Expression of angiogenic factors in placenta of stressed rats
Isis Paloppi Corrêa A , Rodrigo Ruano A C , Nilton Hideto Takiuti A , Rossana Pulcinelli Vieira Francisco A , Estela Bevilacqua B and Marcelo Zugaib A
+ Author Affiliations
- Author Affiliations
A Department of Obstetrics and Gynecology, Faculty of Medicine, University of São Paulo, São Paulo, Brazil.
B Department of Cell and Developmental Biology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
C Corresponding author. Email: rodrigoruano@usp.br
Reproduction, Fertility and Development 24(6) 851-858 https://doi.org/10.1071/RD11202
Submitted: 12 August 2011 Accepted: 8 December 2011 Published: 10 February 2012
Abstract
The aim of the present study was to analyse the influence of stress on pregnant rats, particularly in terms of maternal, placental and fetal weight, placental morphology and placental gene expression of the angiogenic factors Vegfa and Pgf and their receptors. The parameters were evaluated on gestation Day 20. Maternal, fetal and placental weights were statistically lower in stressed animals than controls, suggesting abnormalities in gestational physiology. Morphologically the placentas of rats subjected to stress were reduced in size and weight, with few glycogen cells and a significant increase in the number of apoptotic cells. Stress caused an increase in placental gene expression of Vegfa (P < 0.05) and a reduction in Pgf, Flt1 and Kdr expression (P < 0.05). It has been suggested that increased VEGF is associated with vasodilatation and hypotension, but in this model persistent hypertension was present. This study suggests that the limited hypotensive Vegfa response to stress-induced hypertension could result from reduced expression of Flt1/Kdr disrupting specific VEGF pathways. These findings may elucidate one of the multiple possible factors underlying how stress modulates placental physiology, and could aid the understanding of stress-induced gestational disorders.
Additional keywords: animal models, maternal–fetal interaction, stress.
References
Ahmed, A., Dunk, C., Kniss, D., and Wilkes, M. (1997). Role of VEGF receptor-1 (Flt-1) in mediating calcium-dependent nitric oxide release and limiting DNA synthesis in human trophoblast cells. Lab. Invest. 76, 779–791.| 1:CAS:528:DyaK2sXktlOrsr4%3D&md5=be6d9b72d71c613289d9eee7fda7e53aCAS | 9194854PubMed |
Åsberg, M., Nygren, Å., Leopardi, R., Rylander, G., Peterson, U., Wilczek, L., Källmén, H., Ekstedt, M., Åkerstedt, T., Lekander, M., and Ekman, R. (2009). Novel biochemical markers of psychosocial stress in women. PLoS ONE 4, e3590.
| Novel biochemical markers of psychosocial stress in women.Crossref | GoogleScholarGoogle Scholar | 19177163PubMed |
Baisden, B., Sonne, S., Joshi, R. M., Ganapathy, V., and Shekhawat, P. S. (2007). Antenatal dexamethasone treatment leads to changes in gene expression in a murine late placenta. Placenta 28, 1082–1090.
| Antenatal dexamethasone treatment leads to changes in gene expression in a murine late placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVWmsLnO&md5=ee19a6b2f116b2bda05875c5beb81e15CAS | 17559929PubMed |
Balanos, G. M., Phillips, A. C., Frenneaux, M. P., McIntyre, D., Lykidis, C., Griffin, H. S., and Carroll, D. (2010). Metabolically exaggerated cardiac reactions to acute psychological stress: the effects of resting blood pressure status and possible underlying mechanisms. Biol. Psychol. 85, 104–111.
| Metabolically exaggerated cardiac reactions to acute psychological stress: the effects of resting blood pressure status and possible underlying mechanisms.Crossref | GoogleScholarGoogle Scholar | 20541585PubMed |
Barker, D. J., Osmond, C., Forsen, T. J., Kajantie, E., and Eriksson, J. G. (2007). Maternal and social origins of hypertension. Hypertension 50, 565–571.
