Uterine focal adhesion dynamics during pregnancy in a marsupial (Sminthopsis crassicaudata; Dasyuridae)

Anatomical Record

Volumn 300, Issue 6, 2017, Pages 1150-1159

  Laird, Melanie K ^a   Turancova, Michaela ^a   McAllan, Bronwyn M ^a   Murphy, Christopher R ^a   Thompson, Michael B ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

implantation; paxillin; plasma membrane transformation; talin

Indexed keywords

PAXILLIN; TALIN;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; FEMALE; FOCAL ADHESION; IMMUNOFLUORESCENCE MICROSCOPY; MARSUPIAL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; SMINTHOPSIS CRASSICAUDATA; UTERUS; WESTERN BLOTTING; ANIMAL; BREEDING; CYTOLOGY; METABOLISM; NIDATION; PHYSIOLOGY;

ANIMALS; BLOTTING, WESTERN; EMBRYO IMPLANTATION; FEMALE; FOCAL ADHESIONS; MARSUPIALIA; PAXILLIN; PREGNANCY; PREGNANCY, ANIMAL; TALIN; UTERUS;

EID: 85012065298     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.23535     Document Type: Article

References (47)

1. Adams SM, Lui S, Jones SM, Thompson MB, Murphy CR. 2007. Uterine epithelial changes during placentation in the viviparous skink Eulamprus tympanum. J Morphol 268:385–400.
2. Bennett JH, Breed WG, Hayman DL, Hope RM. 1990. Reproductive and genetic studies with a laboratory colony of the dasyurid marsupial Sminthopsis crassicaudata. Aust J Zool 37:207–222.
3. Biazik JM, Thompson MB, Murphy CR. 2007. The tight junctional protein occludin is found in the uterine epithelium of squamate reptiles. J Comp Physiol B 177:935–943.
4. 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 312:817–826.
5. Biazik JM, Thompson MB, Murphy CR. 2010. Desmosomes in the uterine epithelium of noninvasive skink placentae. Anat Rec 293:502–512.
6. Blackburn DG. 1992. Convergent evolution of viviparity, matrotrophy, and specializations for fetal nutrition in reptiles and other vertebrates. Amer Zool 32:313–321.
7. Blackburn DG. 2015. Evolution of vertebrate viviparity and specializations for fetal nutrition: A quantitative and qualitative analysis. J Morphol 276:961–990.
8. Blankenship TN, Given RL, Parkening TA. 1990. Blastocyst implantation in the Chinese hamster (Cricetulus griseus). Am J Anat 187:137–157.
9. Brandley MC, Young RL, Warren DL, Thompson MB, Wagner GP. 2012. Uterine gene expression in thelive-bearing lizard, Chalcides ocellatus, reveals convergence of squamate and mammalian pregnancy mechanisms. Genome Biol Evol 4:394–411.
10. Breed WG, Leigh CM, Bennett JM. 1989. Spermatozoa morphology and storage in the female reproductive tract of the fat-tailed dunnart, Sminthopsis crassicaudata (Marsupialia: Dasyuridae). Gamete Res 23:61–75.
11. Carter AM, Mess A. 2007. Evolution of the placenta in eutherian mammals. Placenta 28:259–262.
12. Crespi B, Semeniuk C. 2004. Parent-offspring conflict in the evolution of the vertebrate reproductive mode. Am Nat 163:635–653.
13. Czarny NA, Garnham JI, Harris MS, Rodger JC. 2009. Comparison of the production, quality, and in vitro maturation capacity of oocytes from untreated cycling and intermediate phase equine serum gonadotropin treated fat-tailed dunnarts (Sminthopsis crassicaudata). Reproduction 138:23–31.
14. Dudley JS, Murphy CR, Thompson MB, McAllan BM. 2015. Desmoglein-2 during pregnancy and its role in the evolution of viviparity in a marsupial (Sminthopsis crassicaudata; Dasyuridae). J Morphol 276:261–272.
15. Elliot MG, Crespi BJ. 2009. Phylogenetic evidence for early hemochorial placentation in eutheria. Placenta 30:949–967.
16. Enders AC, Schlafke S. 1967. A morphological analysis of the early implantation stages in the rat. Am J Anat 120:185–226.
17. Ferner K, Mess A. 2011. Evolution and development of fetal membranes and placentation in amniote vertebrates. Respir Physiol Neurobiol 178:39–50.
18. Kaneko Y, Lindsay LA, Murphy CR. 2008. Focal adhesions disassemble during early pregnancy in rat uterine epithelial cells. Reprod Fertil Dev 20:892–899.
19. Kaneko Y, Lecce L, Murphy CR. 2009. Ovarian hormones regulate expression of the focal adhesion proteins, talin and paxillin, in rat uterine luminal but not glandular epithelial cells. Histochem Cell Bio 132:613–622.
20. 3 is later localised to the apical plasma membrane of rat uterine luminal epithelial cells at the time of implantation. Reprod Fertil Devel 23:481–495.
21. Kaneko Y, Lecce L, Day ML, Murphy CR, 2012. Focal adhesion kinase localizes to sites of cell-to-cell contact in vivo and increases apically in rat uterine luminal epithelium and the blastocyst at the time of implantation. J Morphol 273:639–650.
