Regulatory Phosphorylation of Ikaros by Bruton's Tyrosine Kinase
Diminished Ikaros function has been implicated in the pathogenesis of acute lymphoblastic leukemia (ALL), the most common form of childhood cancer. Therefore, a stringent regulation of Ikaros is of paramount importance for normal lymphocyte ontogeny. Here we provide genetic and biochemical evidence...
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| Published in | PloS one Vol. 8; no. 8; p. e71302 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
19.08.2013
Public Library of Science (PLoS) |
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| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0071302 |
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| Abstract | Diminished Ikaros function has been implicated in the pathogenesis of acute lymphoblastic leukemia (ALL), the most common form of childhood cancer. Therefore, a stringent regulation of Ikaros is of paramount importance for normal lymphocyte ontogeny. Here we provide genetic and biochemical evidence for a previously unknown function of Bruton's tyrosine kinase (BTK) as a partner and posttranslational regulator of Ikaros, a zinc finger-containing DNA-binding protein that plays a pivotal role in immune homeostasis. We demonstrate that BTK phosphorylates Ikaros at unique phosphorylation sites S214 and S215 in the close vicinity of its zinc finger 4 (ZF4) within the DNA binding domain, thereby augmenting its nuclear localization and sequence-specific DNA binding activity. Our results further demonstrate that BTK-induced activating phosphorylation is critical for the optimal transcription factor function of Ikaros. |
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| AbstractList | Diminished Ikaros function has been implicated in the pathogenesis of acute lymphoblastic leukemia (ALL), the most common form of childhood cancer. Therefore, a stringent regulation of Ikaros is of paramount importance for normal lymphocyte ontogeny. Here we provide genetic and biochemical evidence for a previously unknown function of Bruton's tyrosine kinase (BTK) as a partner and posttranslational regulator of Ikaros, a zinc finger-containing DNA-binding protein that plays a pivotal role in immune homeostasis. We demonstrate that BTK phosphorylates Ikaros at unique phosphorylation sites S214 and S215 in the close vicinity of its zinc finger 4 (ZF4) within the DNA binding domain, thereby augmenting its nuclear localization and sequence-specific DNA binding activity. Our results further demonstrate that BTK-induced activating phosphorylation is critical for the optimal transcription factor function of Ikaros.Diminished Ikaros function has been implicated in the pathogenesis of acute lymphoblastic leukemia (ALL), the most common form of childhood cancer. Therefore, a stringent regulation of Ikaros is of paramount importance for normal lymphocyte ontogeny. Here we provide genetic and biochemical evidence for a previously unknown function of Bruton's tyrosine kinase (BTK) as a partner and posttranslational regulator of Ikaros, a zinc finger-containing DNA-binding protein that plays a pivotal role in immune homeostasis. We demonstrate that BTK phosphorylates Ikaros at unique phosphorylation sites S214 and S215 in the close vicinity of its zinc finger 4 (ZF4) within the DNA binding domain, thereby augmenting its nuclear localization and sequence-specific DNA binding activity. Our results further demonstrate that BTK-induced activating phosphorylation is critical for the optimal transcription factor function of Ikaros. Diminished Ikaros function has been implicated in the pathogenesis of acute lymphoblastic leukemia (ALL), the most common form of childhood cancer. Therefore, a stringent regulation of Ikaros is of paramount importance for normal lymphocyte ontogeny. Here we provide genetic and biochemical evidence for a previously unknown function of Bruton's tyrosine kinase (BTK) as a partner and posttranslational regulator of Ikaros, a zinc finger-containing DNA-binding protein that plays a pivotal role in immune homeostasis. We demonstrate that BTK phosphorylates Ikaros at unique phosphorylation sites S214 and S215 in the close vicinity of its zinc finger 4 (ZF4) within the DNA binding domain, thereby augmenting its nuclear localization and sequence-specific DNA binding activity. Our results further demonstrate that BTK-induced activating phosphorylation is critical for the optimal transcription factor function of Ikaros. |
