Morphological and functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption

Abstract

functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption. Am J Physiol Regul Integr Comp Physiol 307: R1381-R1395, 2014. First published October 22, 2014 doi:10.1152/ajpregu.00033.2014.-For adaptation to highsalinity marine environments, cartilaginous fishes (sharks, skates, rays, and chimaeras) adopt a unique urea-based osmoregulation strategy. Their kidneys reabsorb nearly all filtered urea from the primary urine, and this is an essential component of urea retention in their body fluid. Anatomical investigations have revealed the extraordinarily elaborate nephron system in the kidney of cartilaginous fishes, e.g., the four-loop configuration of each nephron, the occurrence of distinct sinus and bundle zones, and the sac-like peritubular sheath in the bundle zone, in which the nephron segments are arranged in a countercurrent fashion. These anatomical and morphological characteristics have been considered to be important for urea reabsorption; however, a mechanism for urea reabsorption is still largely unknown. This review focuses on recent progress in the identification and mapping of various pumps, channels, and transporters on the nephron segments in the kidney of cartilaginous fishes. The molecules include urea transporters, Na, and aquaporins, which most probably all contribute to the urea reabsorption process. Although research is still in progress, a possible model for urea reabsorption in the kidney of cartilaginous fishes is discussed based on the anatomical features of nephron segments and vascular systems and on the results of molecular mapping. The molecular anatomical approach thus provides a powerful tool for understanding the physiological processes that take place in the highly elaborate kidney of cartilaginous fishes. cartilaginous fish; kidney; osmoregulation; transporters; urea BODY FLUID REGULATION is essential for all organisms to survive in their respective habitats, including freshwater (FW), seawater (SW), and terrestrial environments. It is well known that teleost fish regulate their plasma Na ϩ and Cl Ϫ concentrations and osmolality at levels about one-third of SW. Meanwhile, cartilaginous fishes (sharks, skates, rays, and chimaeras) have adopted a unique osmoregulatory strategy for adaptation to the high-salinity marine environment. Cartilaginous fishes control plasma ions to levels approximately one-half of surrounding SW while they store high concentrations of the nitrogenous compound urea as an osmolyte (the so-called "ureosmotic strategy"). As a result, their body fluids are slightly hyperosmotic to surrounding SW (for instance, plasma osmolality of houndshark is 1,000 mosmol/kg H 2 O in SW of 988 mosmol/kg H 2 O; Ref. 53), and thus cartilaginous fishes do not typically suffer dehydration even in the high-osmolality SW environment. To maintain high concentration of urea in the body, urea production by the ornithine urea cycle (OUC) is essential. Investigations on the OUC enzymes have proved that the liver is the primary organ f...

Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii)

“…7K) and the early distal tubule (EDT) in the bundle zone (Fig. 7L), as previously described (17). No colocalization was observed between cmNKCC2 mRNA (black arrowheads) and the hybridization signals for cmSlc26a1 and cmSlc26a6 mRNAs (black arrows).…”

Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii)

“…7K) and the early distal tubule (EDT) in the bundle zone (Fig. 7L), as previously described (17). No colocalization was observed between cmNKCC2 mRNA (black arrowheads) and the hybridization signals for cmSlc26a1 and cmSlc26a6 mRNAs (black arrows).…”

Molecular and morphological investigations on the renal mechanisms enabling euryhalinity of red stingray Hemitrygon akajei

“…In addition to NaCl, the estimated reabsorption rate for urea was also increased in the stingray acclimated to low-salinity environments. The mechanism for the higher urea reabsorption in low-salinity environments is probably explainable with the urea reabsorption model proposed in cartilaginous fish ( Figure 5 ; Hyodo et al, 2014 ). This model is composed of three steps: 1) active reabsorption of NaCl, 2) passive reabsorption of water, and 3) facilitative urea reabsorption in the bundle zone.…”

“…Using qPCR, we subsequently investigated the expression levels of nkcc2 , nkaα1 , urea transporter ( ut ), and ncc that have been reported to be important for NaCl and urea reabsorption of the kidney in cartilaginous fishes ( Hyodo et al, 2014 ; Imaseki et al, 2019 ; Aburatani et al, 2020 ). The expression levels of nkcc2 and nkaα1 mRNAs in the kidney of FW-acclimated stingray were significantly higher than those of SW control individuals (1.7- and 2.6-fold, respectively; Figures 2A, B ).…”

Comprehensive analysis of genes contributing to euryhalinity in the bull shark, Carcharhinus leucas ; Na+-Cl− co-transporter is one of the key renal factors up-regulated in acclimation to low-salinity environment in bull sharks, but not in houndsharks, Triakis scyllium

