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Antagonistic Regulation of ROMK by Long and Kidney-Specific WNK1 Isoforms
WNK kinases are serine-threonine kinases with an atypical placement of the catalytic lysine. Intronic deletions with increased expression of a ubiquitous long WNK1 transcript cause pseudohypoaldosteronism type 2 (PHA II), characterized by hypertension and hyperkalemia. Here, we report that long WNK1...
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| Published in: | Proceedings of the National Academy of Sciences - PNAS 2006-01, Vol.103 (5), p.1615-1620 |
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| creator | Lazrak, Ahmed Liu, Zhen Huang, Chou-Long |
| description | WNK kinases are serine-threonine kinases with an atypical placement of the catalytic lysine. Intronic deletions with increased expression of a ubiquitous long WNK1 transcript cause pseudohypoaldosteronism type 2 (PHA II), characterized by hypertension and hyperkalemia. Here, we report that long WNK1 inhibited ROMK1 by stimulating its endocytosis. Inhibition of ROMK by long WNK1 was synergistic with, but not dependent on, WNK4. A smaller transcript of WNK1 lacking the N-terminal 1-437 amino acids is expressed highly in the kidney. Whether expression of the KSWNK1 (kidney-specific, KS) is altered in PHA II is not known. We found that KS-WNK1 did not inhibit ROMK1 but reversed the inhibition of ROMK1 caused by long WNK1. Consistent with the lack of inhibition by KS-WNK1, we found that amino acids 1-491 of the long WNK1 were sufficient for inhibiting ROMK. Dietary K⁺ restriction decreases ROMK abundance in the renal cortical-collecting ducts by stimulating endocytosis, an adaptative response important for conservation of K⁺ during K⁺ deficiency. We found that K⁺ restriction in rats increased whole-kidney transcript of long WNK1 while decreasing that of KS-WNK1. Thus, KS-WNK1 is a physiological antagonist of long WNK1. Hyperkalemia in PHA II patients with PHA II mutations may be caused, at least partially, by increased expression of long WNK1 with or without decreased expression of KS-WNK1. |
| doi_str_mv | 10.1073/pnas.0510609103 |
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Intronic deletions with increased expression of a ubiquitous long WNK1 transcript cause pseudohypoaldosteronism type 2 (PHA II), characterized by hypertension and hyperkalemia. Here, we report that long WNK1 inhibited ROMK1 by stimulating its endocytosis. Inhibition of ROMK by long WNK1 was synergistic with, but not dependent on, WNK4. A smaller transcript of WNK1 lacking the N-terminal 1-437 amino acids is expressed highly in the kidney. Whether expression of the KSWNK1 (kidney-specific, KS) is altered in PHA II is not known. We found that KS-WNK1 did not inhibit ROMK1 but reversed the inhibition of ROMK1 caused by long WNK1. Consistent with the lack of inhibition by KS-WNK1, we found that amino acids 1-491 of the long WNK1 were sufficient for inhibiting ROMK. Dietary K⁺ restriction decreases ROMK abundance in the renal cortical-collecting ducts by stimulating endocytosis, an adaptative response important for conservation of K⁺ during K⁺ deficiency. We found that K⁺ restriction in rats increased whole-kidney transcript of long WNK1 while decreasing that of KS-WNK1. Thus, KS-WNK1 is a physiological antagonist of long WNK1. Hyperkalemia in PHA II patients with PHA II mutations may be caused, at least partially, by increased expression of long WNK1 with or without decreased expression of KS-WNK1.