Analysis of placental vascularization in a pharmacological rabbit model of IUGR induced by l-NAME, a nitric oxide synthase inhibitor

Placenta

Volumn 35, Issue 4, 2014, Pages 254-259

  Tarrade, A ^a,b   Lecarpentier, E ^a,b,c   Gil, S ^b,c   Morel, O ^a,d   Zahr, N ^e   Dahirel, M ^a,b   Tsatsaris, V ^b,c,f   Chavatte Palmer, P ^a,b  

^a INRA Institut National de la Recherche Agronomique   (France)

^b Fondation PremUP   (France)

^c INSERM   (France)

^d Maternite Regionale Universitaire   (France)

^e PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^f Maternité Port Royal Hôpital Cochin Université Paris Descartes ^*  (France)

Author keywords

IUGR; l NAME; Placenta; Rabbit; Vascularization

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; N(G) NITROARGININE; N(G) NITROARGININE METHYL ESTER; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VIMENTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DENSITY; CONTROLLED STUDY; DRUG DOSE COMPARISON; FEMALE; FETUS BLOOD; FETUS GROWTH; FETUS WEIGHT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RESTRICTION; INTRAUTERINE GROWTH RETARDATION; LIMIT OF QUANTITATION; MATERNAL BLOOD; NONHUMAN; PLACENTAL TRANSFER; PLACENTAL VASCULARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; SEX DETERMINATION; STEREOMETRY; TROPHOBLAST; VASCULARIZATION; ANGIOGENESIS; ANIMAL; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; FETOMATERNAL TRANSFUSION; GENE EXPRESSION; METABOLISM; PLACENTA; PREGNANCY; RABBIT;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETAL GROWTH RETARDATION; GENE EXPRESSION; MATERNAL-FETAL EXCHANGE; NEOVASCULARIZATION, PHYSIOLOGIC; NG-NITROARGININE METHYL ESTER; NITROARGININE; PLACENTA; PREGNANCY; RABBITS;

EID: 84896544012     PISSN: 01434004     EISSN: 15323102     Source Type: Journal    
DOI: 10.1016/j.placenta.2014.01.013     Document Type: Article

References (45)

