Sexual Maturation and Changes in Water and Salt Transport Components in the Kidney and Intestine of Three-Spined Stickleback (Gasterosteus Aculeatus L.)

Comp Biochem Physiol A Mol Integr Physiol. 2015 Oct;188:107-19. doi: 10.1016/j.cbpa.2015.06.021. Epub 2015 Jun 29.

Abstract

Mature three-spined stickleback males use spiggin threads secreted from their kidney to glue together nest material. This requires strongly hypertrophied renal proximal tubular cells, which compromises renal osmoregulatory function during the breeding period. Experimental evidence suggests that the intestine takes over hypotonic fluid secretion at that stage but the mechanism is unexplored. To unravel the molecular mechanism we analyzed and compared transcript levels of several membrane proteins involved in water and salt transport in intestinal and renal tissues, in non-mature males (NM), mature males (MM), and mature females (MF). Aquaporin paralogs aqp1a, -3a, -8aa, -8ab, -10a, and -10b, two Na(+),K(+)-ATPase alpha-1 subunit isoforms (nka547, nka976), Na(+),K(+),2Cl(-)-, and Na(+),Cl(-)-cotransporters (nkcc1a, nkcc2, ncc), the cystic fibrosis transmembrane conductance regulator (cftr) and two claudin isoforms (cldn2, cldn15a) were expressed in the intestine and kidney in all groups. There were no differences in aqp and cldn expression between intestines of NM and MM; nkcc2 was lower and nka levels tended to be higher in intestines of MM than in NM. In the kidney, aqp1 and aqp8ab levels were lower in MM than in NM, whereas aqp3a, nkcc1a, cldn15a, and spiggin were markedly elevated. This was accompanied by marked hypertrophy of kidney tubules in MM. The data support an altered kidney function in terms of water handling in mature males, whereas there was no support for modified trans-epithelial water permeability or salt-secretory activity in the intestine of mature males. Salt-absorptive activity in the intestine may, however, be down-regulated during male maturation.

Keywords: Aquaporin; Claudin; Intestine; Ion-transporter; Kidney; Spiggin; Stickleback.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Aquaporins / genetics
  • Biological Transport / genetics
  • Biological Transport / physiology
  • Claudins / genetics
  • Cystic Fibrosis Transmembrane Conductance Regulator / genetics
  • Female
  • Fish Proteins / genetics
  • Gene Expression
  • Intestinal Mucosa / metabolism*
  • Kidney / metabolism*
  • Male
  • Models, Genetic
  • Protein Isoforms / genetics
  • Protein Subunits / genetics
  • Reverse Transcriptase Polymerase Chain Reaction
  • Sexual Maturation*
  • Smegmamorpha / genetics*
  • Smegmamorpha / physiology
  • Sodium Chloride / metabolism*
  • Sodium-Potassium-Exchanging ATPase / genetics
  • Water / metabolism*

Substances

  • Aquaporins
  • Claudins
  • Fish Proteins
  • Protein Isoforms
  • Protein Subunits
  • spiggin
  • Water
  • Cystic Fibrosis Transmembrane Conductance Regulator
  • Sodium Chloride
  • Sodium-Potassium-Exchanging ATPase