Ontogeny of ENaC expression in the gills and the kidneys of the Japanese black salamander (<i>Hynobius nigrescens</i> Stejneger)

Uchiyama, Minoru; Kumano, Tomoko; Konno, Norifumi; Yoshizawa, Hideki; Matsuda, Kouhei

doi:10.1002/jez.b.21384

Cited by 11 publications

(9 citation statements)

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“…In amphibians, ENaC mRNA and protein are expressed in the urinary bladder and ventral skin in addition to the kidney [16,19]. We recently studied the ontogeny of ENaC expression in the external gills and the kidney in a primitive urodele, Hynobius nigrescens [19].…”

Section: Discussionmentioning

confidence: 99%

“…Thus, ENaC is important for the evolution of terrestriality during the evolution of early tetrapods, in addition to the acquisition of aldosterone as the most potent sodium-retaining factor in the kidney and colon [19]. Aldosterone is present in tetrapods and in Neoceratodus [20], whereas it is absent in teleosts, elasmobranchs and agnathans [21].…”

Section: Introductionmentioning

confidence: 99%

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The epithelial sodium channel in the Australian lungfish, Neoceratodus forsteri (Osteichthyes: Dipnoi)

et al. 2012

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Epithelial sodium channel (ENaC) is a Na þ -selective, aldosterone-stimulated ion channel involved in sodium transport homeostasis. ENaC is rate-limiting for Na þ absorption in the epithelia of osmoregulatory organs of tetrapods. Although the ENaC/degenerin gene family is proposed to be present in metazoans, no orthologues or paralogues for ENaC have been found in the genome databases of teleosts. We studied full-length cDNA cloning and tissue distributions of ENaCa, b and g subunits in the Australian lungfish, Neoceratodus forsteri, which is the closest living relative of tetrapods. Neoceratodus ENaC (nENaC) comprised three subunits: nENaCa, b and g proteins. The nENaCa, b and g subunits are closely related to amphibian ENaCa, b and g subunits, respectively. Three ENaC subunit mRNAs were highly expressed in the gills, kidney and rectum. Amiloride-sensitive sodium current was recorded from Xenopus oocytes injected with the nENaCabg subunit complementary RNAs under a two-electrode voltage clamp. nENaCa immunoreactivity was observed in the apical cell membrane of the gills, kidney and rectum. Thus, nENaC may play a role in regulating sodium transport of the lungfish, which has a renin -angiotensin-aldosterone system. This is interesting because there may have been an ENaC sodium absorption system controlled by aldosterone before the conquest of land by vertebrates.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The epithelial sodium channel in the Australian lungfish, Neoceratodus forsteri (Osteichthyes: Dipnoi)

et al. 2012

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“…The secondary antibodies used were Alexa Fluor 488‐ and 546‐conjugated goat antirabbit and antiguinea pig Immunoglobulin Gs (IgGs) (Invitrogen). Polyclonal antipeptide antibodies were successfully used as described previously (Uchiyama and Yoshizawa, 2002; Uchiyama et al, 2011).…”

Section: Methodsmentioning

confidence: 99%

“…Using electron microscopy and immunohistochemical techniques, Brunelli and Tripepi (2005) observed that the number of CCs and MRCs in the external gills of larval newts of Triturus italicus increased when these newts were exposed to low pH (pH 4.5) solutions. We also recently reported the cloning and expression of an ENaCα subunit and NHE3 in the Japanese black salamander Hynobius nigrescens (Kumano et al, 2008; Uchiyama et al, 2011). The ENaCα subunit but not NHE3 was observed in the gills and skin of these salamanders.…”

Section: Introductionmentioning

confidence: 98%

“…Thus, the main osmoregulatory organs change from gills and kidney, in the larva to the skin, kidney, and urinary bladder in the postmetamorphic young and adult. In aquatic amphibian larvae, although several channels and cotransporters are expressed in the pronephros and might play an important role in osmoregulation (Kumano et al, 2008; Haugan et al, 2010; Uchiyama et al, 2011), mitochondria‐rich cells (MRCs) and vacuolar‐type H + ‐ATPase (VHA)‐positive cells are not present in amphibian pronephric tubules (Møbjerg et al, 2000; Uchiyama et al, 2011). Thus, acid–base balance regulation of body fluids may depend on other organs such as external gills.…”

