The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron
Recent studies have identified Rhesus proteins as important molecules for ammonia transport in acid-secreting intercalated cells in the distal nephron. Here, we provide evidence for an additional molecule that can mediate NH3/NH4 excretion, the subtype 2 of the hyperpolarization-activated cyclic nuc...
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| Veröffentlicht in: | Kidney international 2011-10, Vol.80 (8), p.832-840 |
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| creator | Carrisoza-Gaytán, Rolando Rangel, Claudia Salvador, Carolina Saldaña-Meyer, Ricardo Escalona, Christian Satlin, Lisa M. Liu, Wen Zavilowitz, Beth Trujillo, Joyce Bobadilla, Norma A. Escobar, Laura I. |
| description | Recent studies have identified Rhesus proteins as important molecules for ammonia transport in acid-secreting intercalated cells in the distal nephron. Here, we provide evidence for an additional molecule that can mediate NH3/NH4 excretion, the subtype 2 of the hyperpolarization-activated cyclic nucleotide-gated channel family (HCN2), in collecting ducts in rat renal cortex and medulla. Chronic metabolic acidosis in rats did not alter HCN2 protein expression but downregulated the relative abundance of HCN2 mRNA. Its cDNA was identical to the homolog from the brain and the protein was post-translationally modified by N-type glycosylation. Electrophysiological recordings in Xenopus oocytes injected with HCN2 cRNA found that potassium was transported better than ammonium, each of which was transported significantly better than sodium, criteria that are compatible with a role for HCN2 in ammonium transport. In microperfused rat outer medullary collecting duct segments, the initial rate of acidification, upon exposure to a basolateral ammonium chloride pulse, was higher in intercalated than in principal cells. A specific inhibitor of HCN2 (ZD7288) decreased acidification only in intercalated cells from control rats. In rats with chronic metabolic acidosis, the rate of acidification doubled in both intercalated and principal cells; however, ZD7288 had no significant inhibitory effect. Thus, HCN2 is a basolateral ammonium transport pathway of intercalated cells and may contribute to the renal regulation of body pH under basal conditions. |
| doi_str_mv | 10.1038/ki.2011.230 |
| format | Article |
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Here, we provide evidence for an additional molecule that can mediate NH3/NH4 excretion, the subtype 2 of the hyperpolarization-activated cyclic nucleotide-gated channel family (HCN2), in collecting ducts in rat renal cortex and medulla. Chronic metabolic acidosis in rats did not alter HCN2 protein expression but downregulated the relative abundance of HCN2 mRNA. Its cDNA was identical to the homolog from the brain and the protein was post-translationally modified by N-type glycosylation. Electrophysiological recordings in Xenopus oocytes injected with HCN2 cRNA found that potassium was transported better than ammonium, each of which was transported significantly better than sodium, criteria that are compatible with a role for HCN2 in ammonium transport. In microperfused rat outer medullary collecting duct segments, the initial rate of acidification, upon exposure to a basolateral ammonium chloride pulse, was higher in intercalated than in principal cells. A specific inhibitor of HCN2 (ZD7288) decreased acidification only in intercalated cells from control rats. In rats with chronic metabolic acidosis, the rate of acidification doubled in both intercalated and principal cells; however, ZD7288 had no significant inhibitory effect. Thus, HCN2 is a basolateral ammonium transport pathway of intercalated cells and may contribute to the renal regulation of body pH under basal conditions.