Intrauterine Growth Restriction and Shallower Implantation Site in Rats with Maternal Hyperinsulinemia are Associated with Altered NOS Expression

Placenta

Volumn 30, Issue 10, 2009, Pages 898-906

  Skarzinski, G ^a   Khamaisi, M ^b   Bursztyn, M ^a   Mekler, J ^a   Lan, D ^c   Evdokimov, P ^c   Ariel, I ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b RAMBAM MEDICAL CENTER   (Israel)

^c Hadassah Academic College   (Israel)

Author keywords

Intrauterine growth restriction; Mesometrial triangle; Nitric oxide synthase; Rat model; Trophoblast invasion

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; NEURONAL NITRIC OXIDE SYNTHASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE MEASUREMENT; CELL INVASION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOTHELIUM CELL; FEMALE; FETUS; FETUS WEIGHT; HYPERINSULINEMIA; IMMUNOHISTOCHEMISTRY; INTRAUTERINE GROWTH RETARDATION; MALE; MATERNAL DIABETES MELLITUS; MATERNAL HYPERTENSION; NIDATION; NITROSYLATION; NONHUMAN; PHENOTYPE; PLACENTA WEIGHT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN VARIANT; RAT; SMALL FOR DATE INFANT; SYSTOLIC BLOOD PRESSURE; TROPHOBLAST; WESTERN BLOTTING;

ANIMALS; BLOOD PRESSURE; CELL CYCLE; CELL PROLIFERATION; EMBRYO IMPLANTATION; ENDOTHELIUM, VASCULAR; FEMALE; FETAL GROWTH RETARDATION; FETAL WEIGHT; HYPERINSULINISM; INSULIN; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; ORGAN SIZE; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS; RATS; RATS, WISTAR; TROPHOBLASTS;

EID: 70249104605     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2009.07.014     Document Type: Article

References (43)

