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First published online March 27, 2009
Journal of Experimental Biology 212, 1202-1211 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025239
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Increased gene expression of a facilitated diffusion urea transporter in the skin of the African lungfish (Protopterus annectens) during massively elevated post-terrestrialization urea excretion

Carrie Y. C. Hung1, Fernando Galvez2, Yuen K. Ip3 and Chris M. Wood1,*

1 Department of Biology, McMaster University, Hamilton, ON, Canada, L8S 4K1
2 Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA
3 Department of Biological Sciences, National University of Singapore, 10 Kent Ridge Road, Singapore 117543, Republic of Singapore


Figure 1
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  		Fig. 1. Nucleotide sequence and translated amino acid sequence of the putative Protopterus annectens urea transporter (lfUT). The nucleotide sequence includes both 5'- and 3'-untranslated regions. The stop codon is indicated by an asterisk. A potential N-glycosylation site is underlined. Potential serine (S), threonine (T) and tyrosine (Y) phosphorylation sites are circled. The putative polyadenylation signal sequence (AATAAA) is boxed.

 

Figure 2
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  		Fig. 2. Amino acid sequence alignment of the putative P. annectens urea transporter (lfUT) with several known urea transporters from other species. Urea transporter sequences are highly conserved across species from different taxa. Identical amino acids are highlighted in black and similar amino acids are shaded. Nine transmembrane (TM) regions were predicted for P. annectens and are underlined. Accession numbers: P. annectens (lungfish, EU716115); Opsanus beta (gulf toadfish, AAD53268); Squalus acanthias (spiny dogfish, AAF66072); Bufo marinus (giant toad, BAE16706); Rana esculenta (edible frog, CAA73322); Homo sapiens (human, CAA65657).

 

Figure 3
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  		Fig. 3. Phylogenetic tree of urea transporters across taxa. The protein sequences were aligned using ClustalW software, followed by neighbour-joining (NJ) matrix for tree reconstruction and evaluated by means of a bootstrap of 1000 replicates at http://power.nhri.org.tw.

 

Figure 4
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  		Fig. 4. Expression of the putative lungfish urea transporter gene (lfUT) in various tissues of aquatic control (C) and post-terrestrialization (T) P. annectens. Consistent expression of the urea transporter was detected in gill, kidney, liver, muscle, and dorsal and ventral skin, but it was only weakly expressed or absent in heart and lung of both control and post-terrestrialization P. annectens.

 

Figure 5
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  		Fig. 5. Rates of urea-N excretion in P. annectens during re-immersion following 33 days of terrestrialization and in control (aquatic) lungfish following 33 days of fasting. Means and 1 s.e.m. (N=6) are shown for the control series and for the data of Series 1; asterisk indicates that the urea-N excretion rate in these post-terrestrialization animals was significantly different from the urea-N excretion rate in control (aquatic) animals at the respective time point (P<0.05). Means only (N=5) are shown for the data of Series 2, s.e.m. values have been omitted for clarity. Arrows indicate the times of biopsies in Series 2. Within treatment groups, multiple comparison testing revealed that in the control group only the 2 and 70 h points were significantly different (P<0.05). Within the post-terrestrialization group of Series 1, urea-N excretion was significantly higher at 14 h than at 2–8 h, and the rates remained significantly elevated up to 56 h. The peak excretion rate occurred at 20 h and was significantly higher than the 2–18, 22, 26 and 30 h through to 72 h post-terrestrialization measurements. Within the post-terrestrialization group of Series 2, urea-N excretion rates at 14–50 h post-terrestrialization were significantly higher than means at 6–10, 54 and 60 h (P<0.05).

 

Figure 6
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  		Fig. 6. Relative expression levels of the urea transporter gene (lfUT; relative to actin), in ventral skin of aquatic, fed control P. annectens and during re-immersion following 33 days of aestivation. Relative expression of lfUT/actin at 14 h following re-immersion was significantly higher than in aquatic fed control animals and in terrestrialized animals 0 h after re-immersion (P<0.05). At 48 h, expression was not significantly different from any other conditions. Values are means and s.e.m. (N=5).

 

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© The Company of Biologists Ltd 2009