</description><identifier>ISSN: 0085-2538</identifier><identifier>EISSN: 1523-1755</identifier><identifier>DOI: 10.1038/ki.2011.230</identifier><identifier>PMID: 21796099</identifier><identifier>CODEN: KDYIA5</identifier><language>eng</language><publisher>Basingstoke: Elsevier Inc</publisher><subject>acid-base homeostasis ; Acidification ; Acidosis - metabolism ; Ammonia ; Ammonium ; Ammonium chloride ; Animals ; Biological and medical sciences ; Biological Transport ; Brain ; Collecting duct ; Electrophysiological recording ; Excretion ; Fluorescent Antibody Technique ; Glycosylation ; hyperpolarization-activated cyclic nucleotide-gated channel ; Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels ; intercalated cell ; ion channels (cyclic nucleotide-gated) ; Ion Channels - analysis ; Ion Channels - physiology ; Kidney ; Kidney Tubules - metabolism ; Kidney Tubules, Distal - metabolism ; Medical sciences ; Medulla oblongata ; Metabolic acidosis ; mRNA ; Nephrology. Urinary tract diseases ; Nephrons ; Oocytes ; pH effects ; Post-translation ; Potassium ; Potassium Channels ; Quaternary Ammonium Compounds - metabolism ; Rats ; renal cortex ; Sodium ; Xenopus</subject><ispartof>Kidney international, 2011-10, Vol.80 (8), p.832-840</ispartof><rights>2011 International Society of Nephrology</rights><rights>2015 INIST-CNRS</rights><rights>Copyright Nature Publishing Group Oct 2011</rights><rights>2011 International Society of Nephrology 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c540t-e56d94c324ddfcebc4dd7762c35db0192703d91c814b7645ab8f4087ee92ecab3</citedby><cites>FETCH-LOGICAL-c540t-e56d94c324ddfcebc4dd7762c35db0192703d91c814b7645ab8f4087ee92ecab3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/895324065?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24562356$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21796099$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Carrisoza-Gaytán, Rolando</creatorcontrib><creatorcontrib>Rangel, Claudia</creatorcontrib><creatorcontrib>Salvador, Carolina</creatorcontrib><creatorcontrib>Saldaña-Meyer, Ricardo</creatorcontrib><creatorcontrib>Escalona, Christian</creatorcontrib><creatorcontrib>Satlin, Lisa M.</creatorcontrib><creatorcontrib>Liu, Wen</creatorcontrib><creatorcontrib>Zavilowitz, Beth</creatorcontrib><creatorcontrib>Trujillo, Joyce</creatorcontrib><creatorcontrib>Bobadilla, Norma A.</creatorcontrib><creatorcontrib>Escobar, Laura I.</creatorcontrib><title>The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron</title><title>Kidney international</title><addtitle>Kidney Int</addtitle><description>Recent studies have identified Rhesus proteins as important molecules for ammonia transport in acid-secreting intercalated cells in the distal nephron. Here, we provide evidence for an additional molecule that can mediate NH3/NH4 excretion, the subtype 2 of the hyperpolarization-activated cyclic nucleotide-gated channel family (HCN2), in collecting ducts in rat renal cortex and medulla. Chronic metabolic acidosis in rats did not alter HCN2 protein expression but downregulated the relative abundance of HCN2 mRNA. Its cDNA was identical to the homolog from the brain and the protein was post-translationally modified by N-type glycosylation. Electrophysiological recordings in Xenopus oocytes injected with HCN2 cRNA found that potassium was transported better than ammonium, each of which was transported significantly better than sodium, criteria that are compatible with a role for HCN2 in ammonium transport. In microperfused rat outer medullary collecting duct segments, the initial rate of acidification, upon exposure to a basolateral ammonium chloride pulse, was higher in intercalated than in principal cells. A specific inhibitor of HCN2 (ZD7288) decreased acidification only in intercalated cells from control rats. In rats with chronic metabolic acidosis, the rate of acidification doubled in both intercalated and principal cells; however, ZD7288 had no significant inhibitory effect. Thus, HCN2 is a basolateral ammonium transport pathway of intercalated cells and may contribute to the renal regulation of body pH under basal conditions.