Section: Introductionmentioning

confidence: 99%

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Immunohistological classification of ionocytes in the external gills of larval Japanese black salamander, Hynobius nigrescens Stejneger

Uchiyama¹,

Kumano²,

Komiyama³

et al. 2011

Journal of Morphology

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In this cytological and immunohistological study, we clarified the localization of the membrane transporters Na(+) , K(+) -ATPase (NKA), vacuolar-type H(+) -ATPase (VHA), and epithelial sodium channel (ENaC) and distinguished ionocyte subtypes in the gill of the Japanese salamander (Hynobius nigrescens). In larvae (IY stages 43-65), NKA immunoreactivity was observed on the basolateral plasma membrane in more than 60% cells and less than 20% cells in the primary filaments and secondary lamellae of the external gills, respectively. VHA immunoreactivity was observed on the apical membrane of some epithelial cells in the secondary lamellae of the external gills. High ENaCα immunoreactivity was widely observed on the apical cell membrane of a population of squamous cells, presumably pavement cells (PVCs), and mitochondria-rich cells (MRCs), in the primary filaments and secondary lamellae of the external gills. Using double immunofluorescence microscopy, epithelial cell types involved in ionic regulation were characterized and divided into three ionocyte types: NKA-, NKA- and ENaC-, and VHA-positive cells. VHA-immunoreactive cells as well as NKA-positive cells were observed during IY stages 43-65 of the salamander larvae. During late stages of metamorphosis, NKA, VHA, and ENaCα immunoreactivities in the external gills decreased and finally disappeared during the completion of metamorphosis (IY stage 68). PVCs and MRCs in the external gills are probably involved in acid-base balance regulation and osmoregulation in urodele amphibian larvae. The results are discussed in relation to the ionocytes previously reported in fish gills and the frog skin epithelium.

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Osmoregulation and Excretion

Larsen

Deaton

Onken

et al. 2014

Comprehensive Physiology

185

141

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The article discusses advances in osmoregulation and excretion with emphasis on how multicellular animals in different osmotic environments regulate their milieu intérieur. Mechanisms of energy transformations in animal osmoregulation are dealt with in biophysical terms with respect to water and ion exchange across biological membranes and coupling of ion and water fluxes across epithelia. The discussion of functions is based on a comparative approach analyzing mechanisms that have evolved in different taxonomic groups at biochemical, cellular and tissue levels and their integration in maintaining whole body water and ion homeostasis. The focus is on recent studies of adaptations and newly discovered mechanisms of acclimatization during transitions of animals between different osmotic environments. Special attention is paid to hypotheses about the diversity of cellular organization of osmoregulatory and excretory organs such as glomerular kidneys, antennal glands, Malpighian tubules and insect gut, gills, integument and intestine, with accounts on experimental approaches and methods applied in the studies. It is demonstrated how knowledge in these areas of comparative physiology has expanded considerably during the last two decades, bridging seminal classical works with studies based on new approaches at all levels of anatomical and functional organization. A number of as yet partially unanswered questions are emphasized, some of which are about how water and solute exchange mechanisms at lower levels are integrated for regulating whole body extracellular water volume and ion homeostasis of animals in their natural habitats. © 2014 American Physiological Society.

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Ontogeny of ENaC expression in the gills and the kidneys of the Japanese black salamander (Hynobius nigrescens Stejneger)

Cited by 11 publications

References 41 publications

The epithelial sodium channel in the Australian lungfish, Neoceratodus forsteri (Osteichthyes: Dipnoi)

The epithelial sodium channel in the Australian lungfish, Neoceratodus forsteri (Osteichthyes: Dipnoi)

Immunohistological classification of ionocytes in the external gills of larval Japanese black salamander, Hynobius nigrescens Stejneger

Osmoregulation and Excretion

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