| Maternal and social origins of hypertension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlyktb4%3D&md5=853a631e59af2a97476154a7a342286dCAS | 17620523PubMed |
Bernatova, I., and Csizmadiova, Z. (2006). Effect of chronic social stress on nitric oxide synthesis and vascular function in rats with family history of hypertension. Life Sci. 78, 1726–1732.
| Effect of chronic social stress on nitric oxide synthesis and vascular function in rats with family history of hypertension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhsl2hs7o%3D&md5=8c14fbfb4f96fe7ad65a505e3e0181cdCAS | 16253277PubMed |
Beydoun, H., and Saftlas, A. F. (2008). Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence. Paediatr. Perinat. Epidemiol. 22, 438–466.
| Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence.Crossref | GoogleScholarGoogle Scholar | 18782252PubMed |
Chan, J., Rabbitt, E. H., Innes, B. A., Bulmer, J. N., Stewart, P. M., Kilby, M. D., and Hewison, M. (2007). Glucocorticoid-induced apoptosis in human decidua: a novel role for 11beta-hydroxysteroid dehydrogenase in late gestation. J. Endocrinol. 195, 7–15.
| Glucocorticoid-induced apoptosis in human decidua: a novel role for 11beta-hydroxysteroid dehydrogenase in late gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlWiurfN&md5=7f44b228308d985ed88d89bc8b591d77CAS | 17911392PubMed |
Cross, M. J., and Claesson-Welsh, L. (2001). FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition. Trends Pharmacol. Sci. 22, 201–207.
| FGF and VEGF function in angiogenesis: signalling pathways, biological responses and therapeutic inhibition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1Wntr8%3D&md5=08bc9ad0f07ea8c6bba039c59c431039CAS | 11282421PubMed |
Djordjevic, J., Vuckovic, T., Jasnic, N., and Cvijic, G. (2007). Effect of various stressors on the blood ACTH and corticosterone concentration in normotensive Wistar and spontaneously hypertensive Wistar–Kyoto rats. Gen. Comp. Endocrinol. 153, 217–220.
| Effect of various stressors on the blood ACTH and corticosterone concentration in normotensive Wistar and spontaneously hypertensive Wistar–Kyoto rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotlSiur0%3D&md5=a682e49993e3e59ea018a1279227bfdfCAS | 17383653PubMed |
D’mello, A. P., and Liu, Y. (2006). Effects of maternal immobilization stress on birth weight and glucose homeostasis in the offspring. Psychoneuroendocrinology 31, 395–406.
| Effects of maternal immobilization stress on birth weight and glucose homeostasis in the offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhsl2jt7w%3D&md5=4d07706bba1352b393b07f48fb68b5b0CAS | 16359821PubMed |
Ferrara, N., Gerber, H. P., and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669–676.
| The biology of VEGF and its receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFOnur4%3D&md5=c20dc1b32afbe799b986677f162e15d3CAS | 12778165PubMed |
Fowden, A. L., Forhead, A. J., Coan, P. M., and Burton, G. J. (2008). The placenta and intrauterine programming. J. Neuroendocrinol. 20, 439–450.
| The placenta and intrauterine programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkslygurc%3D&md5=eb9a565e0225e3df3ae4de7ce3f3044eCAS | 18266944PubMed |
Haelterman, E., Marcoux, S., Croteau, A., and Dramaix, M. (2007). Population-based study on occupational risk factors for preeclampsia and gestational hypertension. Scand. J. Work Environ. Health 33, 304–317.
| 17717623PubMed |
Hewitt, D. P., Mark, P. J., and Waddell, B. J. (2006). Glucocorticoids prevent the normal increase in placental vascular endothelial growth factor expression and placental vascularity during late pregnancy in the rat. Endocrinology 147, 5568–5574.
| Glucocorticoids prevent the normal increase in placental vascular endothelial growth factor expression and placental vascularity during late pregnancy in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1yqtr7M&md5=51cb0a7fe6a02c835e36c70beb314caeCAS | 16959835PubMed |
Hobel, C. J., Goldstein, A., and Barrett, E. S. (2008). Psychosocial stress and pregnancy outcome. Clin. Obstet. Gynecol. 51, 333–348.