1. Osol G., and Mandala M. Maternal uterine vascular remodeling during pregnancy. Physiology 24 (2009) 58-71
2. Kaufmann P., Black S., and Huppertz B. Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol Reprod 69 (2003) 1-7
3. Ain R., Canham L.N., and Soares M.J. Gestation stage-dependent intrauterine trophoblast cell invasion in the rat and mouse: novel endocrine phenotype and regulation. Dev Biol 260 (2003) 176-190
4. Vercruysse L., Caluwaerts S., Luyten C., and Pijnenborg R. Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta 27 (2006) 22-33
5. Caluwaerts S., Vercruysse L., Luyten C., and Pijnenborg R. Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta 26 (2005) 574-584
6. Sowers J.R., Saleh A.A., and Sokol R.J. Hyperinsulinemia and insulin resistance are associated with preeclampsia in African-Americans. Am J Hypertens 8 (1995) 1-4
7. Martinez Abundis E., Gonzalez Ortiz M., Quiñones Galvan A., and Ferrannini E. Hyperinsulinemia in glucose tolerant women with preeclampsia: a controlled study. Am J Hypertens 9 (1996) 610-614
8. Meisel B., Jovanovic-Peterson L., Bevier W., and Peterson C.M. The rubenesque pregnancy: a progression towards higher blood pressure correlates with a measure of endogenous and exogenous insulin levels. Am J Perinatal 14 (1997) 181-186
9. Solomon C.G., and Seely E.W. Brief review: hypertension in pregnancy: a manifestation of the insulin resistance syndrome?. Hypertension 37 (2001) 232-239
10. Podjarny E., Bernheim J., Katz B., Green J., Mekler J., and Bursztyn M. Chronic exogenous hyperinsulinaemia in pregnancy: a rat model of pregnancy-induced hypertension. J Am Soc Nephrol 9 (1998) 9-13
11. Podjarny E., Bursztyn M., Rashed G., Benchetrit S., Katz B., Green J., et al. Chronic exogenous hyperinsulinaemia-induced hypertension in pregnant rats: effect of chronic treatment with l-arginine. Clin Sci (Lond) 100 (2001) 667-671
12. Bursztyn M., Podjarny E., Dahan R., Raz I., and Bernheim J. Insulin-induced hypertension, l-arginine, and endothelial nitric oxide synthase in pregnant rats. Hypertens Pregnancy 22 (2003) 267-274
13. Bursztyn M., Gross M.L., Goltser-Dubner T., Koleganova N., Birman T., Smith Y., et al. Adult hypertension in intrauterine growth-restricted offspring of hyperinsulinemic rats. Evidence of subtle renal damage. Hypertension 48 (2006) 717-723
14. Gude N.M., King R.G., and Brennecke S.P. Role of endothelium-derived nitric oxide in maintenance of low fetal vascular resistance in placenta. Lancet 336 (1990) 1589-1590
15. Brosens A., Robertson W.B., and Dixon H.G. The role of the spiral arteries in the pathogenesis of pre-eclampsia. In: Wynn R.M. (Ed). Obstetrics and gynecology annual vol. 1 (1972), Appleton-Century-Crofts, New York 177-191
16. Rosario G.X., Konno T., and Soares M.J. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol 314 (2008) 362-375
17. Geusens N., Verlohren S., Luyten C., Taube M., Hering L., Vercruysse L., et al. Endovascular trophoblast invasion, spiral artery remodelling and uteroplacental haemodynamics in a transgenic rat model of pre-eclampsia. Placenta 29 (2008) 614-623
18. Lyall F., Robson S.C., Bulmer J.N., Kelly H., and Duffie E. Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am J Pathol 154 (1999) 1105-1114
19. Lyall F. Priming and remodelling of human placental bed spiral arteries during pregnancy - a review. Placenta 26 Suppl. A (2005) S31-S36
20. Harris L.K., McCormick J., Cartwright J.E., Whitley G.S.J., and Dash P.R. S-nitrosylation of proteins at the leading edge of migrating trophoblasts by inducible nitric oxide synthase promotes trophoblast invasion. Exp Cell Res 314 (2008) 1765-1778
21. Bursztyn M., Ben-Ishay D., Mekler J., and Raz I. Chronic exogenous hyperinsulinemia without sugar supplementation: acute salt-sensitive hypertension without changes in resting blood pressure. J Hypertens 11 (1993) 703-707
22. Bursztyn, Mekler J., Peleg E., and Bernheim J. Subpressor dose of L-NAME unmasks hypertensive effect of chronic hyperinsulinemia. Hypertension 36 (2000) 872-877
23. Adamson S.L., Lu Y., Whiteley K.J., Holmyard D., Hemberger M., Pfarrer C., et al. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 250 (2002) 358-373
24. Kusakabe K., Naka M., Ito Y., Eid N., and Otsuki Y. Regulation of natural-killer cell cytotoxicity and enhancement of complement factors in the spontaneously aborted mouse placenta. Fertil Steril 90 4 Suppl. (2008) 1451-1459
25. Ramuz O., Isnardon D., Devilard E., Charafe-Jauffret E., Hassoun J., Birg F., et al. Constitutive nuclear localization and initial cytoplasmic apoptotic activation of endogenous caspase-3 evidenced by confocal microscopy. Int J Exp Pathol 84 (2003) 75-81
26. Khamaisi M., Keynan S., Bursztyn M., Dahan R., Reinhartz E., Ovadia H., et al. Role of renal nitric oxide synthase in diabetic kidney disease during the chronic phase of diabetes. Nephron Physiol 102 (2006) 72-80
27. Hendzel M.J., Wei Y., Mancini M.A., Ranalli T., Brinkley B.R., Bazett-Jones D.P., et al. Mitosis-specific phosphorylation of histone H3 initiates in centromeric heterochromatin and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106 (1997) 348-360
28. Davies J., and Glasser S.R. Histological and fine structural observations on the placenta of the rat. Acta Anat 69 (1968) 542-608
29. Sladek S.M., Magness R.R., and Conrad K.P. Nitric oxide and pregnancy. Am J Physiol 272 (1997) R441-R463
30. Buhimschi I.A., Saade G.R., Chwalisz K., and Garfield R.E. The nitric oxide pathway in pre-eclampsia: pathophysiological implications. Hum Reprod Update 4 (1998) 25-42
31. Schiessl B., Mylonas I., Hantschmann P., Kuhn C., Schulze S., Kunze S., et al. Expression of endothelial NO synthase, inducible NO synthase and estrogen receptors alpha and beta in placental tissue of normal, preeclamptic, and intrauterine growth restricted pregnancies. J Histochem Cytochem 53 (2005) 1441-1449
32. Molnar M., Suto T., Toth T., and Hertelendy F. Prolonged blockade of nitric oxide synthesis in gravid rats produces sustained hypertension, proteinuria, thrombocytopenia, and intrauterine growth retardation. Am J Obstet Gynecol 170 (1994) 1458-1466
33. Yallampalli C., and Garfield R.E. Inhibition of nitric oxide synthesis in rats during pregnancy produces signs similar to those of preeclampsia. Am J Obstet Gynecol 169 (1993) 1316-1320
34. Ariel I., Hochberg A., and Shochina M. Endothelial nitric oxide synthase immunoreactivity in early gestation and in trophoblastic disease. J Clin Pathol 51 (1998) 427-431
35. Zarlingo T.J., Eis A.L., Brockman D.E., Kossenjans W., and Myatt L. Comparative localization of endothelial and inducible nitric oxide synthase isoforms in haemochorial and epitheliochorial placentae. Placenta 18 (1997) 511-520
36. Purcell T.L., Buhimschi I., Given R., Chwalisz K., and Garfield R.E. Inducible nitric oxide synthase is present in the rat placenta at the fetal-maternal interface and decreases prior to labour. Mol Hum Reprod 3 (1997) 485-491
37. Melillo G., Musso T., Sica A., Taylor L.S., Cox G.W., and Varesio L. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182 (1995) 1683-1693
38. Kadyrov M., Kingdom J.C., and Huppertz B. Divergent trophoblast invasion and apoptosis in placental bed spiral arteries from pregnancies complicated by maternal anemia and early-onset preeclampsia/intrauterine growth restriction. Am J Obstet Gynecol 194 (2006) 557-563
39. Hunt J.S., Miller L., Vassmer D., and Croy B.A. Expression of the inducible nitric oxide synthase gene in mouse uterine leukocytes and potential relationships with uterine function during pregnancy. Biol Reprod 57 (1997) 827-836
40. Kim Y.J., Park H.S., Lee H.Y., Ha E.H., Suh S.H., Oh S.K., et al. Reduced l-arginine level and decreased placental eNOS activity in preeclampsia. Placenta 27 (2006) 438-444
41. Khorram O., Han G., and Magee T. Cigarette smoke inhibits endometrial epithelial cell proliferation through a nitric oxide-mediated pathway. Fertil Steril (2008 Nov 18) [Epub ahead of print]
42. Lin I.C., Smartt Jr. J.M., Nah H.D., Ischiropoulos H., and Kirschner R.E. Nitric oxide stimulates proliferation and differentiation of fetal calvarial osteoblasts and dural cells. Plast Reconstr Surg 121 (2008) 1554-1566
43. Thomas D.D., Ridnour L.A., Isenberg J.S., Flores-Santana W., Switzer C.H., Donzelli S., et al. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45 (2008) 18-31