“…Currently, the function of the LDT in SW environment remains to be clarified. In elephant fish and houndsharks, NKCC2 mRNA is expressed in the LDT ( present study and Kakumura et al, 2015), and the LDT is considered to be important for concentrating urea for subsequent urea reabsorption in the CT (Hyodo et al, 2014). However, in the bull shark kidney in a SW environment, neither NKCC2 nor NCC was observed in the LDT (Fig.…”

Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii)

“…7K) and the early distal tubule (EDT) in the bundle zone (Fig. 7L), as previously described (17). No colocalization was observed between cmNKCC2 mRNA (black arrowheads) and the hybridization signals for cmSlc26a1 and cmSlc26a6 mRNAs (black arrows).…”

Molecular and morphological investigations on the renal mechanisms enabling euryhalinity of red stingray Hemitrygon akajei

“…In addition to NaCl, the estimated reabsorption rate for urea was also increased in the stingray acclimated to low-salinity environments. The mechanism for the higher urea reabsorption in low-salinity environments is probably explainable with the urea reabsorption model proposed in cartilaginous fish ( Figure 5 ; Hyodo et al, 2014 ). This model is composed of three steps: 1) active reabsorption of NaCl, 2) passive reabsorption of water, and 3) facilitative urea reabsorption in the bundle zone.…”

“…Using qPCR, we subsequently investigated the expression levels of nkcc2 , nkaα1 , urea transporter ( ut ), and ncc that have been reported to be important for NaCl and urea reabsorption of the kidney in cartilaginous fishes ( Hyodo et al, 2014 ; Imaseki et al, 2019 ; Aburatani et al, 2020 ). The expression levels of nkcc2 and nkaα1 mRNAs in the kidney of FW-acclimated stingray were significantly higher than those of SW control individuals (1.7- and 2.6-fold, respectively; Figures 2A, B ).…”

Comprehensive analysis of genes contributing to euryhalinity in the bull shark, Carcharhinus leucas ; Na+-Cl− co-transporter is one of the key renal factors up-regulated in acclimation to low-salinity environment in bull sharks, but not in houndsharks, Triakis scyllium

“…Currently, the function of the LDT in SW environment remains to be clarified. In elephant fish and houndsharks, NKCC2 mRNA is expressed in the LDT ( present study and Kakumura et al, 2015), and the LDT is considered to be important for concentrating urea for subsequent urea reabsorption in the CT (Hyodo et al, 2014). However, in the bull shark kidney in a SW environment, neither NKCC2 nor NCC was observed in the LDT (Fig.…”

Sulfate transporters involved in sulfate secretion in the kidney are localized in the renal proximal tubule II of the elephant fish (Callorhinchus milii)

“…7K) and the early distal tubule (EDT) in the bundle zone (Fig. 7L), as previously described (17). No colocalization was observed between cmNKCC2 mRNA (black arrowheads) and the hybridization signals for cmSlc26a1 and cmSlc26a6 mRNAs (black arrows).…”

Molecular and morphological investigations on the renal mechanisms enabling euryhalinity of red stingray Hemitrygon akajei

“…In addition to NaCl, the estimated reabsorption rate for urea was also increased in the stingray acclimated to low-salinity environments. The mechanism for the higher urea reabsorption in low-salinity environments is probably explainable with the urea reabsorption model proposed in cartilaginous fish ( Figure 5 ; Hyodo et al, 2014 ). This model is composed of three steps: 1) active reabsorption of NaCl, 2) passive reabsorption of water, and 3) facilitative urea reabsorption in the bundle zone.…”

“…Using qPCR, we subsequently investigated the expression levels of nkcc2 , nkaα1 , urea transporter ( ut ), and ncc that have been reported to be important for NaCl and urea reabsorption of the kidney in cartilaginous fishes ( Hyodo et al, 2014 ; Imaseki et al, 2019 ; Aburatani et al, 2020 ). The expression levels of nkcc2 and nkaα1 mRNAs in the kidney of FW-acclimated stingray were significantly higher than those of SW control individuals (1.7- and 2.6-fold, respectively; Figures 2A, B ).…”

Comprehensive analysis of genes contributing to euryhalinity in the bull shark, Carcharhinus leucas ; Na+-Cl− co-transporter is one of the key renal factors up-regulated in acclimation to low-salinity environment in bull sharks, but not in houndsharks, Triakis scyllium

“…Currently, the function of the LDT in SW environment remains to be clarified. In elephant fish and houndsharks, NKCC2 mRNA is expressed in the LDT ( present study and Kakumura et al, 2015), and the LDT is considered to be important for concentrating urea for subsequent urea reabsorption in the CT (Hyodo et al, 2014). However, in the bull shark kidney in a SW environment, neither NKCC2 nor NCC was observed in the LDT (Fig.…”