| Psychosocial stress and pregnancy outcome.Crossref | GoogleScholarGoogle Scholar | 18463464PubMed |
Hoshida, M. S., Gorjão, R., Lima, C., Daher, S., Curi, R., and Bevilacqua, E. (2007). Regulation of gene expression in mouse trophoblast cells by interferon-gamma. Placenta 28, 1059–1072.
| Regulation of gene expression in mouse trophoblast cells by interferon-gamma.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVWmsLjF&md5=85a7e8f8c15ad36fa79b4e94af790b92CAS | 17544503PubMed |
Houdijk, E. C., Engelbregt, M. J., Popp-Snijders, C., and Delemarre-Vd Waal, H. A. (2000). Endocrine regulation and extended follow-up of longitudinal growth in intrauterine growth-retarded rats. J. Endocrinol. 166, 599–608.
| Endocrine regulation and extended follow-up of longitudinal growth in intrauterine growth-retarded rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmslylsr4%3D&md5=c7de0b8a68c0ef406701da78b5573575CAS | 10974654PubMed |
Kanayama, N., Tsujimura, R., She, L., Maehara, K., and Terao, T. (1997). Cold-induced stress stimulates the sympathetic nervous system, causing hypertension and proteinuria in rats. J. Hypertens. 15, 383–389.
| Cold-induced stress stimulates the sympathetic nervous system, causing hypertension and proteinuria in rats.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szlsV2kug%3D%3D&md5=d5be2556660011fb0c12f44e27380593CAS | 9211173PubMed |
Ku, D. D., Zaleski, J. K., Liu, S., and Brock, T. A. (1993). Vascular endothelial growth factor induces EDRF-dependent relaxation in coronary arteries. Am. J. Physiol. 265, H586–H592.
| 1:CAS:528:DyaK3sXmtFygsbk%3D&md5=3e91217c9f1f4d3e2ea337208b6a2e34CAS | 8368362PubMed |
Leon, D. A., Lithell, H. O., Vâgerö, D., Koupilová, I., Mohsen, R., Berglund, L., Lithell, U. B., and McKeigue, P. M. (1998). Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915–29. BMJ 317, 241–245.
| Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915–29.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czkt1artA%3D%3D&md5=0160dd808df8f103fffd945612bbe9b3CAS | 9677213PubMed |
Lesage, J., Del-Favero, F., Leonhardt, M., Louvart, H., Maccari, S., Vieau, D., and Darnaudery, M. (2004). Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J. Endocrinol. 181, 291–296.
| Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Crt74%3D&md5=f40c2e4f4363d116039acdc583e65f66CAS | 15128277PubMed |
Li, B., Ogasawara, A. K., Yang, R., Wei, W., He, G. W., Zioncheck, T. F., Bunting, S., de Vos, A. M., and Jin, H. (2002). KDR (VEGF receptor 2) is the major mediator for the hypotensive effect of VEGF. Hypertension 39, 1095–1100.
| KDR (VEGF receptor 2) is the major mediator for the hypotensive effect of VEGF.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFWgt7w%3D&md5=814ff066cecf68857b28f57686f8c63dCAS | 12052848PubMed |
Li, Z., Zhang, Y., Ying Ma, J., Kapoun, A. M., Shao, Q., Kerr, I., Lam, A., O’Young, G., Sannajust, F., Stathis, P., Schreiner, G., Karumanchi, S. A., Protter, A. A., and Pollitt, N. S. (2007). Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia. Hypertension 50, 686–692.
| Recombinant vascular endothelial growth factor 121 attenuates hypertension and improves kidney damage in a rat model of preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCrtL7F&md5=148b268e29b2d4d612c2d672be09a104CAS | 17724276PubMed |
Maharaj, A. S., and D’Amore, P. A. (2007). Roles for VEGF in the adult. Microvasc. Res. 74, 100–113.
| Roles for VEGF in the adult.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ykur7N&md5=eb1c3e49d684dde22a7a242510d62895CAS | 17532010PubMed |
Mairesse, J., Lesage, J., Breton, C., Bréant, B., Hahn, T., Darnaudéry, M., Dickson, S. L., Seckl, J., Blondeau, B., Vieau, D., Maccari, S., and Viltart, O. (2007). Maternal stress alters endocrine function of the feto–placental unit in rats. Am. J. Physiol. Endocrinol. Metab. 292, E1526–E1533.
