Morphological and biochemical evidence for the evolution of salt glands in snakes

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 160, Issue 3, 2011, Pages 400-411

  Babonis, Leslie S ^a,b   Evans, David H ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

Aquaporin 3; Cystic fibrosis transmembrane conductance regulator (CFTR); Mucin

Indexed keywords

AQUAPORIN 3; FRESH WATER; MUCIN; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASOLATERAL MEMBRANE; BIOCHEMISTRY; CONTROLLED STUDY; EPITHELIUM; MOLECULAR BIOLOGY; MORPHOLOGY; MUCUS SECRETION; NONHUMAN; SALT GLAND; SNAKE; SUBLINGUAL GLAND;

LATICAUDA SEMIFASCIATA; NERODIA; NERODIA CLARKII CLARKII; NERODIA FASCIATA; SERPENTES; VERTEBRATA;

EID: 80052100260     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2011.07.008     Document Type: Article

References (52)

1. Akabane G., Ogushi Y., Hasegawa T., Suzuki M., Tanaka S. Gene cloning and expression of an aquaporin (AQP-h3BL) in the basolateral membrane of water-permeable epithelial cells in osmoregulatory organs of the tree frog. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R2340-R2351.
2. Akamatsu T., Parvin M.N., Murdiastuti K., Kosugi-Tanaka C., Yao C.J., Miki O., Kanamori N., Hosoi K. Expression and localization of aquaporins, members of the water channel family, during development of the rat submandibular gland. Pflugers Arc.-Eur. J. Physiol. 2003, 446:641-651.
3. Babonis L.S., Hyndman K.A., Lillywhite H.B., Evans D.H. Immunolocalization of Na+/K+-ATPase and Na+/K+/2Cl- cotransporter in the tubular epithelia of sea snake salt glands. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2009, 154:535-540.
4. Babonis L.S., Miller S.N., Evans D.H. Renal responses to salinity change in snakes with and without salt glands. J. Exp. Biol. 2011, 214:2140-2156.
5. Barnitt A.E., Goertemiller C.C. Nasal salt-secreting glands of normal and hyperkalemically stressed Sauromalus obesus - histology and cytology. Copeia 1985, 403-409.
6. Bennett D.C., Hughes M.R. Comparison of renal and salt gland function in three species of wild ducks. J. Exp. Biol. 2003, 206:3273-3284.
7. Bilan F., Thoreau V., Nacfer M., Derand R., Norez C., Cantereau A., Garcia M., Becq F., Kitzis A. Syntaxin 8 impairs trafficking of cystic fibrosis transmembrane conductance regulator (CFTR) and inhibits its channel activity. J. Cell Sci. 2004, 117:1923-1935.
8. Burns B., Pickwell G.V. Cephalic glands in sea snakes (Pelamis, Hydrophis and Laticauda). Copeia 1972, 547-559.
9. Choe K.P., Kato A., Hirose S., Plata C., Sindic A., Romero M.F., Claiborne J.B., Evans D.H. NHE3 in an ancestral vertebrate: primary sequence, distribution, localization, and function in gills. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2005, 289:R1520-R1534.
10. Conant R., Lazell J.D. The Carolina salt marsh snake: a distinct form of Natrix sipedon 1973, 1-11. Brevoria, Museum of Comparative Zoology.
11. Contrera M.G.D., Lopes R.A., Costa J.R.V., Petenusci S.O., Limaverde J.S. The histology of salivary glands in the colubrid snake Sibynomorphus mikanii (Schlegel, 1837). Can. J. Zool. 1983, 61:936-941.
12. Cowan F.B.M. Gross and microscopic anatomy of orbital glands of Malaclemys and other emydine turtles. Can. J. Zool. 1969, 47:723-729.
13. Cowan F.B. The ultrastructure of the lachrymal 'salt' gland and the Harderian gland in the euryhaline Malaclemys and some closely related stenohaline emydines. Can. J. Zool. 1971, 49:691-697.
14. Cramp R.L., Hudson N.J., Holmberg A., Holmgren S., Franklin C.E. The effects of saltwater acclimation on neurotransmitters in the lingual salt glands of the estuarine crocodile, Crocodylus porosus. Regul. Pept. 2007, 140:55-64.
15. Cramp R.L., Hudson N.J., Franklin C.E. Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands of Crocodylus porosus following chronic saltwater acclimation. J. Exp. Biol. 2010, 213:1301-1308.
16. Dantzler W.H., Bradshaw S.D. Osmotic and ionic regulation in reptiles. Osmotic and Ionic Regulation: Cells and Animals 2009, 443-503. CRC Press, Boca Raton, FL. D.H. Evans (Ed.).
17. Dunson W.A. The relation of sodium and water balance to survival in sea water of estuarine and freshwater races of the snakes Nerodia fasciata, Nerodia sipedon and Nerodia valida. Copeia 1980, 268-280.
18. Dunson W.A., Dunson M.K. Convergent evolution of sublingual salt glands in the marine file snake and true sea snakes. J. Comp. Physiol. 1973, 86:193-208.
19. Dunson W.A., Dunson M.K. Interspecific differences in fluid concentration and secretion rate of sea snake salt glands. Am. J. Physiol. 1974, 227:430-438.
20. Dunson W.A., Dunson M.K. Possible new salt gland in a marine Homalopsid snake (Cerberus rhynchops). Copeia 1979, 661-673.
21. Dunson W.A., Packer R.K., Dunson M.K. Sea snakes: an unusual salt gland under the tongue. Science 1971, 173:437-441.
