The Dual Specificity JKAP Specifically Activates the c-Jun N-terminal Kinase Pathway

The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of MAPKs by the direct dephosphorylation of the TXY motif within their activation loop. We report the cloning and characterization of a murine...

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Published inThe Journal of biological chemistry Vol. 277; no. 39; pp. 36592 - 36601
Main Authors Chen, Alice J., Zhou, Guisheng, Juan, Todd, Colicos, Suzanne M., Cannon, John P., Cabriera-Hansen, Maria, Meyer, Christian F., Jurecic, Roland, Copeland, Neal G., Gilbert, Debra J., Jenkins, Nancy A., Fletcher, Fred, Tan, Tse-Hua, Belmont, John W.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 27.09.2002
American Society for Biochemistry and Molecular Biology
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Abstract The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of MAPKs by the direct dephosphorylation of the TXY motif within their activation loop. We report the cloning and characterization of a murine DSP, called JNK pathway-associated phosphatase (JKAP), which lacks the regulatory region present in most other MAP kinase phosphatases (MKPs) and is preferentially expressed in murine Lin−Sca-1+ stem cells. Overexpression of JKAP in human embryonic kidney 293T cells specifically activated c-Jun N-terminal kinase (JNK) but not p38 and extracellular signal-regulated kinase 2. Overexpression of a mutant JKAP, JKAP-C88S, blocked tumor necrosis factor-α-induced JNK activation. Targeted gene disruption in murine embryonic stem cells abolished JNK activation by tumor necrosis factor-α and transforming growth factor-β, but not by ultraviolet-C irradiation, indicating that JKAP is necessary for optimal JNK activation. JKAP associated with JNK and MKK7, but not SEK1, in vivo. However, JKAP did not interact with JNK in vitro, suggesting that JKAP exerts its effect on JNK in an indirect manner. Taken together, these studies identify a positive regulator for the JNK pathway and suggest a novel role for DSP in mitogen-activated protein kinase regulation.
AbstractList The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of MAPKs by the direct dephosphorylation of the TXY motif within their activation loop. We report the cloning and characterization of a murine DSP, called JNK pathway-associated phosphatase (JKAP), which lacks the regulatory region present in most other MAP kinase phosphatases (MKPs) and is preferentially expressed in murine Lin−Sca-1+ stem cells. Overexpression of JKAP in human embryonic kidney 293T cells specifically activated c-Jun N-terminal kinase (JNK) but not p38 and extracellular signal-regulated kinase 2. Overexpression of a mutant JKAP, JKAP-C88S, blocked tumor necrosis factor-α-induced JNK activation. Targeted gene disruption in murine embryonic stem cells abolished JNK activation by tumor necrosis factor-α and transforming growth factor-β, but not by ultraviolet-C irradiation, indicating that JKAP is necessary for optimal JNK activation. JKAP associated with JNK and MKK7, but not SEK1, in vivo. However, JKAP did not interact with JNK in vitro, suggesting that JKAP exerts its effect on JNK in an indirect manner. Taken together, these studies identify a positive regulator for the JNK pathway and suggest a novel role for DSP in mitogen-activated protein kinase regulation.
The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of MAPKs by the direct dephosphorylation of the T X Y motif within their activation loop. We report the cloning and characterization of a murine DSP, called JNK pathway-associated phosphatase (JKAP), which lacks the regulatory region present in most other MAP kinase phosphatases (MKPs) and is preferentially expressed in murine Lin − Sca-1 + stem cells. Overexpression of JKAP in human embryonic kidney 293T cells specifically activated c-Jun N-terminal kinase (JNK) but not p38 and extracellular signal-regulated kinase 2. Overexpression of a mutant JKAP, JKAP-C88S, blocked tumor necrosis factor-α-induced JNK activation. Targeted gene disruption in murine embryonic stem cells abolished JNK activation by tumor necrosis factor-α and transforming growth factor-β, but not by ultraviolet-C irradiation, indicating that JKAP is necessary for optimal JNK activation. JKAP associated with JNK and MKK7, but not SEK1, in vivo . However, JKAP did not interact with JNK in vitro , suggesting that JKAP exerts its effect on JNK in an indirect manner. Taken together, these studies identify a positive regulator for the JNK pathway and suggest a novel role for DSP in mitogen-activated protein kinase regulation.