</description><subject>acid-base homeostasis</subject><subject>Acidification</subject><subject>Acidosis - metabolism</subject><subject>Ammonia</subject><subject>Ammonium</subject><subject>Ammonium chloride</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Biological Transport</subject><subject>Brain</subject><subject>Collecting duct</subject><subject>Electrophysiological recording</subject><subject>Excretion</subject><subject>Fluorescent Antibody Technique</subject><subject>Glycosylation</subject><subject>hyperpolarization-activated cyclic nucleotide-gated channel</subject><subject>Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels</subject><subject>intercalated cell</subject><subject>ion channels (cyclic nucleotide-gated)</subject><subject>Ion Channels - analysis</subject><subject>Ion Channels - physiology</subject><subject>Kidney</subject><subject>Kidney Tubules - metabolism</subject><subject>Kidney Tubules, Distal - metabolism</subject><subject>Medical sciences</subject><subject>Medulla oblongata</subject><subject>Metabolic acidosis</subject><subject>mRNA</subject><subject>Nephrology. Urinary tract diseases</subject><subject>Nephrons</subject><subject>Oocytes</subject><subject>pH effects</subject><subject>Post-translation</subject><subject>Potassium</subject><subject>Potassium Channels</subject><subject>Quaternary Ammonium Compounds - metabolism</subject><subject>Rats</subject><subject>renal cortex</subject><subject>Sodium</subject><subject>Xenopus</subject><issn>0085-2538</issn><issn>1523-1755</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNp9kcuLFDEQxoMo7jh68q6NIArSYx6dflwEGdQVFr2s55BOqney0520SXpg_OtN2-P4QDwVSf346qv6EHpM8IZgVr_emw3FhGwow3fQinDKclJxfhetMK55TjmrL9CDEG5xejcM30cXlFRNiZtmhez1DrLdcQQ_ul56801G42wuVTQHGUFn6qh6ozI7qR5cNBrymx__l9tPNFM7aS30WfTShtH5GDI5DM6aaciMzWLS1iZE2WcWxp139iG618k-wKNTXaMv799dby_zq88fPm7fXuWKFzjmwEvdFIrRQutOQatSraqSKsZ1i0lDK8x0Q1RNirYqCy7buitwXQE0FJRs2Rq9WXTHqR1AK7DJYi9Gbwbpj8JJI_7sWLMTN-4gWJXuV9Ak8OIk4N3XCUIUgwkK-l5acFMQdcNrXs3wGr38L0lww4qSpHQS-uwv9NZN3qZDzHppW1zyBL1aIOVdCB66s2uCxRy42BsxBy4WySe_L3pmfyacgOcnQAYl-y4lpUz4xRW8pIyXiXu6cFbGycMZ2Jt51jKKLwSk4A4GvAjKgFWgjQcVhXbmnxa_A-RU0co</recordid><startdate>20111001</startdate><enddate>20111001</enddate><creator>Carrisoza-Gaytán, Rolando</creator><creator>Rangel, Claudia</creator><creator>Salvador, Carolina</creator><creator>Saldaña-Meyer, Ricardo</creator><creator>Escalona, Christian</creator><creator>Satlin, Lisa M.</creator><creator>Liu, Wen</creator><creator>Zavilowitz, Beth</creator><creator>Trujillo, Joyce</creator><creator>Bobadilla, Norma A.</creator><creator>Escobar, Laura I.</creator><general>Elsevier Inc</general><general>Nature Publishing Group</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><scope>IQODW</scope><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>3V.</scope><scope>7QP</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7TM</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20111001</creationdate><title>The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron</title><author>Carrisoza-Gaytán, Rolando ; Rangel, Claudia ; Salvador, Carolina ; Saldaña-Meyer, Ricardo ; Escalona, Christian ; Satlin, Lisa M. ; Liu, Wen ; Zavilowitz, Beth ; Trujillo, Joyce ; Bobadilla, Norma A. ; Escobar, Laura I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c540t-e56d94c324ddfcebc4dd7762c35db0192703d91c814b7645ab8f4087ee92ecab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>acid-base homeostasis</topic><topic>Acidification</topic><topic>Acidosis - metabolism</topic><topic>Ammonia</topic><topic>Ammonium</topic><topic>Ammonium chloride</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Biological Transport</topic><topic>Brain</topic><topic>Collecting duct</topic><topic>Electrophysiological recording</topic><topic>Excretion</topic><topic>Fluorescent Antibody Technique</topic><topic>Glycosylation</topic><topic>hyperpolarization-activated cyclic nucleotide-gated channel</topic><topic>Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels</topic><topic>intercalated cell</topic><topic>ion channels (cyclic nucleotide-gated)</topic><topic>Ion Channels - analysis</topic><topic>Ion Channels - physiology</topic><topic>Kidney</topic><topic>Kidney Tubules - metabolism</topic><topic>Kidney Tubules, Distal - metabolism</topic><topic>Medical sciences</topic><topic>Medulla oblongata</topic><topic>Metabolic acidosis</topic><topic>mRNA</topic><topic>Nephrology. Urinary tract diseases</topic><topic>Nephrons</topic><topic>Oocytes</topic><topic>pH effects</topic><topic>Post-translation</topic><topic>Potassium</topic><topic>Potassium Channels</topic><topic>Quaternary Ammonium Compounds - metabolism</topic><topic>Rats</topic><topic>renal cortex</topic><topic>Sodium</topic><topic>Xenopus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Carrisoza-Gaytán, Rolando</creatorcontrib><creatorcontrib>Rangel, Claudia</creatorcontrib><creatorcontrib>Salvador, Carolina</creatorcontrib><creatorcontrib>Saldaña-Meyer, Ricardo</creatorcontrib><creatorcontrib>Escalona, Christian</creatorcontrib><creatorcontrib>Satlin, Lisa M.