiency and neuronal degeneration. We anticipate that these collective results will enable ongoing DNA-PKcs functional analyses with biological and medical implications. |
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| AbstractList | DNA-dependent protein kinase catalytic subunit (DNA-PKcs) is a key member of the phosphatidylinositol-3 kinase-like (PIKK) family of protein kinases with critical roles in DNA-double strand break repair, transcription, metastasis, mitosis, RNA processing, and innate and adaptive immunity. The absence of DNA-PKcs from many model organisms has led to the assumption that DNA-PKcs is a vertebrate-specific PIKK. Here, we find that DNA-PKcs is widely distributed in invertebrates, fungi, plants, and protists, and that threonines 2609, 2638, and 2647 of the ABCDE cluster of phosphorylation sites are highly conserved amongst most Eukaryotes. Furthermore, we identify highly conserved amino acid sequence motifs and domains that are characteristic of DNA-PKcs relative to other PIKKs. These include residues in the Forehead domain and a novel motif we have termed YRPD, located in an α helix C-terminal to the ABCDE phosphorylation site loop. Combining sequence with biochemistry plus structural data on human DNA-PKcs unveils conserved sequence and conformational features with functional insights and implications. The defined generally progressive DNA-PKcs sequence diversification uncovers conserved functionality supported by Evolutionary Trace analysis, suggesting that for many organisms both functional sites and evolutionary pressures remain identical due to fundamental cell biology. The mining of cancer genomic data and germline mutations causing human inherited disease reveal that robust DNA-PKcs activity in tumors is detrimental to patient survival, whereas germline mutations compromising function are linked to severe immunodeficiency and neuronal degeneration. We anticipate that these collective results will enable ongoing DNA-PKcs functional analyses with biological and medical implications. DNA-dependent protein kinase catalytic subunit (DNA-PKcs) is a key member of the phosphatidylinositol-3 kinase-like (PIKK) family of protein kinases with critical roles in DNA-double strand break repair, transcription, metastasis, mitosis, RNA processing, and innate and adaptive immunity. The absence of DNA-PKcs from many model organisms has led to the assumption that DNA-PKcs is a vertebrate-specific PIKK. Here, we find that DNA-PKcs is widely distributed in invertebrates, fungi, plants, and protists, and that threonines 2609, 2638, and 2647 of the ABCDE cluster of phosphorylation sites are highly conserved amongst most Eukaryotes. Furthermore, we identify highly conserved amino acid sequence motifs and domains that are characteristic of DNA-PKcs relative to other PIKKs. These include residues in the Forehead domain and a novel motif we have termed YRPD, located in an α helix C-terminal to the ABCDE phosphorylation site loop. Combining sequence with biochemistry plus structural data on human DNA-PKcs unveils conserved sequence and conformational features with functional insights and implications. The defined generally progressive DNA-PKcs sequence diversification uncovers conserved functionality supported by Evolutionary Trace analysis, suggesting that for many organisms both functional sites and evolutionary pressures remain identical due to fundamental cell biology. The mining of cancer genomic data and germline mutations causing human inherited disease reveal that robust DNA-PKcs activity in tumors is detrimental to patient survival, whereas germline mutations compromising function are linked to severe immunodeficiency and neuronal degeneration. We anticipate that these collective results will enable ongoing DNA-PKcs functional analyses with biological and medical implications.DNA-dependent protein kinase catalytic subunit (DNA-PKcs) is a key member of the phosphatidylinositol-3 kinase-like (PIKK) family of protein kinases with critical roles in DNA-double strand break repair, transcription, metastasis, mitosis, RNA processing, and innate and adaptive immunity. The absence of DNA-PKcs from many model organisms has led to the assumption that DNA-PKcs is a vertebrate-specific PIKK. Here, we find that DNA-PKcs is widely distributed in invertebrates, fungi, plants, and protists, and that threonines 2609, 2638, and 2647 of the ABCDE cluster of phosphorylation sites are highly conserved amongst most Eukaryotes. Furthermore, we identify highly conserved amino acid sequence motifs and domains that are characteristic of DNA-PKcs relative to other PIKKs. These include residues in the Forehead domain and a novel motif we have termed YRPD, located in an α helix C-terminal to the ABCDE phosphorylation site loop. Combining sequence with biochemistry plus structural data on human DNA-PKcs unveils conserved sequence and conformational features with functional insights and implications. The defined generally progressive DNA-PKcs sequence diversification uncovers conserved functionality supported by Evolutionary Trace analysis, suggesting that for many organisms both functional sites and evolutionary pressures remain identical due to fundamental cell biology. The mining of cancer genomic data and germline mutations causing human inherited disease reveal that robust DNA-PKcs activity in tumors is detrimental to patient survival, whereas germline mutations compromising function are linked to severe immunodeficiency and neuronal degeneration. We anticipate that these collective results will enable ongoing DNA-PKcs functional analyses with biological and medical implications. |
