Nuchal Edema and Venous-Lymphatic Phenotype Disturbance in Human Fetuses and Mouse Embryos With Aneuploidy

Journal of the Society for Gynecologic Investigation

Volumn 13, Issue 3, 2006, Pages 209-216

  Bekker, Mireille N ^a,b   van den Akker, Nynke M S ^b   Bartelings, Margot M ^b   Arkesteijn, Jenny B ^b   Fischer, Sigrid G L ^b   Polman, Japke A E ^b   Haak, Monique C ^a   Webb, Sandra ^c   Poelmann, Robert E ^b   van Vugt, John M G ^a   Gittenberger de Groot, Adriana C ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

endothelial differentiation; jugular lymphatic sac; lymphangiogenesis; Nuchal translucency; pathophysiology

Indexed keywords

BIOLOGICAL MARKER; LYMPHATIC VESSEL ENDOTHELIAL HYALURONAN RECEPTOR; NEUROPILIN 1; PODOPLANIN; PROTEIN; PROX 1; SMOOTH MUSCLE ACTIN; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ANEUPLOIDY; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL; CELL DIFFERENTIATION; CONTROLLED STUDY; EDEMA; EMBRYO; EMBRYO (ANATOMY); FETUS; FETUS (ANATOMY); GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPH VESSEL ENDOTHELIUM; MOUSE; MOUSE STRAIN; NONHUMAN; NUCHAL EDEMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE; TRISOMY 16; TRISOMY 18; TRISOMY 21; VEIN DISEASE; WILD TYPE;

ANEUPLOIDY; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; DISEASE MODELS, ANIMAL; EDEMA; EMBRYO; ENDOTHELIAL CELLS; ENDOTHELIUM, LYMPHATIC; FETUS; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; LYMPHANGIOGENESIS; MICE; NECK; NUCHAL TRANSLUCENCY MEASUREMENT; PHENOTYPE; SKIN;

EID: 33646075955     PISSN: 10715576     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsgi.2006.02.003     Document Type: Article

References (37)

