Carbonic anhydrase II is found in the placenta of a viviparous, matrotrophic lizard and likely facilitates embryo-maternal CO2 transport

Journal of Experimental Zoology Part B: Molecular and Developmental Evolution

Volumn 324, Issue 7, 2015, Pages 636-646

  Van Dyke, James U ^a   Lindsay, Laura A ^a   Murphy, Christopher R ^a   Thompson, Michael B ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CARBONATE DEHYDRATASE II;

ANIMAL; EMBRYOLOGY; FEMALE; LIZARD; METABOLISM; NONMAMMALIAN EMBRYO; VIVIPARITY;

ANIMALS; CARBON DIOXIDE; CARBONIC ANHYDRASE II; EMBRYO, NONMAMMALIAN; FEMALE; LIZARDS; VIVIPARITY, NONMAMMALIAN;

EID: 84944463107     PISSN: 15525007     EISSN: 15525015     Source Type: Journal    
DOI: 10.1002/jez.b.22621     Document Type: Article

References (42)

1. Adams SM, Biazik JM, Thompson MB, Murphy CR. 2005. Cyto-epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: a new placental morphotype. J Morphol 264:264-276.
2. Biazik JM, Thompson MB, Murphy CR. 2009. Lysosomal and alkaline phosphatase activity indicate macromolecule transport across the uterine epithelium in two viviparous skinks with complex placenta. J Exp Zool B 312:817-826.
3. Biazik JM, Thompson MB, Murphy CR. 2010. Paracellular and transcellular transport across the squamate uterine epithelium. Herpetol Conserv Biol 5:257-262.
4. Birchard GF, Black CP, Schuett G, Black V. 1984. Influence of pregnancy on oxygen consumption, heart rate, and hematology in the garter snake: implications for the "cost of reproduction" in live bearing reptiles. Comp Biochem Physiol 77A:519-523.
5. Blackburn DG. in press. Evolution of vertebrate viviparity and specializations for fetal nutrition: a quantitative and qualitative analysis. J Morphol. DOI: 10.1002/jmor.20272
6. Chegwidden WR, Carter ND. 2000. Introduction to the carbonic anhydrases. In: Chegwidden WR, Carter ND, Edwards YH, editors. The carbonic anhydrases: new horizons. Verlag Basel/Switzerland: Birkhäuser. p 13-28.
7. Clark H, Sisken BF. 1956. Nitrogenous excretion by embryos of the viviparous snake Thamnophis s. sirtalis. J Exp Biol 33:384-393.
8. Dufaure JP, Hubert J. 1961. Table de developpement du lezard vivipare: Lacerta (Zootica) vivipara Jacquin. Arch Anat Microsc Morphol Exp 50:309-328.
9. Ecay TW, Fregoso SP, Khambaty M, Stewart JR. 2010. Developmental expression of carbonic anhydrase II in the extraembryonic membranes of oviparous and viviparous snakes. FASEB J 24:813-814.
10. Forster RE, Dodgson SJ. 2000. Membrane transport and provision of substrates for carbonic anhydrase: in vertebrates. In: Chegwidden WR, Carter ND, Edwards YH, editors. The carbonic anhydrases: new horizons. Verlag Basel/Switzerland: Birkhäuser. p 263-280.
11. Gilmour KM, Perry SF. 2009. Carbonic anhydrase and acid-base regulation in fish. J Exp Biol 212:1647-1661.
12. Gresham EL, James EJ, Raye JR, et al. 1972. Production and excretion of urea by the fetal lamb. Pediatrics 50:372-379.
13. Griffith OW, Ujvari B, Belov K, Thompson MB. 2013a. Placental lipoprotein lipase (LPL) gene expression in a placentotrophic lizard, Pseudemoia entrecasteauxii. J Exp Zool B 320:465-470.
14. Griffith OW, Van Dyke JU, Thompson MB. 2013b. No implantation in an extrauterine pregnancy of a placentotrophic reptile. Placenta 34:510-511.
15. Griffith OW, Blackburn DG, Brandley MC, et al. in press. Ancestral state reconstructions require biological evidence to test evolutionary hypotheses: A case study examining the evolution of reproductive mode in squamate reptiles. J Exp Zool B. DOI: 10.1002/jez.b.22614
16. 2 in the isolated guinea pig placenta. Placenta 10:213-221.
17. Lindskog S, Silverman DN. 2000. The catalytic mechanism of mammalian carbonic anhydrases. In: Chegwidden WR, Carter ND, Edwards YH, editors. The carbonic anhydrases: new horizons. Verlag Basel/Switzerland: Birkhäuser. p 175-195.
18. Mühlhauser J, Crescimanno C, Rajaniemi H, et al. 1994. Immunohistochemistry of carbonic anhydrase in human placenta and fetal membranes. Histochemistry 101:91-98.