</creatorcontrib><creatorcontrib>Liu, Wen</creatorcontrib><creatorcontrib>Zavilowitz, Beth</creatorcontrib><creatorcontrib>Trujillo, Joyce</creatorcontrib><creatorcontrib>Bobadilla, Norma A.</creatorcontrib><creatorcontrib>Escobar, Laura I.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Nucleic Acids Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Kidney international</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Carrisoza-Gaytán, Rolando</au><au>Rangel, Claudia</au><au>Salvador, Carolina</au><au>Saldaña-Meyer, Ricardo</au><au>Escalona, Christian</au><au>Satlin, Lisa M.</au><au>Liu, Wen</au><au>Zavilowitz, Beth</au><au>Trujillo, Joyce</au><au>Bobadilla, Norma A.</au><au>Escobar, Laura I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron</atitle><jtitle>Kidney international</jtitle><addtitle>Kidney Int</addtitle><date>2011-10-01</date><risdate>2011</risdate><volume>80</volume><issue>8</issue><spage>832</spage><epage>840</epage><pages>832-840</pages><issn>0085-2538</issn><eissn>1523-1755</eissn><coden>KDYIA5</coden><abstract>Recent studies have identified Rhesus proteins as important molecules for ammonia transport in acid-secreting intercalated cells in the distal nephron. Here, we provide evidence for an additional molecule that can mediate NH3/NH4 excretion, the subtype 2 of the hyperpolarization-activated cyclic nucleotide-gated channel family (HCN2), in collecting ducts in rat renal cortex and medulla. Chronic metabolic acidosis in rats did not alter HCN2 protein expression but downregulated the relative abundance of HCN2 mRNA. Its cDNA was identical to the homolog from the brain and the protein was post-translationally modified by N-type glycosylation. Electrophysiological recordings in Xenopus oocytes injected with HCN2 cRNA found that potassium was transported better than ammonium, each of which was transported significantly better than sodium, criteria that are compatible with a role for HCN2 in ammonium transport. In microperfused rat outer medullary collecting duct segments, the initial rate of acidification, upon exposure to a basolateral ammonium chloride pulse, was higher in intercalated than in principal cells. A specific inhibitor of HCN2 (ZD7288) decreased acidification only in intercalated cells from control rats. In rats with chronic metabolic acidosis, the rate of acidification doubled in both intercalated and principal cells; however, ZD7288 had no significant inhibitory effect. Thus, HCN2 is a basolateral ammonium transport pathway of intercalated cells and may contribute to the renal regulation of body pH under basal conditions.</abstract><cop>Basingstoke</cop><pub>Elsevier Inc</pub><pmid>21796099</pmid><doi>10.1038/ki.2011.230</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | acid-base homeostasis Acidification Acidosis - metabolism Ammonia Ammonium Ammonium chloride Animals Biological and medical sciences Biological Transport Brain Collecting duct Electrophysiological recording Excretion Fluorescent Antibody Technique Glycosylation hyperpolarization-activated cyclic nucleotide-gated channel Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels intercalated cell ion channels (cyclic nucleotide-gated) Ion Channels - analysis Ion Channels - physiology Kidney Kidney Tubules - metabolism Kidney Tubules, Distal - metabolism Medical sciences Medulla oblongata Metabolic acidosis mRNA Nephrology. Urinary tract diseases Nephrons Oocytes pH effects Post-translation Potassium Potassium Channels Quaternary Ammonium Compounds - metabolism Rats renal cortex Sodium Xenopus |
| title | The hyperpolarization-activated cyclic nucleotide-gated HCN2 channel transports ammonium in the distal nephron |
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