Embryonic mobilization of calcium in a viviparous reptile: Evidence for a novel pattern of placental calcium secretion

Fregoso, Santiago P.; Stewart, James R.; Ecay, Tom W.

doi:10.1016/j.cbpa.2010.01.014

Cited by 13 publications

(31 citation statements)

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“…Our finding that chorioallantois calbindin‐D 28K expression increases in late development in concert with elevated placental calcium transport is additional evidence that a calbindin‐D 28K ‐dependent mechanism for calcium transport operates in V. striatula chorioallantois. The pattern of calbindin‐D 28K expression in the chorioallantois and yolk splanchnopleure of V. striatula is similar to that described in the oviparous snake P. guttatus (Ecay et al, ) and reflects the underlying calcium transport activity of each tissue (Stewart et al, ; Fregoso et al, ). In both species, yolk splanchnopleure calbindin‐D 28K expression is low prior to significant embryonic growth and calcium accumulation (i.e., prior to stage 35).…”

Section: Discussionsupporting

confidence: 60%

“…However, most viviparous squamates display some level of placental calcium transfer that, at least partially, compensates for the loss of eggshell calcium (Stewart and Ecay, ). Studies of the timing of embryonic calcium accumulation show that oviparous and viviparous embryos acquire calcium with similar kinetics, suggesting that the timing of uterine calcium secretion shifts with reproductive mode from early egg shelling‐associated transport in oviparity to direct transport to late developmental stage embryos in viviparity (Stewart et al, ,; Fregoso et al, ). This change in the timing of uterine calcium secretion ensures that placental calcium transport is matched to embryonic growth demands.…”

mentioning

confidence: 99%

“…Virginia striatula is a viviparous natricid snake with a pattern of embryonic nutrition characterized as predominantly lecithotrophic (Stewart, ). Embryos receive a substantial amount of calcium from placental transport (Stewart, ; Sangha et al, ; Fregoso et al, ). The pattern of growth and calcium accumulation by embryos of V. striatula is comparable to oviparous species of snakes (Packard et al, ; Packard and Packard, ; Stewart et al, ) in that embryos mobilize a considerable quantity of calcium during late stages of development (Fregoso et al, ).…”

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confidence: 99%

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Expression of Calcium Transport Proteins in the Extraembryonic Membranes of a Viviparous Snake, virginia striatula

2012

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Yolk is the primary source of calcium for embryonic growth and development for most squamates, irrespective of mode of parity. The calcified eggshell is a secondary source for embryonic calcium in all oviparous eggs, but this structure is lost in viviparous lineages. Virginia striatula is a viviparous snake in which embryos obtain calcium from both yolk and placental transport of uterine calcium secretions. The developmental pattern of embryonic calcium acquisition in V. striatula is similar to that for oviparous snakes. Calbindin-D(28K) is a marker for epithelial calcium transport activity and plasma membrane Ca(2+)-ATPase (PMCA) provides the energy to catalyze the final step in calcium transport. Expression of calbindin-D(28K) and PMCA was measured by immunoblotting in yolk sac splanchnopleure and chorioallantois of a developmental series of V. striatula to test the hypothesis that these proteins mediate calcium transport to embryos. In addition, we compared the expression of calbindin-D(28K) in extraembryonic membranes of V. striatula throughout development to a previously published expression pattern in an oviparous snake to test the hypothesis that the ontogeny of calcium transport function is independent of reproductive mode. Expression of calbindin-D(28K) increased in yolk sac splanchnopleure and chorioallantois coincident with calcium mobilization from yolk and uterine sources and with embryonic growth. The amount of PMCA in the chorioallantois did not change through development suggesting its expression is not rate limiting for calcium transport. The pattern of expression of calbindin-D(28K) and PMCA confirms our initial hypothesis that these proteins mediate embryonic calcium uptake. In addition, the developmental pattern of calbindin-D(28K) expression in V. striatula is similar to that of an oviparous snake, which suggests that calcium transport mechanisms and their regulation are independent of reproductive mode.

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Section: Discussionsupporting

confidence: 60%

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confidence: 99%

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confidence: 99%

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Expression of Calcium Transport Proteins in the Extraembryonic Membranes of a Viviparous Snake, virginia striatula

2012

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“…The described mechanisms of embryonic uptake of Ca from extraembryonic membranes involve e.g. Ca channels, Ca binding proteins and Ca ATPases (Fregoso et al, 2010(Fregoso et al, , 2012Gabrielli and Accili, 2010;Stewart et al, 2011). It is shown that the uptake of Ca is low in early development, reaching the maximum absorption point during mid-development followed by a decrease at the end of development, for which the pattern of expression of these proteins follows the Ca uptake.…”

Section: Discussionmentioning

confidence: 96%

Development of an embryotoxicity test for Enchytraeus crypticus – The effect of Cd

Gonçalves¹,

Bicho²,

Rêma

et al. 2015

Chemosphere

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“…However, under conditions of viviparity, loss of the eggshell requires that calcium be replaced by the pregnant uterus and be taken up by these same fetal membranes, i.e., by placental means (Stewart et al, 2009a, b;Linville et al, 2010;Fregoso et al, 2012;Stewart and Ecay, 2010;Stinnett et al, 2012;Stewart, 2013). As is the case with oxygen, embryonic needs for calcium are accentuated late in development when the skeleton becomes ossified (Fregoso et al, 2010;Stewart, 2013).…”

Section: Evidence From Extant Reptilesmentioning

confidence: 99%

Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles

Blackburn

Sidor²

2014

Int. J. Dev. Biol.

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Although viviparity (live-bearing reproduction) is widely distributed among lizards and snakes, it is entirely absent from other extant Reptilia and many extinct forms. However, paleontological evidence reveals that viviparity was present in at least nine nominal groups of pre-Cenozoic reptiles, representing a minimum of six separate evolutionary origins of this reproductive mode. Two viviparous clades (sauropterygians and ichthyopterygians) lasted more than 155 million years, a figure that rivals the duration of mammalian viviparity. Circumstantial evidence indicates that extinct viviparous reptiles had internal fertilization, amniotic fetal membranes, and placentas that sustained developing embryos via provision of respiratory gases, water, calcium, and possibly organic nutrients. Production of offspring via viviparity facilitated the invasion of marine habitats in at least five reptilian lineages. Thus, this pattern of embryonic development and reproduction was central to the ecology and evolution of these ancient animals, much as it is to numerous extant species of vertebrates.

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Embryonic mobilization of calcium in a viviparous reptile: Evidence for a novel pattern of placental calcium secretion

Cited by 13 publications

References 16 publications

Expression of Calcium Transport Proteins in the Extraembryonic Membranes of a Viviparous Snake, virginia striatula

Expression of Calcium Transport Proteins in the Extraembryonic Membranes of a Viviparous Snake, virginia striatula

Development of an embryotoxicity test for Enchytraeus crypticus – The effect of Cd

Evolution of viviparous reproduction in Paleozoic and Mesozoic reptiles

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