| Maternal stress alters endocrine function of the feto–placental unit in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvF2mtrw%3D&md5=6ef67b793a5d586b53c89dcfca337941CAS | 17264224PubMed |
Manni, L., Antonelli, A., Costa, N., and Aloe, L. (2005). Stress alters vascular endothelial growth factor expression in rat arteries: role of nerve growth factor. Basic Res. Cardiol. 100, 121–130.
| Stress alters vascular endothelial growth factor expression in rat arteries: role of nerve growth factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVGkur4%3D&md5=fad5f5476eda92e9f56f90947fa003ecCAS | 15739121PubMed |
Maynard, S. E., Min, J. Y., Merchan, J., Lim, K. H., Li, J., Mondal, S., Libermann, T. A., Morgan, J. P., Sellke, F. W., Stillman, I. E., Epstein, F. H., Sukhatme, V. P., and Karumanchi, S. A. (2003). Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111, 649–658.
| 1:CAS:528:DC%2BD3sXhvFentbc%3D&md5=487e0c4f5c7df15e05680f99b7884c2dCAS | 12618519PubMed |
McCance, D. R., Pettitt, D. J., Hanson, R. L., Jacobsson, L. T., Knowler, W. C., and Bennett, P. H. (1994). Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype or surviving small-baby genotype? BMJ 308, 942–945.
| Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype or surviving small-baby genotype?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c3islKitA%3D%3D&md5=e654f08c085f7c4511054ab09f11b96bCAS | 8173400PubMed |
Mondo, C. K., Zhang, Y., de Macedo Possamai, V., Miao, Y., Schyvens, C. G., McKenzie, K. U., Hu, L., Guo, Z., and Whitworth, J. A. (2006). n-acetylcysteine antagonizes the development but does not reverse ACTH-induced hypertension in the rat. Clin. Exp. Hypertens. 28, 73–84.
| n-acetylcysteine antagonizes the development but does not reverse ACTH-induced hypertension in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xhs1aju74%3D&md5=5d7fb1d638ef26bcb7b20938304b63ffCAS | 16546835PubMed |
O’Donnell, K., O’Connor, T. G., and Glover, V. (2009). Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev. Neurosci. 31, 285–292.
| Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsFekurs%3D&md5=76b5005499824409695152ff7ed706edCAS | 19546565PubMed |
Oliveira, A. O., Fileto, C., and Melis, M. S. (2004). Effect of strenuous maternal exercise before and during pregnancy on rat progeny renal function. Braz. J. Med. Biol. Res. 37, 907–911.
| Effect of strenuous maternal exercise before and during pregnancy on rat progeny renal function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czlvVSisA%3D%3D&md5=db92f02a5df6722c39ce5638180031a9CAS | 15264035PubMed |
Osol, G., Celia, G., Gokina, N., Barron, C., Chien, E., Mandala, M., Luksha, L., and Kublickiene, K. (2008). Placental growth factor is a potent vasodilator of rat and human resistance arteries. Am. J. Physiol. Heart Circ. Physiol. 294, H1381–H1387.
| Placental growth factor is a potent vasodilator of rat and human resistance arteries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFymt7g%3D&md5=df46c8bdfcde64ffdc8a1070b1274363CAS | 18192215PubMed |
Ozanne, S. E., and Hales, C. N. (2002). Early programming of glucose–insulin metabolism. Trends Endocrinol. Metab. 13, 368–373.
| Early programming of glucose–insulin metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVSiu70%3D&md5=b87060cbebcc0d663e7e9ef8663e41c5CAS | 12367817PubMed |
Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
| A new mathematical model for relative quantification in real-time RT-PCR.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nis12jtw%3D%3D&md5=54b36b3c1054987092ad32dfe1b8f6acCAS | 11328886PubMed |
Plante, G. E. (2002). Vascular response to stress in health and disease. Metabolism 51, 25–30.