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0510609103</identifier><identifier>PMID: 16428287</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Amino Acid Sequence ; Amino acids ; Animals ; Antagonist drugs ; B lymphocytes ; Biological Sciences ; Blotting, Western ; Cell Line ; Clathrin - metabolism ; Diet ; DNA - chemistry ; DNA - metabolism ; Dose-Response Relationship, Drug ; Dynamins - metabolism ; Electrophysiology ; Endocytosis ; Enzymes ; Exons ; Female ; Gene expression ; Gene Expression Regulation ; Genetic mutation ; Green Fluorescent Proteins - metabolism ; Humans ; Hyperkalemia ; Hypertension ; Immunoprecipitation ; Intracellular Signaling Peptides and Proteins ; Kidney - metabolism ; Kidneys ; Male ; Minor Histocompatibility Antigens ; Models, Biological ; Models, Genetic ; Molecular Sequence Data ; Mutation ; Patch-Clamp Techniques ; Potassium - chemistry ; Potassium - metabolism ; Potassium Channels, Inwardly Rectifying - physiology ; Protein Isoforms ; Protein Structure, Tertiary ; Protein-Serine-Threonine Kinases - biosynthesis ; Protein-Serine-Threonine Kinases - metabolism ; Rats ; Rats, Sprague-Dawley ; RNA, Messenger - metabolism ; RNA, Small Interfering - metabolism ; Small interfering RNA ; Transfection ; WNK Lysine-Deficient Protein Kinase 1</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2006-01, Vol.103 (5), p.1615-1620</ispartof><rights>Copyright 2006 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Jan 31, 2006</rights><rights>Copyright © 2006, The National Academy of Sciences 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-81053634120aa85eb71ce84b55309234ea3afe21d3c601817438d73557159af3</citedby><cites>FETCH-LOGICAL-c526t-81053634120aa85eb71ce84b55309234ea3afe21d3c601817438d73557159af3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/103/5.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/30048421$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/30048421$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,730,783,787,888,27936,27937,53804,53806,58566,58799</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16428287$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lazrak, Ahmed</creatorcontrib><creatorcontrib>Liu, Zhen</creatorcontrib><creatorcontrib>Huang, Chou-Long</creatorcontrib><title>Antagonistic Regulation of ROMK by Long and Kidney-Specific WNK1 Isoforms</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>WNK kinases are serine-threonine kinases with an atypical placement of the catalytic lysine. Intronic deletions with increased expression of a ubiquitous long WNK1 transcript cause pseudohypoaldosteronism type 2 (PHA II), characterized by hypertension and hyperkalemia. Here, we report that long WNK1 inhibited ROMK1 by stimulating its endocytosis. Inhibition of ROMK by long WNK1 was synergistic with, but not dependent on, WNK4. A smaller transcript of WNK1 lacking the N-terminal 1-437 amino acids is expressed highly in the kidney. Whether expression of the KSWNK1 (kidney-specific, KS) is altered in PHA II is not known. We found that KS-WNK1 did not inhibit ROMK1 but reversed the inhibition of ROMK1 caused by long WNK1. Consistent with the lack of inhibition by KS-WNK1, we found that amino acids 1-491 of the long WNK1 were sufficient for inhibiting ROMK. Dietary K⁺ restriction decreases ROMK abundance in the renal cortical-collecting ducts by stimulating endocytosis, an adaptative response important for conservation of K⁺ during K⁺ deficiency. We found that K⁺ restriction in rats increased whole-kidney transcript of long WNK1 while decreasing that of KS-WNK1. Thus, KS-WNK1 is a physiological antagonist of long WNK1. Hyperkalemia in PHA II patients with PHA II mutations may be caused, at least partially, by increased expression of long WNK1 with or without decreased expression of KS-WNK1.