Plasma membrane transformation

The plasma membrane transformation is a concept introduced by Christopher R. Murphy of The University of Sydney to encapsulate the idea that a series of changes in the plasma membrane of uterine epithelial cells is essential to the development of the receptivity of the uterus (womb) for attachment of the blastocyst (fertilized egg) and the beginning of a pregnancy.

Originally advanced in 1993 (Murphy 1993)[1] and subsequently elaborated in 1994 (Murphy and Shaw 1994),[2] the concept has gained widespread acceptance [3][4][5][6][7][8] as a useful way to think about changes in the epithelial cells which line the uterus as they progress towards becoming receptive for blastocyst implantation.

Subsequent reviews in 2000[9][10] and 2004[11] elaborated on the concept which has been extended to encompass all placental animals with live birth.

The final section of Murphy 2004[11] is a good summary of the concept and reads (slightly edited for this forum):

The many changes which take place in the uterine epithelium during early pregnancy have been suggested to represent a loss of polarity in these cells and this thought has been extended to suggest further that an epithelial-mesenchymal transition may occur in the cells during this time. These perceptive insights highlight the critical importance of uterine epithelial cells in uterine receptivity and in one sense recall earlier suggestions on events in uterine epithelial cells. These early thoughts on uterine epithelial cells highlighted the apical plasma membrane flattening and led to the term ‘attachment reaction’ being used to describe some of the membrane changes which occur during early pregnancy. This term was used to apply to those changes in the apical membrane of uterine epithelial cells upon contact with the blastocyst itself, or when opposing uterine epithelial cells came into physical contact at around the same time of early pregnancy in rats and mice. In particular, the term indicated that in those species with an ‘attachment reaction’, closure of the uterine lumen was involved such that little or no luminal space remained. However, as is now known, considerable change occurs in all compartments of the plasma membrane of uterine epithelial cells and these changes occupy most of early pregnancy in the rat and mouse with long, regular microvilli being converted into short, irregular structures as early as d 3, 2 to 3 days before the blastocyst even enters the uterus. As we have also seen, in a wide diversity of species, there are changes in the apical plasma membrane which have features in common with those seen in rats and mice and in many of these other species, closure of the uterine lumen does not occur.

A common process is especially suggested by observations in animals with an epitheliochorial placenta like pigs and camels: here, the epithelium is not breached and the mature placenta consists of extensive interdigitation of very long trophoblastic and uterine epithelial microvilli throughout pregnancy. Nonetheless, before and during initial contact between uterine epithelial cells and the blastocyst, the regular microvilli of the uterine epithelium flatten out, much as they do in rats and mice, after which they return (within the next 48 h) to form the interface of the mature placenta. Moreover, as we have also seen, there are molecular alterations in the plasma membrane during early pregnancy which have common aspects across species and here some of the large mucin molecules (such as MUC-1) are particularly instructive. Changes in the basal and lateral plasma membrane regions have also been documented in many species during early pregnancy in preparation for attachment, and these too show common aspects across species—especially some membrane junctional structures.

Therefore, to highlight that membrane alterations are a process during early pregnancy—not just an event at the time of attachment itself, to recognise the fact that both apical and basolateral alterations occur, that molecular changes are also evident, and that moreover, there appears to be a degree of commonality across species, we have suggested that alterations in the plasma membrane of uterine epithelial cells during early pregnancy be referred to collectively as “the plasma membrane transformation”. This term encapsulates the concept of a common and necessary process of change in all compartments of the plasma membrane of uterine epithelial cells as characteristic, across species, of the development of uterine receptivity for implantation.

References

  1. ↑ Murphy, C.R. The plasma membrane of uterine epithelial cells: structure and histochemistry. Gustav Fischer Verlag: Stuttgart and New York. 1993. (ISBN 3-437-11514-6). (also published as Progress in Histochemistry and Cytochemistry, volume 27, no. 3).
  2. ↑ Murphy, C.R. and T.J. Shaw. Plasma membrane transformation: a common response of uterine epithelial cells during the peri-implantation period. Cell Biology International 18: 1115-1128. 1994.
  3. ↑ Garrido-Gomez et al. Profiling the gene signature of endometrial receptivity: clinical results. Fertility and Sterility: 99: 1079-1085. 2013.
  4. ↑ Gipson, Ilene K., et al. "MUC16 is lost from the uterodome (pinopode) surface of the receptive human endometrium: in vitro evidence that MUC16 is a barrier to trophoblast adherence." Biology of reproduction 78.1 (2008): 134-142.
  5. ↑ Kabir-Salmani, M., Nikzad, H., Shiokawa, S., Akimoto, Y., & Iwashita, M. (2005). Secretory role for human uterodomes (pinopods): secretion of LIF. Molecular human reproduction, 11(8), 553-559.
  6. ↑ Kurihara, I., Lee, D. K., Petit, F. G., Jeong, J., Lee, K., Lydon, J. P., ... & Tsai, S. Y. (2007). COUP-TFII mediates progesterone regulation of uterine implantation by controlling ER activity. PLoS genetics, 3(6), e102. doi:10.1371/journal.pgen.0030102
  7. ↑ Díaz-Gimeno, P., Horcajadas, J. A., Martínez-Conejero, J. A., Esteban, F. J., Alamá, P., Pellicer, A., & Simón, C. (2011). A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertility and sterility, 95(1), 50-60.
  8. ↑ Chen, Jenny IC, Natalie J. Hannan, Yunxian Mak, Peter K. Nicholls, Jin Zhang, Adam Rainczuk, Peter G. Stanton, David M. Robertson, Lois A. Salamonsen, and Andrew N. Stephens. "Proteomic characterization of midproliferative and midsecretory human endometrium." Journal of proteome research 8, no. 4 (2009): 2032-2044.
  9. ↑ Murphy, C.R. Junctional barrier complexes undergo major alterations during the plasma membrane transformation of uterine epithelial cells. Human Reproduction 15, Supplement 3: 182-188. 2000.
  10. ↑ Murphy, C.R., M.J. Hosie and M.B. Thompson. The plasma membrane transformation facilitates pregnancy in both reptiles and lizards. Comparative Biochemistry and Physiology A 127: 433-439. 2000.
  11. 1 2 Murphy, C.R. Uterine receptivity and the plasma membrane transformation. Cell Research 14: 258-267. 2004.
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