| Author | Lees-Miller, Susan P. Tsutakawa, Susan E. Lichtarge, Olivier Lees-Miller, James P. Bacolla, Albino Hammel, Michal Tainer, John A. Katsonis, Panagiotis Cobban, Alexander Meek, Katheryn Anderson, Dave W. |
| AuthorAffiliation | b Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA d Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA e College of Veterinary Medicine, Department of Microbiology & Molecular Genetics, And Department of Pathobiology & Diagnostic Investigation, Michigan State University, East Lansing, MI, 48824, USA a Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada c Departments of Cancer Biology and of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, 6767 Bertner Avenue, Houston, TX, 77030, USA |
| AuthorAffiliation_xml | – name: d Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA – name: c Departments of Cancer Biology and of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, 6767 Bertner Avenue, Houston, TX, 77030, USA – name: a Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada – name: b Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA – name: e College of Veterinary Medicine, Department of Microbiology & Molecular Genetics, And Department of Pathobiology & Diagnostic Investigation, Michigan State University, East Lansing, MI, 48824, USA |
| Author_xml | – sequence: 1 givenname: James P. surname: Lees-Miller fullname: Lees-Miller, James P. organization: Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada – sequence: 2 givenname: Alexander surname: Cobban fullname: Cobban, Alexander organization: Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada – sequence: 3 givenname: Panagiotis orcidid: 0000-0002-7172-1644 surname: Katsonis fullname: Katsonis, Panagiotis organization: Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA – sequence: 4 givenname: Albino orcidid: 0000-0003-0206-8423 surname: Bacolla fullname: Bacolla, Albino organization: Departments of Cancer Biology and of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, 6767 Bertner Avenue, Houston, TX, 77030, USA – sequence: 5 givenname: Susan E. orcidid: 0000-0002-4918-4571 surname: Tsutakawa fullname: Tsutakawa, Susan E. organization: Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA – sequence: 6 givenname: Michal orcidid: 0000-0002-5610-9289 surname: Hammel fullname: Hammel, Michal organization: Molecular Biophysics and Integrated Bioimaging, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA – sequence: 7 givenname: Katheryn surname: Meek fullname: Meek, Katheryn organization: College of Veterinary Medicine, Department of Microbiology & Molecular Genetics, And Department of Pathobiology & Diagnostic Investigation, Michigan State University, East Lansing, MI, 48824, USA – sequence: 8 givenname: Dave W. orcidid: 0000-0002-5130-0885 surname: Anderson fullname: Anderson, Dave W. organization: Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada – sequence: 9 givenname: Olivier surname: Lichtarge fullname: Lichtarge, Olivier organization: Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA – sequence: 10 givenname: John A. surname: Tainer fullname: Tainer, John A. email: jtainer@MDAnderson.org organization: Departments of Cancer Biology and of Molecular and Cellular Oncology, University of Texas MD Anderson Cancer Center, 6767 Bertner Avenue, Houston, TX, 77030, USA – sequence: 11 givenname: Susan P. surname: Lees-Miller fullname: Lees-Miller, Susan P. email: leesmill@ucalgary.ca organization: Department of Biochemistry and Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, Alberta, T2N 4N1, Canada |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33035590$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/2470822$$D View this record in Osti.gov |
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| Keywords | Motifs Kinase Sequence analysis DNA repair DNA damage Response Cryo-electron microscopy Crystal structure |
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| SubjectTerms | BASIC BIOLOGICAL SCIENCES Cryo-electron microscopy Crystal structure DNA - metabolism DNA damage Response DNA repair DNA-Activated Protein Kinase - genetics DNA-Activated Protein Kinase - metabolism DNA-Binding Proteins - metabolism Humans Kinase Motifs Nuclear Proteins - metabolism Phosphorylation Phylogeny Sequence analysis |
| Title | Uncovering DNA-PKcs ancient phylogeny, unique sequence motifs and insights for human disease |
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