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Compensatory regulation of Na+ absorption by Na+/H+ exchanger and Na+-Cl- cotransporter in zebrafish (Danio rerio).

Chang WJ, Wang YF, Hu HJ, Wang JH, Lee TH, Hwang PP - Front. Zool. (2013)

Bottom Line: Environmental acid stress suppressed nhe3b expression in HR cells and decreased Na+ content, which was followed by up-regulation of NCC cells accompanied by recovery of Na+ content.Moreover, knockdown of ncc resulted in a significant decrease of Na+ content in acid-acclimated zebrafish.These results provide evidence that HR and NCC cells exhibit functional redundancy in Na+ absorption, similar to the regulatory mechanisms in mammalian kidney, and suggest this functional redundancy is a critical strategy used by zebrafish to survive in a harsh environment that disturbs body fluid Na+ homeostasis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan. pphwang@gate.sinica.edu.tw.

ABSTRACT

Introduction: In mammals, internal Na+ homeostasis is maintained through Na+ reabsorption via a variety of Na+ transport proteins with mutually compensating functions, which are expressed in different segments of the nephrons. In zebrafish, Na+ homeostasis is achieved mainly through the skin/gill ionocytes, namely Na+/H+ exchanger (NHE3b)-expressing H+-ATPase rich (HR) cells and Na+-Cl- cotransporter (NCC)-expressing NCC cells, which are functionally homologous to mammalian proximal and distal convoluted tubular cells, respectively. The present study aimed to investigate whether or not the functions of HR and NCC ionocytes are differentially regulated to compensate for disruptions of internal Na+ homeostasis and if the cell differentiation of the ionocytes is involved in this regulation pathway.

Results: Translational knockdown of ncc caused an increase in HR cell number and a resulting augmentation of Na+ uptake in zebrafish larvae, while NHE3b loss-of-function caused an increase in NCC cell number with a concomitant recovery of Na+ absorption. Environmental acid stress suppressed nhe3b expression in HR cells and decreased Na+ content, which was followed by up-regulation of NCC cells accompanied by recovery of Na+ content. Moreover, knockdown of ncc resulted in a significant decrease of Na+ content in acid-acclimated zebrafish.

Conclusions: These results provide evidence that HR and NCC cells exhibit functional redundancy in Na+ absorption, similar to the regulatory mechanisms in mammalian kidney, and suggest this functional redundancy is a critical strategy used by zebrafish to survive in a harsh environment that disturbs body fluid Na+ homeostasis.

No MeSH data available.


Knockdown of nhe3b increases NCC cell number. (A, B): NCC (arrow) immunostaining images of 5-dpf wild type larvae (WT) and nhe3b morphants. Scale bar = 100 μm. (C): Comparison of NCC cell number in different areas between 5-dpf wild type larvae (white bars) and nhe3b morphants (gray bars) (n = 8). (D): Whole body Na+ content in wild type larvae (white bars) and nhe3b morphants (gray bars) at different developmental stages (n = 6). Mean ± SD. *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
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Figure 3: Knockdown of nhe3b increases NCC cell number. (A, B): NCC (arrow) immunostaining images of 5-dpf wild type larvae (WT) and nhe3b morphants. Scale bar = 100 μm. (C): Comparison of NCC cell number in different areas between 5-dpf wild type larvae (white bars) and nhe3b morphants (gray bars) (n = 8). (D): Whole body Na+ content in wild type larvae (white bars) and nhe3b morphants (gray bars) at different developmental stages (n = 6). Mean ± SD. *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).

Mentions: A similar compensatory effect was also observed in nhe3b morphants. NCC cells were increased in 5-dpf nhe3b morphants as compared to wild type larvae, and the increase was mainly observed in the head region of the morphants (Figure 3A-C). Knockdown of nhe3b significantly decreased Na+ accumulation in the larvae from as early as 2 dpf, but levels had begun to recover by 5 dpf (Figure 3D). As for gcm2 knockdown, down-regulation of nhe3b translation impairs Na+ uptake, which is thereafter compensated by enhanced NCC cell differentiation and Na+ absorption ability.


