Independent regulation of Piezo1 activity by principal and intercalated cells of the collecting duct

Pyrshev, Kyrylo; Atamanchuk-Stavniichuk, Anna; Kordysh, Mariya; Zaika, Oleg; Tomilin, Viktor N.; Pochynyuk, Oleh

doi:10.1016/j.jbc.2023.105524

Cited by 6 publications

(2 citation statements)

References 52 publications

(105 reference statements)

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“…We observed that an HK diet increases both PIEZO1 expression in ICs and PCs ( Figure 4 ) and PIEZO1 functional activity, as demonstrated by Yoda1-dependent increases in [Ca 2+ ] i in ICs and well as PCs ( Figure 2 ). In contrast, recent work by Pyrshev et al did not observe an increase in PIEZO1 expression in response to an HK diet (although immunofluorescence was not quantified), and the authors did not examine changes in [Ca 2+ ] i in response to an increase in tubular flow ( 16 ). It is unclear why these potentially discrepant results were observed, and the mechanisms by which an HK diet increases PIEZO1 expression and activity (based on our observations) remain to be defined.…”

Section: Discussionmentioning

confidence: 88%

“…The apical cilia decorating PCs and apical microvilli/microplicae of ICs have been proposed to sense fluid flow ( 9 ); however, how these pathways would regulate basolateral Ca 2+ entry is unknown. One possible candidate is PIEZO1, a mechanoactivated nonselective cation channel ( 13 , 14 ) that is selectively localized to the basolateral surface of epithelial cells in mouse ASDN ( 15 ), although basolateral and apical expression of PIEZO1 was recently reported by Pyrshev et al ( 16 ). Numerous studies report that PIEZO1 and its closely related family member PIEZO2 function as mechanosensors, which are directly activated by cell membrane tension generated in response to membrane stretch or fluid shear stress ( 17 , 18 ).…”

Section: Introductionmentioning

confidence: 99%

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PIEZO1 is a distal nephron mechanosensor and is required for flow-induced K+ secretion

Carrisoza-Gaytan,

Mutchler,

Carattino

et al. 2024

Journal of Clinical Investigation

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Ca 2+ -activated BK channels in renal intercalated cells (ICs) mediate luminal flow–induced K + secretion (FIKS), but how ICs sense increased flow remains uncertain. We examined whether PIEZO1, a mechanosensitive Ca 2+ -permeable channel expressed in the basolateral membranes of ICs, is required for FIKS. In isolated cortical collecting ducts (CCDs), the mechanosensitive cation-selective channel inhibitor GsMTx4 dampened flow-induced increases in intracellular Ca 2+ concentration ([Ca 2+ ] i ), whereas the PIEZO1 activator Yoda1 increased [Ca 2+ ] i and BK channel activity. CCDs from mice fed a high-K + (HK) diet exhibited a greater Yoda1-dependent increase in [Ca 2+ ] i than CCDs from mice fed a control K + diet. ICs in CCDs isolated from mice with a targeted gene deletion of Piezo1 in ICs (IC- Piezo1 -KO) exhibited a blunted [Ca 2+ ] i response to Yoda1 or increased flow, with an associated loss of FIKS in CCDs. Male IC- Piezo1 -KO mice selectively exhibited an increased blood [K + ] in response to an oral K + bolus and blunted urinary K + excretion following a volume challenge. Whole-cell expression of BKα subunit was reduced in ICs of IC- Piezo1 -KO mice fed an HK diet. We conclude that PIEZO1 mediates flow-induced basolateral Ca 2+ entry into ICs, is upregulated in the CCD in response to an HK diet, and is necessary for FIKS.

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Section: Discussionmentioning

confidence: 88%

Section: Introductionmentioning

confidence: 99%

PIEZO1 is a distal nephron mechanosensor and is required for flow-induced K+ secretion

Carrisoza-Gaytan,

Mutchler,

Carattino

et al. 2024

Journal of Clinical Investigation

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Dietary potassium loads call on intercalated cell PIEZO1 to go with the flow

Alper,

Chebib

2024

Kidney International

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Postnatal renal tubule development: roles of tubular flow and flux

Cheng,

Chen,

Cheng

2024

Current Opinion in Nephrology &Amp; Hypertension

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Purpose of review Postnatal renal tubule development is critical to adult kidney function. Several postnatal changes regulate the differentiation and proliferation of renal tubular cells. Here, we review the literature and our efforts on thick ascending limb (TAL) development in Bartter syndrome (BS). Recent findings Glomerular filtrate quickly increases after birth, imposing fluid shear stress and circumferential stretch on immature renal tubules. Recent studies showed that kidney organoids under flow (superfusion) have better development of tubular structures and the expression of cilia and solute transporters. These effects are likely mediated by mechanosensors, such as cilia and the piezo1 channel. Improved renal oxygenation and sodium pump-dependent active transport can stimulate mitochondrial respiration and biogenesis. The functional coupling between transport and mitochondria ensures ATP supply for energy-demanding reactions in tubular cells, including cell cycle progression and proliferation. We recently discovered that postnatal renal medulla maturation and TAL elongation are impaired in Clc-k2-deficient BS mice. Primary cultured Clc-k2-deficient TAL cells have G1-S transition and proliferation delay. These developmental defects could be part of the early pathogenesis of BS and worsen the phenotype. Summary Understanding how tubular flow and transepithelial ion fluxes regulate renal tubule development may improve the treatment of congenital renal tubulopathies.

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Independent regulation of Piezo1 activity by principal and intercalated cells of the collecting duct

Cited by 6 publications

References 52 publications

PIEZO1 is a distal nephron mechanosensor and is required for flow-induced K+ secretion

PIEZO1 is a distal nephron mechanosensor and is required for flow-induced K+ secretion

Dietary potassium loads call on intercalated cell PIEZO1 to go with the flow

Postnatal renal tubule development: roles of tubular flow and flux

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