</description><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Antagonist drugs</subject><subject>B lymphocytes</subject><subject>Biological Sciences</subject><subject>Blotting, Western</subject><subject>Cell Line</subject><subject>Clathrin - metabolism</subject><subject>Diet</subject><subject>DNA - chemistry</subject><subject>DNA - metabolism</subject><subject>Dose-Response Relationship, Drug</subject><subject>Dynamins - metabolism</subject><subject>Electrophysiology</subject><subject>Endocytosis</subject><subject>Enzymes</subject><subject>Exons</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Genetic mutation</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Humans</subject><subject>Hyperkalemia</subject><subject>Hypertension</subject><subject>Immunoprecipitation</subject><subject>Intracellular Signaling Peptides and Proteins</subject><subject>Kidney - metabolism</subject><subject>Kidneys</subject><subject>Male</subject><subject>Minor Histocompatibility Antigens</subject><subject>Models, Biological</subject><subject>Models, Genetic</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Patch-Clamp Techniques</subject><subject>Potassium - chemistry</subject><subject>Potassium - metabolism</subject><subject>Potassium Channels, Inwardly Rectifying - physiology</subject><subject>Protein Isoforms</subject><subject>Protein Structure, Tertiary</subject><subject>Protein-Serine-Threonine Kinases - biosynthesis</subject><subject>Protein-Serine-Threonine Kinases - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>RNA, Messenger - metabolism</subject><subject>RNA, Small Interfering - metabolism</subject><subject>Small interfering RNA</subject><subject>Transfection</subject><subject>WNK Lysine-Deficient Protein Kinase 1</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><recordid>eNqF0ktvEzEQAGALgWgInDmBVhzgtO2MH7veC1JV8YgSqFQqcbScXW9wtLFT24vIv8dRoqZwgJMt-ZvxeMaEvEQ4R6jZxdbpeA4CoYIGgT0iE8ybsuINPCYTAFqXklN-Rp7FuAaARkh4Ss6w4lRSWU_I7NIlvfLOxmTb4sasxkEn613h--Lm-su8WO6KhXerQruumNvOmV35bWta22f-_esci1n0vQ-b-Jw86fUQzYvjOiW3Hz_cXn0uF9efZleXi7IVtEqlRBCsYhwpaC2FWdbYGsmXQjBoKONGM90bih1rK0CJNWeyq5kQNYpG92xK3h_SbsflxnStcSnoQW2D3eiwU15b9eeJsz_Uyv9UyCoQ-YYpeXtMEPzdaGJSGxtbMwzaGT9GVee-YpNL_B_MpdVcMpnhm7_g2o_B5SYoCsi4zO3O6OKA2uBjDKa_LxlB7Wep9rNUp1nmiNcPX3ryx-E9APvIUzqmREYoMnj3T6D6cRiS-ZWyfHWQ65h8uKcMgOf_g-w3nsO5Ow</recordid><startdate>20060131</startdate><enddate>20060131</enddate><creator>Lazrak, Ahmed</creator><creator>Liu, Zhen</creator><creator>Huang, Chou-Long</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7ST</scope><scope>7U6</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060131</creationdate><title>Antagonistic Regulation of ROMK by Long and Kidney-Specific WNK1 Isoforms</title><author>Lazrak, Ahmed ; Liu, Zhen ; Huang, Chou-Long</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-81053634120aa85eb71ce84b55309234ea3afe21d3c601817438d73557159af3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Amino Acid Sequence</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Antagonist drugs</topic><topic>B lymphocytes</topic><topic>Biological Sciences</topic><topic>Blotting, Western</topic><topic>Cell Line</topic><topic>Clathrin - metabolism</topic><topic>Diet</topic><topic>DNA - chemistry</topic><topic>DNA - metabolism</topic><topic>Dose-Response Relationship, Drug</topic><topic>Dynamins - metabolism</topic><topic>Electrophysiology</topic><topic>Endocytosis</topic><topic>Enzymes</topic><topic>Exons</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Genetic mutation</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Humans</topic><topic>Hyperkalemia</topic><topic>Hypertension</topic><topic>Immunoprecipitation</topic><topic>Intracellular Signaling Peptides and Proteins</topic><topic>Kidney - metabolism</topic><topic>Kidneys</topic><topic>Male</topic><topic>Minor Histocompatibility Antigens</topic><topic>Models, Biological</topic><topic>Models, Genetic</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Patch-Clamp Techniques</topic><topic>Potassium - chemistry</topic><topic>Potassium - metabolism</topic><topic>Potassium Channels, Inwardly Rectifying - physiology</topic><topic>Protein Isoforms</topic><topic>Protein