| Audience | Academic |
| Author | Ma, Hong Ozer, Zahide Zhang, Jian Qazi, Sanjive Ishkhanian, Rita Uckun, Fatih M. |
| AuthorAffiliation | 2 Department of Biology and Bioinformatics Program, Gustavus Adolphus College, St. Peter, Minnesota, United States of America 5 Department of Pediatrics, University of Southern California Keck School of Medicine, Los Angeles, California, United States of America 4 Medicinal Bioinformatics Center, Shanghai Jiatong University, Shanghai, China 1 Systems Immunobiology Laboratory, Children's Center for Cancer and Blood Diseases, Children's Hospital Los Angeles, Los Angeles, California, United States of America 3 Molecular Oncology Program, Parker Hughes Institute, St. Paul, Minnesota, United States of America Westmead Millennium Institute, University of Sydney, Australia |
| AuthorAffiliation_xml | – name: 4 Medicinal Bioinformatics Center, Shanghai Jiatong University, Shanghai, China – name: 2 Department of Biology and Bioinformatics Program, Gustavus Adolphus College, St. Peter, Minnesota, United States of America – name: 3 Molecular Oncology Program, Parker Hughes Institute, St. Paul, Minnesota, United States of America – name: Westmead Millennium Institute, University of Sydney, Australia – name: 1 Systems Immunobiology Laboratory, Children's Center for Cancer and Blood Diseases, Children's Hospital Los Angeles, Los Angeles, California, United States of America – name: 5 Department of Pediatrics, University of Southern California Keck School of Medicine, Los Angeles, California, United States of America |
| Author_xml | – sequence: 1 givenname: Hong surname: Ma fullname: Ma, Hong – sequence: 2 givenname: Sanjive surname: Qazi fullname: Qazi, Sanjive – sequence: 3 givenname: Zahide surname: Ozer fullname: Ozer, Zahide – sequence: 4 givenname: Jian surname: Zhang fullname: Zhang, Jian – sequence: 5 givenname: Rita surname: Ishkhanian fullname: Ishkhanian, Rita – sequence: 6 givenname: Fatih M. surname: Uckun fullname: Uckun, Fatih M. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23977012$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2013 Public Library of Science 2013 Ma et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2013 Ma et al 2013 Ma et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceived and designed the experiments: HM SQ JZ ZO RI FMU. Performed the experiments: HM SQ JZ ZO RI FMU. Analyzed the data: HM SQ JZ FMU. Contributed reagents/materials/analysis tools: JZ. Wrote the paper: HM SQ JZ ZO RI FMU. Reviewed and revised the paper: HM SQ ZO JZ RI FMU. Competing Interests: The authors have declared that no competing interests exist. |
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| SubjectTerms | Acute lymphoblastic leukemia Agammaglobulinaemia Tyrosine Kinase Animals Apoptosis B-Lymphocytes - metabolism B-Lymphocytes - pathology Bioinformatics Biology Biotechnology Blood diseases Bruton's tyrosine kinase Cancer Cell Line, Tumor Cell Nucleus - genetics Cell Nucleus - metabolism Children Children & youth Cooperation Deoxyribonucleic acid DNA DNA binding proteins DNA-binding protein Gene Expression Regulation, Leukemic Genes Homeostasis Human subjects Humans Ikaros protein Ikaros Transcription Factor - genetics Ikaros Transcription Factor - metabolism Infant Kinases Laboratories Leukemia Localization Lymphatic leukemia Lymphocytes Lymphoma Medical prognosis Medicine Mice Nucleotide sequence Ontogeny Pathogenesis Phenols (Class of compounds) Phosphorylation Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - genetics Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - metabolism Precursor B-Cell Lymphoblastic Leukemia-Lymphoma - pathology Protein Binding Protein-tyrosine kinase Protein-Tyrosine Kinases - genetics Protein-Tyrosine Kinases - metabolism Proteins Signal Transduction Transcription factors Tyrosine Young Adult Zinc Zinc finger proteins Zinc Fingers |
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| Title | Regulatory Phosphorylation of Ikaros by Bruton's Tyrosine Kinase |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/23977012 https://www.proquest.com/docview/1430785914 https://www.proquest.com/docview/1428270453 https://pubmed.ncbi.nlm.nih.gov/PMC3747153 https://doaj.org/article/607ba95772884b01bdd3ba20110abf62 http://dx.doi.org/10.1371/journal.pone.0071302 |
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