1. S.D. Chernausek Update: Consequences of abnormal fetal growth J Clin Endocrinol Metab 97 3 2012 689 695
2. L.M. Nardozza, E. Araujo Junior, M.M. Barbosa, A.C. Caetano, D.J. Lee, and A.F. Moron Fetal growth restriction: Current knowledge to the general Obs/Gyn Arch Gynecol Obstet 286 1 2012 1 13
3. L. Myatt, A.L. Eis, D.E. Brockman, I.A. Greer, and F. Lyall Endothelial nitric oxide synthase in placental villous tissue from normal, pre-eclamptic and intrauterine growth restricted pregnancies Hum Reprod 12 1 1997 167 172
4. L.G. Thaete, D.M. Kushner, E.R. Dewey, and M.G. Neerhof Endothelin and the regulation of uteroplacental perfusion in nitric oxide synthase inhibition-induced fetal growth restriction Placenta 26 2-3 2005 242 250
5. S.M. Sladek, R.R. Magness, and K.P. Conrad Nitric oxide and pregnancy Am J Physiol 272 2 Pt 2 1997 R441 R463
6. B.J. Krause, M.A. Hanson, and P. Casanello Role of nitric oxide in placental vascular development and function Placenta 32 11 2011 797 805
7. J.K. Chang, C. Roman, and M.A. Heymann Effect of endothelium-derived relaxing factor inhibition on the umbilical-placental circulation in fetal lambs in utero Am J Obstet Gynecol 166 2 1992 727 734
8. A.L. McCarthy, R.G. Woolfson, B.J. Evans, D.R. Davies, S.K. Raju, and L. Poston Functional characteristics of small placental arteries Am J Obstet Gynecol 170 3 1994 945 951
9. L. Myatt, A.S. Brewer, G. Langdon, and D.E. Brockman Attenuation of the vasoconstrictor effects of thromboxane and endothelin by nitric oxide in the human fetal-placental circulation Am J Obstet Gynecol 166 1 Pt 1 1992 224 230
10. C. Yallampalli, and R.E. Garfield Inhibition of nitric oxide synthesis in rats during pregnancy produces signs similar to those of preeclampsia Am J Obstet Gynecol 169 5 1993 1316 1320
11. L.A. Hefler, C.B. Tempfer, R.M. Moreno, W.E. O'Brien, and A.R. Gregg Endothelial-derived nitric oxide and angiotensinogen: Blood pressure and metabolism during mouse pregnancy Am J Physiol Regul Integr Comp Physiol 280 1 2001 R174 R182
12. L.C. Kusinski, J.L. Stanley, M.R. Dilworth, C.J. Hirt, I.J. Andersson, and L.J. Renshall et al. eNOS knockout mouse as a model of fetal growth restriction with an impaired uterine artery function and placental transport phenotype Am J Physiol Regul Integr Comp Physiol 303 1 2012 R86 R93
13. S. Kulandavelu, K.J. Whiteley, S.A. Bainbridge, D. Qu, and S.L. Adamson Endothelial NO synthase augments fetoplacental blood flow, placental vascularization, and fetal growth in mice Hypertension 61 1 2013 259 266
14. B. Fischer, P. Chavatte-Palmer, C. Viebahn, A. Navarrete Santos, and V. Duranthon Rabbit as a reproductive model for human health Reproduction 144 1 2012 1 10
15. A.C. Enders Reasons for diversity of placental structure Placenta 30 Suppl. A 2009 S15 S18
16. P. Chavatte-Palmer, P. Laigre, E. Simonoff, P. Chesne, M. Challah-Jacques, and J.P. Renard In utero characterisation of fetal growth by ultrasound scanning in the rabbit Theriogenology 69 7 2008 859 869
17. E. Lecarpentier, O. Morel, A. Tarrade, M. Dahirel, M. Bonneau, and E. Gayat et al. Quantification of utero-placental vascularization in a rabbit model of IUGR with three-dimensional power Doppler angiography Placenta 33 10 2012 769 775
18. J. Mao, X. Zhang, P.T. Sieli, M.T. Falduto, K.E. Torres, and C.S. Rosenfeld Contrasting effects of different maternal diets on sexually dimorphic gene expression in the murine placenta Proc Natl Acad Sci U S A 107 12 2010 5557 5562
19. C. Gallou-Kabani, A. Gabory, J. Tost, M. Karimi, S. Mayeur, and J. Lesage et al. Sex- and diet-specific changes of imprinted gene expression and DNA methylation in mouse placenta under a high-fat diet PLoS One 5 12 2010 e14398
20. A. Tarrade, D. Rousseau-Ralliard, M. Aubrière, N. Peynot, M. Dahirel, and J. Bertrand-Michel et al. Sexual dimorphism of the feto-placental phenotype in response to a high fat and control maternal diets in a rabbit model PloS One 8 12 2013 e83458
21. V. Diaz-Hernandez, A. Leon del Rio, M. Zamora, and H. Merchant-Larios Expression profiles of SRY and SOX9 in rabbit gonads: The classical model of mammalian sex differentiation Sex Dev 2 3 2008 152 166
22. P.O. Favaron, A.M. Mess, M.F. de Oliveira, A. Gabory, M.A. Miglino, and P. Chavatte-Palmer et al. Morphometric analysis of the placenta in the new world mouse necromys lasiurus (Rodentia, Cricetidae): A comparison of placental development in cricetids and murids Reprod Biol Endocrinol 11 1 2013 10
23. J.A. Avontuur, S.L. Buijk, and H.A. Bruining Distribution and metabolism of N(G)-nitro-L-arginine methyl ester in patients with septic shock Eur J Clin Pharmacol 54 8 1998 627 631