Structure, Tertiary</topic><topic>Protein-Serine-Threonine Kinases - biosynthesis</topic><topic>Protein-Serine-Threonine Kinases - metabolism</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>RNA, Messenger - metabolism</topic><topic>RNA, Small Interfering - metabolism</topic><topic>Small interfering RNA</topic><topic>Transfection</topic><topic>WNK Lysine-Deficient Protein Kinase 1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lazrak, Ahmed</creatorcontrib><creatorcontrib>Liu, Zhen</creatorcontrib><creatorcontrib>Huang, Chou-Long</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>Sustainability Science Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lazrak, Ahmed</au><au>Liu, Zhen</au><au>Huang, Chou-Long</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Antagonistic Regulation of ROMK by Long and Kidney-Specific WNK1 Isoforms</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2006-01-31</date><risdate>2006</risdate><volume>103</volume><issue>5</issue><spage>1615</spage><epage>1620</epage><pages>1615-1620</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>WNK kinases are serine-threonine kinases with an atypical placement of the catalytic lysine. Intronic deletions with increased expression of a ubiquitous long WNK1 transcript cause pseudohypoaldosteronism type 2 (PHA II), characterized by hypertension and hyperkalemia. Here, we report that long WNK1 inhibited ROMK1 by stimulating its endocytosis. Inhibition of ROMK by long WNK1 was synergistic with, but not dependent on, WNK4. A smaller transcript of WNK1 lacking the N-terminal 1-437 amino acids is expressed highly in the kidney. Whether expression of the KSWNK1 (kidney-specific, KS) is altered in PHA II is not known. We found that KS-WNK1 did not inhibit ROMK1 but reversed the inhibition of ROMK1 caused by long WNK1. Consistent with the lack of inhibition by KS-WNK1, we found that amino acids 1-491 of the long WNK1 were sufficient for inhibiting ROMK. Dietary K⁺ restriction decreases ROMK abundance in the renal cortical-collecting ducts by stimulating endocytosis, an adaptative response important for conservation of K⁺ during K⁺ deficiency. We found that K⁺ restriction in rats increased whole-kidney transcript of long WNK1 while decreasing that of KS-WNK1. Thus, KS-WNK1 is a physiological antagonist of long WNK1. Hyperkalemia in PHA II patients with PHA II mutations may be caused, at least partially, by increased expression of long WNK1 with or without decreased expression of KS-WNK1.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>16428287</pmid><doi>10.1073/pnas.0510609103</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Amino Acid Sequence Amino acids Animals Antagonist drugs B lymphocytes Biological Sciences Blotting, Western Cell Line Clathrin - metabolism Diet DNA - chemistry DNA - metabolism Dose-Response Relationship, Drug Dynamins - metabolism Electrophysiology Endocytosis Enzymes Exons Female Gene expression Gene Expression Regulation Genetic mutation Green Fluorescent Proteins - metabolism Humans Hyperkalemia Hypertension Immunoprecipitation Intracellular Signaling Peptides and Proteins Kidney - metabolism Kidneys Male Minor Histocompatibility Antigens Models, Biological Models, Genetic Molecular Sequence Data Mutation Patch-Clamp Techniques Potassium - chemistry Potassium - metabolism Potassium Channels, Inwardly Rectifying - physiology Protein Isoforms Protein Structure, Tertiary Protein-Serine-Threonine Kinases - biosynthesis Protein-Serine-Threonine Kinases - metabolism Rats Rats, Sprague-Dawley RNA, Messenger - metabolism RNA, Small Interfering - metabolism Small interfering RNA Transfection WNK Lysine-Deficient Protein Kinase 1 |
| title | Antagonistic Regulation of ROMK by Long and Kidney-Specific WNK1 Isoforms |
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