Novel 3D Microscopic Analysis of Human Placental Villous Trees Reveals Unexpected Significance of Branching Angles

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Haeussner, Eva ^a   Buehlmeyer, Antonia ^a   Schmitz, Christoph ^a   Von Koch, Franz Edler ^b   Frank, Hans Georg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b Department of Obstetrics and Gynaecology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANATOMY AND HISTOLOGY; CHORION VILLUS; FEMALE; HUMAN; PREGNANCY; THREE DIMENSIONAL IMAGING;

CHORIONIC VILLI; FEMALE; HUMANS; IMAGING, THREE-DIMENSIONAL; PREGNANCY;

EID: 84906673336     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep06192     Document Type: Article

References (43)

1. Boyd, J. D. & Hamilton, W. J. The human placenta. (Heffer, Cambridge, 1970).
2. Kaufmann, P. Development and differentiation of the human placental villous tree. Bibl. Anat. 22, 29-39 (1982).
3. Kingdom, J., Huppertz, B., Seaward, G. & Kaufmann, P. Development of the placental villous tree and its consequences for fetal growth. Eur. J. Obstet. Gynecol. Reprod. Biol. 92, 35-43 (2000).
4. Benirschke, K., Burton, G. & Baergen, R. N. Pathology of the human placenta. (Springer, Berlin and London, 2012).
5. Barker, S. B., Cumming, G. & Horsfield, K. Quantitative morphometry of the branching structure of trees. J. Theor. Biol. 40, 33-43 (1973).
6. Wollaston,W. H. Description of the Camera Lucida. Philosophical Magazine 27, 343-347 (1807).
7. Halavi, M., Hamilton, K. A., Parekh, R. & Ascoli, G. A. Digital reconstructions of neuronal morphology: three decades of research trends. Front. Neurosci. 6, 49-61 (2012).
8. Marx, M., Günter, R. H., Hucko, W., Radnikow, G. & Feldmeyer, D. Improved biocytin labeling and neuronal 3Dreconstruction. Nat. Protoc. 7, 394-407 (2012).
9. Aguiar, P., Sousa, M. & Szucs, P. Versatile morphometric analysis and visualization of the three-dimensional structure of neurons. Neuroinformatics 11, 393-403 (2013).
10. Földy, C., Malenka, R. C. & Südhof, T. C. Autism-associated neuroligin-3 mutations commonly disrupt tonic endocannabinoid signaling. Neuron 78, 498-509 (2013).
11. Eisenstein, M. Neural circuits: Putting neurons on the map. Nature 461, 1149-1152 (2009).
12. Helmstaedter, M., Sakmann, B. & Feldmeyer, D. The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. Cereb. Cortex 19, 938-950 (2009).
13. Oberlaender,M. et al. Three-dimensional axon morphologies of individual layer 5 neurons indicate cell type-specific intracortical pathways for whisker motion and touch. Proc. Natl. Acad. Sci. USA 108, 4188-4193 (2011).
14. Oberlaender, M. et al. Cell type-specific three-dimensional structure of thalamocortical circuits in a column of rat vibrissal cortex. Cereb. Cortex 22, 2375-2391 (2012).
15. Kaufmann, P., Mayhew, T. M. & Charnock-Jones, D. S. Aspects of human fetoplacental vasculogenesis and angiogenesis. II. Changes during normal pregnancy. Placenta 25, 114-126 (2004).
16. Howard, C. V. & Reed, M. G. Unbiased stereology: Three-dimensional measurement in microscopy. (BIOS Scientific Publ., Oxford, 1998).
17. Mayhew, T.M. Stereology and the placenta:where's the point? - a review. Placenta 27, S17-25 (2006).
18. Castellucci, M., Scheper, M., Scheffen, I., Celona, A. & Kaufmann, P. The development of the human placental villous tree. Anat. Embryol. (Berl) 181, 117-128 (1990).
19. Habashi, S., Burton, G. J. & Steven, D. H. Morphological study of the fetal vasculature of the human term placenta: scanning electron microscopy of corrosion casts. Placenta 4, 41-56 (1983).
20. Karen, P., Jirkovska, M., Tomori, Z., Demjenova, E., Janacek, J. & Kubinova, L. Three-dimensional computer reconstruction of large tissue volumes based on composing series of high-resolution confocal images by GlueMRC and LinkMRC software. Microsc. Res. Tech. 62, 415-422 (2003).