24. A. Kaya, A. Boztosun, H. Seckin, A.S. Guven, Z. Kucukdurmaz, and S. Gulturk et al. The evaluation of hypoxia-inducible factor 1 in N-nitro-l-arginine methyl ester preeclampsia model of pregnant rats J Investig Med 59 8 2011 1268 1272
25. G. Losonczy, I. Mucha, V. Muller, T. Kriston, Z. Ungvari, and L. Tornoci et al. The vasoconstrictor effects of L-NAME, a nitric oxide synthase inhibitor, in pregnant rabbits Br J Pharmacol 118 4 1996 1012 1018
26. M.O. Bahtiyar, C. Buhimschi, V. Ravishankar, J. Copel, E. Norwitz, and S. Julien et al. Contrasting effects of chronic hypoxia and nitric oxide synthase inhibition on circulating angiogenic factors in a rat model of growth restriction Am J Obstet Gynecol 196 1 2007 72 e1-6
27. H. Khan, K.T. Kusakabe, S. Wakitani, M. Hiyama, A. Takeshita, and Y. Kiso Expression and localization of NO synthase isoenzymes (iNOS and eNOS) in development of the rabbit placenta J Reprod Dev 58 2 2012 231 236
28. A.N. Sferruzzi-Perri, J.A. Owens, K.G. Pringle, J.S. Robinson, and C.T. Roberts Maternal insulin-like growth factors-I and -II act via different pathways to promote fetal growth Endocrinology 147 7 2006 3344 3355
29. C.P. Sibley, P.M. Coan, A.C. Ferguson-Smith, W. Dean, J. Hughes, and P. Smith et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta Proc Natl Acad Sci U S A 101 21 2004 8204 8208
30. M. Constancia, E. Angiolini, I. Sandovici, P. Smith, R. Smith, and G. Kelsey et al. Adaptation of nutrient supply to fetal demand in the mouse involves interaction between the Igf2 gene and placental transporter systems Proc Natl Acad Sci U S A 102 52 2005 19219 19224
31. C.T. Roberts, J.A. Owens, and A.N. Sferruzzi-Perri Distinct actions of insulin-like growth factors (IGFs) on placental development and fetal growth: Lessons from mice and guinea pigs Placenta 29 Suppl. A 2008 S42 S47
32. F. Herr, O.D. Liang, J. Herrero, U. Lang, K.T. Preissner, and V.K. Han et al. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy J Clin Endocrinol Metab 88 10 2003 4811 4817
33. S. Cebe-Suarez, A. Zehnder-Fjallman, and K. Ballmer-Hofer The role of VEGF receptors in angiogenesis; complex partnerships Cell Mol Life Sci 63 5 2006 601 615
34. J. Kroll, and J. Waltenberger VEGF-A induces expression of eNOS and iNOS in endothelial cells via VEGF receptor-2 (KDR) Biochem Biophys Res Commun 252 3 1998 743 746
35. D. Fukumura, T. Gohongi, A. Kadambi, Y. Izumi, J. Ang, and C.O. Yun et al. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability Proc Natl Acad Sci U S A 98 5 2001 2604 2609
36. M. Ziche, L. Morbidelli, R. Choudhuri, H.T. Zhang, S. Donnini, and H.J. Granger et al. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis J Clin Invest 99 11 1997 2625 2634
37. T. Murohara, T. Asahara, M. Silver, C. Bauters, H. Masuda, and C. Kalka et al. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia J Clin Invest 101 11 1998 2567 2578
38. H. Abe, W. Ishikawa, T. Kushima, T. Nishimura, C. Mori, and A. Onuki et al. Nitric oxide induces vascular endothelial growth factor expression in the rat placenta in vivo and in vitro Biosci Biotechnol Biochem 77 5 2013 971 976
39. I.M. Grumbach, W. Chen, S.A. Mertens, and D.G. Harrison A negative feedback mechanism involving nitric oxide and nuclear factor kappa-B modulates endothelial nitric oxide synthase transcription J Mol Cell Cardiol 39 4 2005 595 603
40. H. Bassan, L.L. Trejo, N. Kariv, M. Bassan, E. Berger, and A. Fattal et al. Experimental intrauterine growth retardation alters renal development Pediatr Nephrol 15 3-4 2000 192 195
41. M. Camprubi, A. Ortega, A. Balaguer, I. Iglesias, M. Girabent, and J. Callejo et al. Cauterization of meso-ovarian vessels, a new model of intrauterine growth restriction in rats Placenta 30 9 2009 761 766
42. E. Eixarch, F. Figueras, E. Hernandez-Andrade, F. Crispi, A. Nadal, and I. Torre et al. An experimental model of fetal growth restriction based on selective ligature of uteroplacental vessels in the pregnant rabbit Fetal Diagn Ther 26 4 2009 203 211
43. H. Bassan, D. Kidron, M. Bassan, M. Rotstein, N. Kariv, and E. Giladi et al. The effects of vascular intrauterine growth retardation on cortical astrocytes J Matern Fetal Neonatal Med 23 7 2010 595 600
44. E. Eixarch, E. Hernandez-Andrade, F. Crispi, M. Illa, I. Torre, and F. Figueras et al. Impact on fetal mortality and cardiovascular Doppler of selective ligature of uteroplacental vessels compared with undernutrition in a rabbit model of intrauterine growth restriction Placenta 32 4 2011 304 309
45. U. Neitzke, T. Harder, and A. Plagemann Intrauterine growth restriction and developmental programming of the metabolic syndrome: A critical appraisal Microcirculation 18 4 2011 304 311