22. Ellis R.A., Goertemiller C.C. Cytological effects of salt-stress and localization of transport adenosine triphosphatase in the lateral nasal glands of the desert iguana, Dipsosaurus dorsalis. Anat. Rec. 1974, 180:285-297.
23. Evans D.H., Claiborne J.B. Osmotic and ionic regulation in fishes. Osmotic and Ionic Regulation: Cells and Animals 2009, 295-366. CRC Press, Boca Raton, FL. D.H. Evans (Ed.).
24. Gresz V., Kwon T.H., Hurley P.T., Varga G., Zelles T., Nielsen S., Case R.M., Steward M.C. Identification and localization of aquaporin water channels in human salivary glands. Am. J. Physiol. Gastrointest. Liver Physiol. 2001, 281:G247-G254.
25. Hazard L.C. Ion secretion by the nasal salt gland of an herbivorous desert lizard, Dipsosaurus dorsalis. Ph.D. Dissertation 1999, University of California, Riverside, CA, pp. 148.
26. Hildebrandt J.P. Coping with excess salt: adaptive functions of extrarenal osmoregulatory organs in vertebrates. Zoology 2001, 104:209-220.
27. Humason G.L. Animal Tissue Techniques 1972, W.H. Freeman and Company, San Francisco. Third ed.
28. Knight C.H., Peaker M. Adaptive hyperplasia and compensatory growth in the salt glands of ducks and geese. J. Physiol. 1979, 294:145-151.
29. Kochva E. Oral Glands of the Reptilia. Biol. Reptil. 1978, 43-161. Academic Press, New York and London. C. Gans, K.A. Gans (Eds.).
30. Lignot J.H., Cutler C.P., Hazon N., Cramb G. Immunolocalisation of aquaporin 3 in the gill and the gastrointestinal tract of the European eel Anguilla anguilla (L.). J. Exp. Biol. 2002, 205:2653-2663.
31. Lillie R.D. Further experiments with the Masson trichrome modification of the Mallory connective tissue stain. Stain. Technol. 1940, 15:17-22.
32. Lowy R.J., Dawson D.C., Ernst S.A. Mechanism of ion transport by avian salt gland primary cell cultures. Am. J. Physiol. 1989, 256:R1184-R1191.
33. Lytle C., Xu J.C., Biemesderfer D., Forbush B. Distribution and diversity of Na+/K+/Cl- cotransport proteins: a study with monoclonal antibodies. Am. J. Physiol. 1995, 269:C1496-C1505.
34. Martin B.J., Philpott C.W. The adaptive response of the salt glands of adult mallard ducks to a salt water regime: an ultrastructural and tracer study. J. Exp. Zool. 1973, 186:111-122.
35. Mobasheri A., Wray S., Marples D. Distribution of AQP2 and AQP3 water channels in human tissue microarrays. J. Mol. Hist. 2005, 36:1-14.
36. Muller C., Sendler M., Hildebrandt J.P. Downregulation of aquaporins 1 and 5 in nasal gland by osmotic stress in ducklings, Anas platyrhynchos: implications for the production of hypertonic fluid. J. Exp. Biol. 2006, 209:4067-4076.
37. Peaker M., Linzell J.L. Salt Glands in Birds and Reptiles 1975, 307. Cambridge University Press, London, New York.
38. Pettus D. Salinity and subspeciation in Natrix sipedon. Copeia 1963, 499-504.
39. Pyron R.A., Burbrink F.T., Colli G.R., de Oca A.N.M., Vitt L.J., Kuczynski C.A., Wiens J.J. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Mol. Phylogenet. Evol. 2011, 58:329-342.
40. R Development Core Team R: A Language and Environment for Statistical Computing 2008, R Foundation for Statistical Computing, Vienna, Austria.
41. Riordan J.R., Forbush B., Hanrahan J.W. The molecular basis of chloride transport in shark rectal gland. J. Exp. Biol. 1994, 196:405-418.
42. Rose T.M., Henikoff J.G., Henikoff S. CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucleic Acids Res. 2003, 31:3763-3766.
43. Saint-Girons H. The cephalic exocrine glands of reptiles. 1. Anatomical and histological data. Ann. Sci. Nat.-Zool. Biol. Anim. 1988, 9:221-255.
44. Schmidt-Nielsen K., Fange R. Salt glands in marine reptiles. Nature 1958, 182:783-785.
45. Shuttleworth T.J., Hildebrandt J.P. Vertebrate salt glands: short- and long-term regulation of function. J. Exp. Zool. 1999, 283:689-701.
46. Staaland H. Anatomical and physiological adaptations of the nasal glands in Charadriiformes birds. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 1967, 23:933-944.
47. Takeyasu K., Tamkun M.M., Renaud K.J., Fambrough D.M. Ouabain-sensitive Na+/K+-ATPase activity expressed in mouse L cells by transfection with DNA encoding the alpha-subunit of an avian sodium pump. J. Biol. Chem. 1988, 263:4347-4354.
48. Taplin L.E., Grigg G.C. Salt glands in the tongue of the estuarine crocodile Crocodylus porosus. Science 1981, 212:1045-1047.
49. Taplin L.E., Grigg G.C., Harlow P., Ellis T.M., Dunson W.A. Lingual salt glands in Crocodylus acutus and Crocodylus johnstoni and their absence from Alligator mississipiensis and Caiman crocodilus. J. Comp. Physiol. 1982, 149:43-47.
50. Taub A.M. Ophidian cephalic glands. J. Morphol. 1966, 118:529-542.
51. Untergasser A., Nijveen H., Rao X., Bisseling T., Geurts R., Leunissen J.A. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007, 35:W71-W74.
52. VanLennep E.W., Komnick H. Fine structure of the nasal salt gland in the desert lizard Uromastyx acanthinurus. Cytobiologie 1970, 2:47-67.