The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of MAPKs by the direct dephosphorylation of the TXY motif within their activation loop. We report the cloning and characterization of a murine DSP, called JNK pathway-associated phosphatase (JKAP), which lacks the regulatory region present in most other MAP kinase phosphatases (MKPs) and is preferentially expressed in murine Lin(-)Sca-1(+) stem cells. Overexpression of JKAP in human embryonic kidney 293T cells specifically activated c-Jun N-terminal kinase (JNK) but not p38 and extracellular signal-regulated kinase 2. Overexpression of a mutant JKAP, JKAP-C88S, blocked tumor necrosis factor-alpha-induced JNK activation. Targeted gene disruption in murine embryonic stem cells abolished JNK activation by tumor necrosis factor-alpha and transforming growth factor-beta, but not by ultraviolet-C irradiation, indicating that JKAP is necessary for optimal JNK activation. JKAP associated with JNK and MKK7, but not SEK1, in vivo. However, JKAP did not interact with JNK in vitro, suggesting that JKAP exerts its effect on JNK in an indirect manner. Taken together, these studies identify a positive regulator for the JNK pathway and suggest a novel role for DSP in mitogen-activated protein kinase regulation.
Author Gilbert, Debra J.
Belmont, John W.
Meyer, Christian F.
Juan, Todd
Copeland, Neal G.
Fletcher, Fred
Chen, Alice J.
Jurecic, Roland
Tan, Tse-Hua
Jenkins, Nancy A.
Cannon, John P.
Cabriera-Hansen, Maria
Zhou, Guisheng
Colicos, Suzanne M.
Author_xml – sequence: 1
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  organization: Department of Immunology, Baylor College of Medicine, Houston, Texas 77030
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  organization: Department of Experimental Hematology, Amgen, Inc., Thousand Oaks, California 91320
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  organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030
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  organization: Department of Immunology, Baylor College of Medicine, Houston, Texas 77030
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  organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030
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  givenname: Neal G.
  surname: Copeland
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  organization: Mammalian Genetics Laboratory, ABL-Basic Research Program, NCI-Frederick Cancer Research and Development Center, Frederick, Maryland 21702
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  givenname: Debra J.
  surname: Gilbert
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  surname: Belmont
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  organization: Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, Texas 77030
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Snippet The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of...
The involvement of dual specificity phosphatases (DSPs) in the mitogen-activated protein kinase (MAPK) signaling has been mostly limited to the inactivation of...
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SubjectTerms Amino Acid Sequence
Animals
Cell Line
Crosses, Genetic
DNA, Complementary - metabolism
Dose-Response Relationship, Drug
Enzyme Activation
Hematopoietic Stem Cells - metabolism
Humans
In Situ Hybridization
JNK Mitogen-Activated Protein Kinases
MAP Kinase Kinase 4
MAP Kinase Kinase 7
MAP Kinase Signaling System
Mice
Mice, Inbred C57BL
Mitogen-Activated Protein Kinase 1 - metabolism
Mitogen-Activated Protein Kinase Kinases - metabolism
Mitogen-Activated Protein Kinases
Models, Genetic
Molecular Sequence Data
Mutation
p38 Mitogen-Activated Protein Kinases
Phosphoprotein Phosphatases - metabolism
Phosphoprotein Phosphatases - physiology
Plasmids - metabolism
Precipitin Tests
Protein Binding
RNA, Messenger - metabolism
Sequence Homology, Amino Acid
Signal Transduction
Substrate Specificity
Tissue Distribution
Transfection
Transforming Growth Factor beta - pharmacology
Tumor Necrosis Factor-alpha - metabolism
Ultraviolet Rays
Title The Dual Specificity JKAP Specifically Activates the c-Jun N-terminal Kinase Pathway
URI https://dx.doi.org/10.1074/jbc.M200453200
http://www.jbc.org/content/277/39/36592.abstract
https://www.ncbi.nlm.nih.gov/pubmed/12138158
Volume 277
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