Compensatory regulation of Na+ absorption by Na+/H+ exchanger and Na+-Cl- cotransporter in zebrafish (Danio rerio).

Chang WJ, Wang YF, Hu HJ, Wang JH, Lee TH, Hwang PP - Front. Zool. (2013)

Knockdown of nhe3b increases NCC cell number. (A, B): NCC (arrow) immunostaining images of 5-dpf wild type larvae (WT) and nhe3b morphants. Scale bar = 100 μm. (C): Comparison of NCC cell number in different areas between 5-dpf wild type larvae (white bars) and nhe3b morphants (gray bars) (n = 8). (D): Whole body Na+ content in wild type larvae (white bars) and nhe3b morphants (gray bars) at different developmental stages (n = 6). Mean ± SD. *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750650&req=5

Figure 3: Knockdown of nhe3b increases NCC cell number. (A, B): NCC (arrow) immunostaining images of 5-dpf wild type larvae (WT) and nhe3b morphants. Scale bar = 100 μm. (C): Comparison of NCC cell number in different areas between 5-dpf wild type larvae (white bars) and nhe3b morphants (gray bars) (n = 8). (D): Whole body Na+ content in wild type larvae (white bars) and nhe3b morphants (gray bars) at different developmental stages (n = 6). Mean ± SD. *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
Mentions: A similar compensatory effect was also observed in nhe3b morphants. NCC cells were increased in 5-dpf nhe3b morphants as compared to wild type larvae, and the increase was mainly observed in the head region of the morphants (Figure 3A-C). Knockdown of nhe3b significantly decreased Na+ accumulation in the larvae from as early as 2 dpf, but levels had begun to recover by 5 dpf (Figure 3D). As for gcm2 knockdown, down-regulation of nhe3b translation impairs Na+ uptake, which is thereafter compensated by enhanced NCC cell differentiation and Na+ absorption ability.

Bottom Line: Environmental acid stress suppressed nhe3b expression in HR cells and decreased Na+ content, which was followed by up-regulation of NCC cells accompanied by recovery of Na+ content.Moreover, knockdown of ncc resulted in a significant decrease of Na+ content in acid-acclimated zebrafish.These results provide evidence that HR and NCC cells exhibit functional redundancy in Na+ absorption, similar to the regulatory mechanisms in mammalian kidney, and suggest this functional redundancy is a critical strategy used by zebrafish to survive in a harsh environment that disturbs body fluid Na+ homeostasis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan. pphwang@gate.sinica.edu.tw.

ABSTRACT

Introduction: In mammals, internal Na+ homeostasis is maintained through Na+ reabsorption via a variety of Na+ transport proteins with mutually compensating functions, which are expressed in different segments of the nephrons. In zebrafish, Na+ homeostasis is achieved mainly through the skin/gill ionocytes, namely Na+/H+ exchanger (NHE3b)-expressing H+-ATPase rich (HR) cells and Na+-Cl- cotransporter (NCC)-expressing NCC cells, which are functionally homologous to mammalian proximal and distal convoluted tubular cells, respectively. The present study aimed to investigate whether or not the functions of HR and NCC ionocytes are differentially regulated to compensate for disruptions of internal Na+ homeostasis and if the cell differentiation of the ionocytes is involved in this regulation pathway.

Results: Translational knockdown of ncc caused an increase in HR cell number and a resulting augmentation of Na+ uptake in zebrafish larvae, while NHE3b loss-of-function caused an increase in NCC cell number with a concomitant recovery of Na+ absorption. Environmental acid stress suppressed nhe3b expression in HR cells and decreased Na+ content, which was followed by up-regulation of NCC cells accompanied by recovery of Na+ content. Moreover, knockdown of ncc resulted in a significant decrease of Na+ content in acid-acclimated zebrafish.

Conclusions: These results provide evidence that HR and NCC cells exhibit functional redundancy in Na+ absorption, similar to the regulatory mechanisms in mammalian kidney, and suggest this functional redundancy is a critical strategy used by zebrafish to survive in a harsh environment that disturbs body fluid Na+ homeostasis.

No MeSH data available.