Aquaporins in avian kidneys: function and perspectives

Abstract

For terrestrial vertebrates, water economy is a prerequisite for survival, and the kidney is their major osmoregulatory organ. Birds are the only vertebrates other than mammals that can concentrate urine in adaptation to terrestrial environments. Aquaporin (AQP) and glyceroporin (GLP) are phylogenetically old molecules and have been found in plants, microbial organisms, invertebrates, and vertebrates. Currently, 13 AQPs/aquaGLPs and isoforms are known to be present in mammals. AQPs 1, 2, 3, 4, 6, 7, 8, and 11 are expressed in the kidney; of these, AQPs 1, 2, 3, 4, and 7 are shown to be involved in fluid homeostasis. In avian kidneys, AQPs 1, 2, 3, and 4 have been identified and characterized. Also, gene and/or amino acid sequences of AQP5, AQP7, AQP8, AQP9, AQP11, and AQP12 have been reported in birds. AQPs 2 and 3 are expressed along cortical and medullary collecting ducts (CDs) and are responsible, respectively, for the water inflow and outflow of CD epithelial cells. While AQP4 plays an important role in water exit in the CD of mammalian kidneys, it is unlikely to participate in water outflow in avian CDs. This review summarizes current knowledge on structure and function of avian AQPs and compares them to those in mammalian and nonmammalian vertebrates. Also, we aim to provide input into, and perspectives on, the role of renal AQPs in body water homeostasis during ontogenic and phylogenetic advancement.

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

“…Water reabsorption is one of the most important functions in tetrapod kidneys. This is particularly true in birds and mammals, and their kidneys have developed the urine concentrating mechanism consisting of a juxtamedullary nephron and countercurrent multiplier and exchange systems (87,91). As already described in the previous sections, marine cartilaginous fishes maintain their body fluid slightly hyperosmotic to the surrounding SW.…”

“…The kidney is one of the most important organs for urea retention in cartilaginous fishes, where urea, as well as water and other small molecules, are freely filtered by the glomerulus. As mentioned in other review articles (87,91), mammals and birds have developed elaborate mechanisms for renal water reabsorption. Their kidneys contain juxtamedullary nephrons that are characterized by a countercurrent multiplier system.…”

“…As reviewed by Nishimura and Yang (87), aquaporins (AQPs) are a family of small, hydrophobic proteins. AQPs are phylogenetically old molecules and have been found in most organisms including plants, microbial organisms, invertebrates, and vertebrates.…”

Age-related changes in renal AQP3 and AQP4 expression in Sprague Dawley rats

“…AVP regulates AQP2 via short-term and long-term regulatory mechanisms, which are fundamentally different (Nielsen and Agre, 1995;Poulsen et al, 2013) AQP2 null mice fail to thrive and die postnatally as a result of excessive extracellular fluid loss, indicating that the concentration of urine is dependent on the presence of AQP2 (Tamma et al, 2012;Xing et al, 2014). AQP3 and AQP4 are localized to the basolateral plasma membranes of principal cells in the connecting tubule and collecting duct (Murillo-Carretero et al, 1999;Nielsen et al, 1999;Tamma et al, 2012;Kortenoeven and Fenton, 2014) and provide potential pathways of water reabsorption via AQP2 (Wang et al, 2002;Nishimura and Yang, 2013;Koetenoeven and Fenton, 2014;Marlar et al, 2014). AQP3 is located in the cortical and outer medullary collecting ducts and AQP4 is located in the inner medullary collecting duct membrane (Terris et al, 1995;Verkman, 1998;Nielsen et al, 2002;Kim et al, 2005;Verkman, 2006;Nishimura and Yang, 2013) AQP3 is regulated by long-term AVP stimulation (Terris et al, 1995;Yang et al, 2013;Xing et al, 2014) and extracellular pH (Zelenina et al, 2003;Castle, 2005).…”

“…AQP3 and AQP4 are localized to the basolateral plasma membranes of principal cells in the connecting tubule and collecting duct (Murillo-Carretero et al, 1999;Nielsen et al, 1999;Tamma et al, 2012;Kortenoeven and Fenton, 2014) and provide potential pathways of water reabsorption via AQP2 (Wang et al, 2002;Nishimura and Yang, 2013;Koetenoeven and Fenton, 2014;Marlar et al, 2014). AQP3 is located in the cortical and outer medullary collecting ducts and AQP4 is located in the inner medullary collecting duct membrane (Terris et al, 1995;Verkman, 1998;Nielsen et al, 2002;Kim et al, 2005;Verkman, 2006;Nishimura and Yang, 2013) AQP3 is regulated by long-term AVP stimulation (Terris et al, 1995;Yang et al, 2013;Xing et al, 2014) and extracellular pH (Zelenina et al, 2003;Castle, 2005). In addition to water, AQP3 also transports glycerol and urea (King and Agre, 1996;Lee et al, 1997;Kuwahara et al, 1997) AQP4 enables water permeation in the basolateral plasma membrane of the rat inner medullary collecting duct (Ma et al, 2000).…”