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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.


Related in: MedlinePlus

Effects of acid stress on Na+ accumulation and NCC expression in zebrafish larvae. (A, B): Comparison of whole body Na+ content (A) and ncc mRNA expression (B) in larvae treated with control pH7 (white bars) or acidic pH4 FW (gray bars) for 4 d. Mean ± SD (n = 6). (C, D): Immunostaining images of NCC (arrow) in 4-dpf larvae under pH7 or pH4 FW for 4 d. Scale bar = 100 μm. (E): Comparison of NCC cell number in different areas of 4-dpf larvae treated with pH7 (white bars) or pH4 FW (gray bars) (n = 8). *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
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Figure 6: Effects of acid stress on Na+ accumulation and NCC expression in zebrafish larvae. (A, B): Comparison of whole body Na+ content (A) and ncc mRNA expression (B) in larvae treated with control pH7 (white bars) or acidic pH4 FW (gray bars) for 4 d. Mean ± SD (n = 6). (C, D): Immunostaining images of NCC (arrow) in 4-dpf larvae under pH7 or pH4 FW for 4 d. Scale bar = 100 μm. (E): Comparison of NCC cell number in different areas of 4-dpf larvae treated with pH7 (white bars) or pH4 FW (gray bars) (n = 8). *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).

Mentions: Whole body Na+ content was significantly decreased in acid-acclimated larvae as compared to controls raised in pH 7 FW during the first 2~3 d (Figure 6A); however, the difference between test and control groups declined by 4 dpf, suggesting a recovery of Na+ absorption ability in the acid-acclimated larvae. In addition, expression of ncc mRNA in larvae was significantly increased after 3~4 d acid treatment (Figure 6B), and NCC cell number in the head region, and thus larval skin overall, was also increased after acid acclimation (Figure 6C-E). This suggests that the recovery of Na+ accumulation may have resulted from increased ncc expression and NCC cell differentiation during acid acclimation.


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)

Effects of acid stress on Na+ accumulation and NCC expression in zebrafish larvae. (A, B): Comparison of whole body Na+ content (A) and ncc mRNA expression (B) in larvae treated with control pH7 (white bars) or acidic pH4 FW (gray bars) for 4 d. Mean ± SD (n = 6). (C, D): Immunostaining images of NCC (arrow) in 4-dpf larvae under pH7 or pH4 FW for 4 d. Scale bar = 100 μm. (E): Comparison of NCC cell number in different areas of 4-dpf larvae treated with pH7 (white bars) or pH4 FW (gray bars) (n = 8). *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 6: Effects of acid stress on Na+ accumulation and NCC expression in zebrafish larvae. (A, B): Comparison of whole body Na+ content (A) and ncc mRNA expression (B) in larvae treated with control pH7 (white bars) or acidic pH4 FW (gray bars) for 4 d. Mean ± SD (n = 6). (C, D): Immunostaining images of NCC (arrow) in 4-dpf larvae under pH7 or pH4 FW for 4 d. Scale bar = 100 μm. (E): Comparison of NCC cell number in different areas of 4-dpf larvae treated with pH7 (white bars) or pH4 FW (gray bars) (n = 8). *p < 0.05; **p < 0.01; ***p < 0.001 (Student’s t-test).
Mentions: Whole body Na+ content was significantly decreased in acid-acclimated larvae as compared to controls raised in pH 7 FW during the first 2~3 d (Figure 6A); however, the difference between test and control groups declined by 4 dpf, suggesting a recovery of Na+ absorption ability in the acid-acclimated larvae. In addition, expression of ncc mRNA in larvae was significantly increased after 3~4 d acid treatment (Figure 6B), and NCC cell number in the head region, and thus larval skin overall, was also increased after acid acclimation (Figure 6C-E). This suggests that the recovery of Na+ accumulation may have resulted from increased ncc expression and NCC cell differentiation during acid acclimation.

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.


Related in: MedlinePlus