21. Jirkovska, M. et al. Topological properties and spatial organization of villous capillaries in normal and diabetic placentas. J. Vasc. Res. 39, 268-278 (2002).
22. Jirkovska, M., Janacek, J., Kalab, J. & Kubinova, L. Three-dimensional arrangement of the capillary bed and its relationship to microrheology in the terminal villi of normal term placenta. Placenta 29, 892-897 (2008).
23. Jirkovska, M. et al. The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta 33, 343-351 (2012).
24. Haeussner, E., Schmitz, C., Koch, F. V. & Frank, H. G. Birth weight correlates with size but not shape of the normal human placenta. Placenta 34, 574-582 (2013).
25. Burton, G. J. The fine structure of the human placental villus as revealed by scanning electron microscopy. Scanning Microsc. 1, 1811-1828 (1987).
26. Kubínová, L. et al. Confocal stereology and image analysis: methods for estimating geometrical characteristics of cells and tissues from three-dimensional confocal images. Physiol. Res. 53 Suppl 1, S47-55 (2004).
27. Glaser, J. &Glaser, E.Neuron imaging with neurolucida-A PC-based system for image combining microscopy. Comput. Med. Imag. Grap. 14, 307-317 (1990).
28. van Oppenraaij, R. H. F. et al. Vasculogenesis and angiogenesis in the first trimester human placenta: An innovative 3D study using an immersive virtual reality system. Placenta. 30, 220-222 (2009).
29. Kaufmann, P., Sen, D. K.&Schweikhart, G. Classification of human placental villi. I. Histology. Cell Tissue Res. 200, 409-423 (1979).
30. Sen, D. K., Kaufmann, P. &Schweikhart, G. Classification of human placental villi. II. Morphometry. Cell Tissue Res. 200, 425-434 (1979).
31. Mayhew, T. M. Fetoplacental angiogenesis during gestation is biphasic, longitudinal and occurs by proliferation and remodelling of vascular endothelial cells. Placenta 23, 742-750 (2002).
32. Rath, W. Geburtshilfe und Perinatologie. (Thieme, Stuttgart, 2010).
33. Karimu, A. L. & Burton, G. J. Star volume estimates of the intervillous clefts in the human placenta: How changes in umbilical arterial pressure might influence the maternal placental circulation. J. Dev. Physiol. 19, 137-142 (1993).
34. Mayhew, T. M. & Sisley, I. Quantitative studies on the villi, trophoblast and intervillous pores of placentae from women with well-controlled diabetes mellitus. Placenta 19, 371-377 (1998).
35. Radley, J. J. et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125, 1-6 (2004).
36. Cetin, I. & Taricco, E. [Clinical causes and aspects of placental insufficiency] The Placenta and Human Developmental Programming [Burton, G., Barker, D., Moffett, A. & Thornburg, K. (eds.)] [114-125] (Cambridge University Press, Cambridge, 2011).
37. Gundersen, H. J. & Jensen, E. B. The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229-263 (1987).
38. Schmitz, C. & Hof, P. R. Design-based stereology in neuroscience. Neuroscience 130, 813-831 (2005).
39. Sholl, D. A. Dendritic organization in the neurons of the visual and motor cortices of the cat. J. Anat. 87, 387-406 (1953).
40. Bronstein, I. N. & Semendjajew, K. A. Taschenbuch der Mathematik (Deutsch, Thun, 2001).
41. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B 57, 289-300 (1995).
42. R Core Team. R: A Language and Environment for Statistical Computing. Vienna and Austria: R Foundation for Statistical Computing. URL: http://www.R-project. org/ (Date of access:12/04/2014) (2013).
43. Revelle, W. psych: Procedures for Psychological, Psychometric, and Personality Research. Evanston and Illinois: Northwestern University. URL: http://CRAN.Rproject. org/package5psych (Date of access:12/04/2014) (2013).