19. McEvoy TG, Robinson JJ, Aitken RP, Findlay PA, Robertson IS. 1997. Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Anim Reprod Sci 47:71-90.
20. Nicolaides KH, Economides DL, Soothill PW. 1989. Blood gases, pH, and lactate in appropriate- and small-for-gestational-age fetuses. Am J Obstet Gynecol 161:996-1001.
21. Parker SL, Murphy CR, Thompson MB. 2010. Uterine angiogenesis in squamate reptiles: implications for the evolution of viviparity. Herpetol Conserv Biol 5:330-334.
22. Renfree MB. 2010. Review: marsupials: placental mammals with a difference. Placenta 32:S21-S26.
23. Ridderstråle Y, Persson E, Dantzer V, Leiser R. 1997. Carbonic anhydrase activity in different placenta types: a comparative study of pig, horse, cow, mink, rat, and human. Microsc Res Techniq 38:115-124.
24. Robert KA, Thompson MB. 2000. Energy consumption by embryos of a viviparous lizard, Eulamprus tympanum, during development. Comp Biochem Physiol A 127:481-486.
25. Sims EAH, Krantz KE. 1958. Serial studies of renal function during pregnancy and the puerperium in normal women. J Clin Investig 37:1764-1774.
26. Stewart JR, Thompson MB. 1996. Evolution of reptilian placentation: development of extraembryonic membranes of the Australian scincid lizards, Bassiana duperreyi (Oviparous) and Pseudemoia entrecasteauxii (Viviparous). J Morphol 227:349-370.
27. Stewart JR, Thompson MB, Attaway MB, Herbert JF, Murphy CR. 2006. Uptake of Dextran-FITC by epithelial cells of the chorioallantoic placentome and the omphalopleure of the placentotrophic lizard, Pseudemoia entrecasteauxii. J Exp Zool 305A:883-889.
28. Stewart JR. 2013. Fetal nutrition in lecithotrophic squamate reptiles: toward a comprehensive model for evolution of viviparity and placentation. J Morphol 274:824-843.
29. Swenson ER. 2000. Respiratory and renal roles of carbonic anhydrase in gas exchange and acid-base regulation. In: Chegwidden WR, Carter ND, Edwards YH, editors. The carbonic anhydrases: new horizons. Verlag Basel/Switzerland: Birkhäuser. p 281-341.
30. Thompson J. 1977. The transfer of amino acids across the placenta of a viviparous lizard, Sphenomorphus quoyii. Theriogenology 8:158.
31. Thompson MB, Stewart JR, Speake BK. 2000. Comparison of nutrient transport across the placenta of lizards differing in placental complexity. Comp Biochem Physiol A 127:469-479.
32. Thompson MB, Adams SM, Herbert JF, Biazik JM, Murphy CR. 2004. Placental function in lizards. Int Congr Ser 1275:218-225.
33. Van Dyke JU, Beaupre SJ. 2011. Bioenergetic components of reproductive effort in viviparous snakes: costs of vitellogenesis exceed costs of pregnancy. Comp Biochem Physiol A 160:504-515.
34. Van Dyke JU, Beaupre SJ. 2012. Stable isotope tracer reveals that viviparous snakes transport amino acids to offspring during gestation. J Exp Biol 215:760-765.
35. Van Dyke JU, Brandley MC, Thompson MB. 2014a. The evolution of viviparity: molecular and genomic data from squamate reptiles advance understanding of live birth in amniotes. Reproduction (Camb) 147:R15-R26.
36. Van Dyke JU, Griffith OW, Thompson MB. 2014b. High food abundance permits the evolution of placentotrophy: evidence from a placental lizard, Pseudemoia entrecasteauxii. Am Nat 184:198-210.
37. Weekes HC. 1935. A review of placentation among reptiles with particular regard to the function and evolution of the placenta. Proc Zool Soc Lond 2:625-645.
38. Wetzel P, Gros G. 1990. Sarcolemmal carbonic anhydrase in red and white rabbit skeletal muscle. Arch Biochem Biophys 279:345-354.
39. Whittington CM, Grau GE, Murphy CR, Thompson MB. 2015. Unusual angiogenic factor plays a role in lizard pregnancy but is not unique to viviparity. J Exp Zool B 324:152-158.
40. Yue F, Tang X-L, Zhang D-J, et al. 2012. Body temperature and standard metabolic rate of the female viviparous lizard Eremias multiocellata during reproduction. Can J Zool 90:79-84.
41. Zeh JA, Zeh DW. 1996. The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc B 263:1711-1717.
42. Zeh DW, Zeh JA. 2000. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays 22:938-946.