Renal expression of osmotically responsive cation channel TRPV4 is restricted to water-impermeant nephron segments

Wei Tian, Michele Salanova, Hongshi Xu, Jessie N. Lindsley, Terry T. Oyama, Sharon Anderson, Sebastian Bachmann, David Cohen

Research output: Contribution to journalArticle

102 Citations (Scopus)

Abstract

TRPV4, a nonselective cation channel of the transient receptor potential (TRP) family, is gated by hypotonicity. Expression of TRPV4 mRNA has been detected in the circumventricular organs of the brain responsible for sensing systemic tonicity and in the kidney distal convoluted tubule (DCT), among other sites. No analysis of TRPV4 expression at the protein level has been undertaken and no systematic analysis of expression of this channel has been reported in the kidney. Via RNAse protection assay and immunoblotting, abundant expression of TRPV4 was detected in the cortex, medulla, and papilla. The expression pattern of TRPV4 was characterized in both rat and mouse kidney, which revealed similar patterns of immunoreactivity. TRPV4 expression was absent from the proximal tubule (PT) and descending thin limb (DTL), whereas the strongest expression was observed in the ascending thin limb (ATL). The thick ascending limb (TAL) was strongly positive as was the DCT and connecting tubule. Importantly, the water-permeant cells of the macula densa were unstained. Moderate TRPV4 expression was noted in all collecting duct portions and in papillary epithelium; intercalated cells (type A) exhibited a particularly strong signal. In all positive segments, TRPV4 expression was concentrated at the basolateral membrane. Therefore, TRPV4 is expressed in only those nephron segments that are constitutively (i.e., ATL, TAL, and DCT) or conditionally (i.e., collecting duct) water impermeant and where generation of a substantial transcellular osmotic gradient could be expected. TRPV4 expression is absent from nephron segments exhibiting constitutive water permeability and unregulated apical aquaporin expression (i.e., PT and DTL). These data, although circumstantial, are consistent with a role for TRPV4 in the response to anisotonicity in the mammalian kidney.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Renal Physiology
Volume287
Issue number1 56-1
DOIs
StatePublished - Jul 2004

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Nephrons
Cations
Extremities
Kidney
Water
Distal Kidney Tubule
Transient Receptor Potential Channels
Aquaporins
Immunoblotting
Permeability
Epithelium
Messenger RNA
Membranes
Brain
Proteins

Keywords

  • Transient receptor potential
  • Water permeability

ASJC Scopus subject areas

  • Physiology

Cite this

Renal expression of osmotically responsive cation channel TRPV4 is restricted to water-impermeant nephron segments. / Tian, Wei; Salanova, Michele; Xu, Hongshi; Lindsley, Jessie N.; Oyama, Terry T.; Anderson, Sharon; Bachmann, Sebastian; Cohen, David.

In: American Journal of Physiology - Renal Physiology, Vol. 287, No. 1 56-1, 07.2004.

Research output: Contribution to journalArticle

Tian, Wei ; Salanova, Michele ; Xu, Hongshi ; Lindsley, Jessie N. ; Oyama, Terry T. ; Anderson, Sharon ; Bachmann, Sebastian ; Cohen, David. / Renal expression of osmotically responsive cation channel TRPV4 is restricted to water-impermeant nephron segments. In: American Journal of Physiology - Renal Physiology. 2004 ; Vol. 287, No. 1 56-1.
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abstract = "TRPV4, a nonselective cation channel of the transient receptor potential (TRP) family, is gated by hypotonicity. Expression of TRPV4 mRNA has been detected in the circumventricular organs of the brain responsible for sensing systemic tonicity and in the kidney distal convoluted tubule (DCT), among other sites. No analysis of TRPV4 expression at the protein level has been undertaken and no systematic analysis of expression of this channel has been reported in the kidney. Via RNAse protection assay and immunoblotting, abundant expression of TRPV4 was detected in the cortex, medulla, and papilla. The expression pattern of TRPV4 was characterized in both rat and mouse kidney, which revealed similar patterns of immunoreactivity. TRPV4 expression was absent from the proximal tubule (PT) and descending thin limb (DTL), whereas the strongest expression was observed in the ascending thin limb (ATL). The thick ascending limb (TAL) was strongly positive as was the DCT and connecting tubule. Importantly, the water-permeant cells of the macula densa were unstained. Moderate TRPV4 expression was noted in all collecting duct portions and in papillary epithelium; intercalated cells (type A) exhibited a particularly strong signal. In all positive segments, TRPV4 expression was concentrated at the basolateral membrane. Therefore, TRPV4 is expressed in only those nephron segments that are constitutively (i.e., ATL, TAL, and DCT) or conditionally (i.e., collecting duct) water impermeant and where generation of a substantial transcellular osmotic gradient could be expected. TRPV4 expression is absent from nephron segments exhibiting constitutive water permeability and unregulated apical aquaporin expression (i.e., PT and DTL). These data, although circumstantial, are consistent with a role for TRPV4 in the response to anisotonicity in the mammalian kidney.",
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AU - Tian, Wei

AU - Salanova, Michele

AU - Xu, Hongshi

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AU - Oyama, Terry T.

AU - Anderson, Sharon

AU - Bachmann, Sebastian

AU - Cohen, David

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