1. Sabin F.R. The lymphatic system in human embryos, with a consideration of the morphology of the system as a whole. Am J Anat 9 (1909) 43-91
2. Wigle J.T., and Oliver G. Prox1 function is required for the development of the murine lymphatic system. Cell 98 (1999) 769-778
3. Petrova T.V., Makinen T., Makela T.P., et al. Lymphatic endothelial reprogramming of vascular endothelial cells by the Prox-1 homeobox transcription factor. EMBO J 21 (2002) 4593-4599
4. Haak M.C., Bartelings M.M., Jackson D.G., Webb S., Van Vugt J.M.G., and Gittenberger-de Groot A.C. Increased nuchal translucency is associated with jugular lymphatic distension. Hum Reprod 17 (2002) 1086-1092
5. Gittenberger-De Groot A.C., Van Den Akker N.M., Bartelings M.M., Webb S., van Vugt J.M., and Haak M.C. Abnormal lymphatic development in trisomy 16 mouse embryos precedes nuchal edema. Dev Dyn 230 (2004) 378-384
6. Bekker M.N., Haak M.C., Rekoert-Hollander M., Twisk J.W.R., and van Vugt J.M.G. Increased nuchal translucency and distended jugular lymphatic sacs by first-trimester ultrasound. Ultrasound Obstet Gynecol 25 (2005) 239-245
7. Webb S., Brown N.A., and Anderson R.H. Cardiac morphology at late fetal stages in the mouse with trisomy 16. Consequences for different formation of the atrioventricular junction when compared to humans with trisomy 21. Cardiovasc Res 34 (1997) 515-524
8. Schacht V., Ramirez M.I., Hong Y.K., et al. T1alpha/podoplanin deficiency disrupts normal lymphatic vasculature formation and causes lymphedema. EMBO J 22 (2003) 3546-3556
9. Karkkainen M.J., and Alitalo K. Lymphatic endothelial regulation, lymphoedema, and lymph node metastasis. Semin Cell Dev Biol 13 (2002) 9-18
10. Lymboussaki A., Olofsson B., Eriksson U., and Alitalo K. Vascular endothelial growth factor (VEGF) and VEGF-C show overlapping binding sites in embryonic endothelia and distinct sites in differentiated adult endothelia. Circ Res 85 (1999) 992-999
11. Yuan L., Moyon D., Pardanaud L., et al. Abnormal lymphatic vessel development in neuropilin 2 mutant mice. Development 129 (2002) 4797-4806
12. Flamme I., von Reutern M., Drexler H.C., Syed-Ali S., and Risau W. Overexpression of vascular endothelial growth factor in the avian embryo induces hypervascularization and increased vascular permeability without alterations of embryonic pattern formation. Dev Biol 171 (1995) 399-414
13. Larcher F., Murillas R., Bolontrade M., Conti C.J., and Jorcano J.L. VEGF/VPF overexpression in skin of transgenic mice induces angiogenesis, vascular hyperpermeability and accelerated tumor development. Oncogene 17 (1998) 303-311
14. Nagy J.A., Vasile E., Feng D., et al. Vascular permeability factor/vascular endothelial growth factor induces lymphangiogenesis as well as angiogenesis. J Exp Med 196 (2002) 1497-1506
15. Martyn U., and Schulte-Merker S. Zebrafish neuropilins are differentially expressed and interact with vascular endothelial growth factor during embryonic vascular development. Dev Dyn 231 (2004) 33-42
16. Webb S., Browne N.A., and Anderson R.N. Cardiac morphology at late fetal stages in the mouse with trisomy 16. Consequences for different formation of the atrioventricular junction when compared to humans with trisomy 21. Cardiovasc Res 34 (1997) 515-524
17. Jackson D.G. Biology of the lymphatic marker LYVE-1 and applications in research into lymphatic tracking and lymphangiogenesis. APMIS 112 (2004) 526-538
18. Soker S., Miao H.Q., Nomi M., Takashima S., and Klagsbrun M. VEGF165 mediates formation of complexes containing VEGFR-2 and neuropilin-1 that enhance VEGF165-receptor binding. J Cell Biochem 85 (2002) 357-368
19. Kawasaki T., Kitsukawa T., Bekku Y., et al. A requirement for neuropilin-1 in embryonic vessel formation. Development 126 (1999) 4895-4902
20. Yamada Y., Takakura N., Yasue H., Ogawa H., Fujisawa H., and Suda T. Exogenous clustered neuropilin 1 enhances vasculogenesis and angiogenesis. Blood 97 (2001) 1671-1678
21. Bates D.O., and Harper S.J. Regulation of vascular permeability by vascular endothelial growth factors. Vasc Pharmacol 39 (2002) 225-237
22. Hattori M., Fujiyama A., Taylor T.D., et al. The DNA sequence of human chromosome 21. Nature 405 (2000) 311-319
23. Nagy J.A., Vasile E., Feng D., et al. VEGF-A induces angiogenesis, arteriogenesis, lymphangiogenesis, and vascular malformations. Cold Spring Harb Symp Quant Biol 67 (2002) 227-237
24. Petrova T.V., Karpanen T., Norrmen C., et al. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med 10 (2004) 974-981
25. Wigle J.T., Harvey N., Detmar M., et al. An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. EMBO J 21 (2002) 1505-1513
26. Pandya P.P., Kondylios A., Hilbert L., Snijders R.J., and Nicolaides K.H. Chromosomal defects and outcome in 1015 fetuses with increased nuchal translucency. Ultrasound Obstet Gynecol 5 (1995) 15-19
27. Bekker M.N., Arkesteijn J.B., Van Den Akker N.M., et al. Increased NCAM expression and vascular development in trisomy 16 mouse embryos. Relationship with nuchal translucency. Pediatr Res 58 (2005) 1222-1227
28. Akitaya T., and Bronner-Fraser M. Expression of cell adhesion molecules during initiation and cessation of neural crest cell migration. Dev Dyn 194 (1992) 12-20
29. Walsh F.S., and Doherty P. Neural cell adhesion molecules of the immunoglobulin superfamily. Role in axon growth and guidance. Annu Rev Cell Dev Biol 13 (1997) 425-456
30. Osborne N.J., Begbie J., Chilton J.K., Schmidt H., and Eickholt B.J. Semaphorin/neuropilin signaling influences the positioning of migratory neural crest cells within the hindbrain region of the chick. Dev Dyn 232 (2005) 939-949
31. Mukouyama Y.S., Gerber H.P., Ferrara N., Gu C., and Anderson D.J. Peripheral nerve-derived VEGF promotes arterial differentiation via neuropilin 1-mediated positive feedback. Development 132 (2005) 941-952
32. Torii M., Matsuzaki F., Osumi N., et al. Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 126 (1999) 443-456
33. Hyett J., Moscoso G., Papapanagiotou G., Perdu M., and Nicolaides K.H. Abnormalities of the heart and great arteries in chromosomally normal fetuses with increased nuchal translucency thickness at 11-13 weeks of gestation. Ultrasound Obstet Gynecol 7 (1996) 245-250
34. Hyett J., Moscoso G., and Nicolaides K. Abnormalities of the heart and great arteries in first trimester chromosomally abnormal fetuses. Am J Med Genet 69 (1997) 207-216
35. Waller III B.R., McQuinn T., Phelps A.L., et al. Conotruncal anomalies in the trisomy 16 mouse. An immunohistochemical analysis with emphasis on the involvement of the neural crest. Anat Rec 260 (2000) 279-293
36. Bergwerff M., DeRuiter M.C., Hall S., Poelmann R.E., and Gittenberger-De Groot A.C. Unique vascular morphology of the fourth aortic arches. Possible implications for pathogenesis of type-B aortic arch interruption and anomalous right subclavian artery. Cardiovasc Res 44 (1999) 185-196
37. Kirby M.L. Neural crest and the morphogenesis of Down syndrome with special emphasis on cardiovascular development. Prog Clin Biol Res 373 (1991) 215-225