22. Laird MK, Thompson MB, Murphy CR, McAllan BM, 2014. Uterine epithelial cell changes during pregnancy in a marsupial (Sminthopsis crassicaudata; Dasyuridae). J Morphol 275:1081–1092.
23. McAllan BM. 2003. Timing of reproduction in carnivorous marsupials. In: Jones M, Dickman C, Archer M, editors. Predators with pouches: The biology of carnivorous marsupials. Victoria, Australia: CSIRO Publishers. p 147–164.
24. McAllan BM, Feay N, Bradley AJ, Geiser F. 2012. The influence of reproductive hormones on the torpor patterns of the marsupial Sminthopsis macroura: Bet-hedging in an unpredictable environment. Gen Comp Endocrinol 179:265–276.
25. Mess A. 2014. Placental evolution within the supraordinal clades of Eutheria with the perspective of alternative animal models for human placentation. Adv Biol 2014:1–21.
26. Murphy CR. 2004. Uterine receptivity and the plasma membrane transformation. Cell Res 14:259–267.
27. Murphy CR, Hosie MJ, Thompson MB. 2000. The plasma membrane transformation facilitates pregnancy in both reptiles and mammals. Comp Biochem Physiol A 127:433–439.
28. Nayal A, Webb DJ, Horitz AF, 2004. Talin: An emerging focal point of adhesion dynamics. Curr Opin Cell Biol 16:94–98.
29. Orchard M, Murphy CR. 2002. Alterations in tight junction molecules of uterine epithelial cells during early pregnancy in the rat. Acta Histochem 104:149–155.
30. Pollock K, Booth R, Wilson R, Keeley T, Grogan K, Kennerley P, Johnston SD. 2010. Oestrus in the Julia Creek dunnart (Sminthopsis douglasi) is associated with wheel running behaviour but not necessarily changes in body weight, food consumption or pouch morphology. Anim Reprod Sci 117:135–146.
31. Ramirez-Pinilla MP, Parker SL, Murphy CR, Thompson MB. 2012. Uterine and chorioallantoic angiogenesis and changes in the uterine epithelium during gestation in the viviparous lizard, Niveoscincus conventryi (Squamata: Scincidae). J Morphol 273:8–23.
32. Roberts CT, Breed WG. 1994a. Placentation in the dasyurid marsupial, Sminthopsis crassicaudata, the fat tailed dunnart, and notes on placentation of the didelphid, Monodelphis domestica. J Reprod Fertil 100:105–113.
33. Roberts CT, Breed WG. 1994b. Embryonic-maternal cell interactions at implantation in the fat-tailed dunnart, a dasyurid marsupial. Anat Rec 240:59–76.
34. Roberts CT, Breed WG. 1996. Changes in structure of the trophectoderm of a marsupial in mid-pregnancy up to the time of implantation. Reprod Fertil Dev 8:797–802.
35. Schlafke S, Enders AC. 1975. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod 12:41–65.
36. Selwood L, Woolley PA. 1991. A timetable of embryonic development, and ovarian and uterine changes during pregnancy, in the stripe-faced dunnart, Sminthopsis macroura (Marsupialia: Dasyuridae). J Reprod Fertil 91:213–227.
37. Shion YL, Murphy CR. 1995. The basal plasma membrane and lamina densa of uterine epithelial cells are both altered during early pregnancy and by ovarian hormones in the rat. Eur J Morphol 33:257–264.
38. Smith MJ, Bennett JH, Chesson CM. 1978. Photoperiod and some other factors affecting reproduction in female Sminthopsis crassicaudata (Gould) (Marsupialia: Dasyuridae) in captivity. Aust J Zool 26:449–463.
39. Smith MJ, Godfrey GK. 1970. Ovulation induced by gonadotrophins in the marsupial, Sminthopsis crassicaudata (Gould). J Reprod Fertil 22:41–47.
40. Song G, Bailey DW, Dunlap KA, Burghardt RC, Spencer TE, Bazer FW, Johnson GA, 2010. Cathepsin B, cathepsin L, and cystatin C in the porcine uterus and placenta: Potential roles in endometrial placental remodeling and in fluid-phase transport of proteins secreted by uterine epithelia across placental areolae. Biol Repro 82:854–864.
41. Thompson MB, Stewart JR, Speake BK, Hosie MJ, Murphy CR, 2002. Evolution of viviparity: What can Australian lizards tell us?. Comp Biochem Physiol B 131:631–643.
42. Turner CE. 2000. Paxillin and focal adhesion signalling. Nature Cell Biol 2:E231−23E236.
43. Turner CE, Schaller MD, Parsons JT. 1993. Tyrosine phosphorylation of the focal adhesion kinase pp125FAK during development: Relation to paxillin. J Cell Sci 105:637–645.
44. Tyndale-Biscoe H, Renfree MB. 1987. Reproductive physiology of Marsupials. Cambridge: Cambridge University Press.
45. Woolley PA. 1990. Reproduction in Sminthopsis macroura (Marsupialia: Dasyuridae) 1. The female. Aust J Zool 38:187–205.
46. Wu Q, Thompson MB, Murphy CR. 2011. Changing distribution of cadherins during gestation in the uterine epithelium of lizards. J Exp Zool 316:440–450.
47. Zhang S, Kong S, Lu J, Wang Q, Chen Y, Wang W, Wang B, Wang H. 2013. Deciphering the molecular basis of uterine receptivity. Mol Reprod Dev 80:8–21.