| Vascular response to stress in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlCrtb4%3D&md5=8b390a0a3e4210b6015c723248aae9d7CAS | 12040537PubMed |
Ribatti, D. (2008). The discovery of the placental growth factor and its role in angiogenesis: a historical review. Angiogenesis 11, 215–221.
| The discovery of the placental growth factor and its role in angiogenesis: a historical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVCgur8%3D&md5=2ef467bd2ede4d7c6ed3d297271e46a5CAS | 18568405PubMed |
Roodhart, J. M., Langenberg, M. H., Witteveen, E., and Voest, E. E. (2008). The molecular basis of class side effects due to treatment with inhibitors of the VEGF/VEGFR pathway. Curr. Clin. Pharmacol. 3, 132–143.
| The molecular basis of class side effects due to treatment with inhibitors of the VEGF/VEGFR pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVGntrY%3D&md5=b2be6f0a1a8314b0063976b84f861763CAS | 18690886PubMed |
Seckl, J. R. (2004). Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151, U49–U62.
| Prenatal glucocorticoids and long-term programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFSht7vL&md5=1ab88a52a09cd9246eeec02a96d5419eCAS | 15554887PubMed |
Shibuya, M. (2006). Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis. J. Biochem. Mol. Biol. 39, 469–478.
| Differential roles of vascular endothelial growth factor receptor-1 and receptor-2 in angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFWqsb3M&md5=6cf7acd86285973d78b7064e95f00faaCAS | 17002866PubMed |
Steptoe, A. (2008). Psychophysiological stress reactivity and hypertension. Hypertension 52, 220–221.
| Psychophysiological stress reactivity and hypertension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVymt73L&md5=47c0a53b506a85328c3a12c2fa978c2cCAS | 18574067PubMed |
Takiuti, N. H., Kahhale, S., and Zugaib, M. (2002). Stress in pregnancy: a new Wistar rat model for human preeclampsia. Am. J. Obstet. Gynecol. 186, 544–550.
| Stress in pregnancy: a new Wistar rat model for human preeclampsia.Crossref | GoogleScholarGoogle Scholar | 11904621PubMed |
Tegethoff, M., Greene, N., Olsen, J., Meyer, A. H., and Meinlschmidt, G. (2010). Maternal psychosocial stress during pregnancy and placenta weight: evidence from a national cohort study. PLoS ONE 5, e14478.
| Maternal psychosocial stress during pregnancy and placenta weight: evidence from a national cohort study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXms1Gisg%3D%3D&md5=bbe877bed1e8ee0f8c09b3f4f9079eddCAS | 21217829PubMed |
Teixeira, P. G., Cabral, A. C., Andrade, S. P., Reis, Z. S., da Cruz, L. P., Pereira, J. B., Martins, B. O., and Rezende, C. A. (2008). Placental growth factor (PlGF) is a surrogate marker in preeclamptic hypertension. Hypertens. Pregnancy 27, 65–73.
| Placental growth factor (PlGF) is a surrogate marker in preeclamptic hypertension.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXit1CltLY%3D&md5=fbb6595a77a601fe1d2dd08c29d0a3b7CAS | 18293205PubMed |
Török, J. (2008). Participation of nitric oxide in different models of experimental hypertension. Physiol. Res. 57, 813–825.
| 19154086PubMed |
Tsatsaris, V., Goffin, F., Munaut, C., Brichant, J. F., Pignon, M. R., Noel, A., Schaaps, J. P., Cabrol, D., Frankenne, F., and Foidart, J. M. (2003). Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences. J. Clin. Endocrinol. Metab. 88, 5555–5563.
| Overexpression of the soluble vascular endothelial growth factor receptor in preeclamptic patients: pathophysiological consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptVyntLc%3D&md5=27b3ed3ece3d5a15b3da5052cce3fbf6CAS | 14602804PubMed |
Vieira, J. M., Ruhrberg, C., and Schwarz, Q. (2010). VEGF receptor signalling in vertebrate development. Organogenesis 6, 97–106.
| VEGF receptor signalling in vertebrate development.Crossref | GoogleScholarGoogle Scholar | 20885856PubMed |
Waddell, B. J., Hisheh, S., Dharmarajan, A. M., and Burton, P. J. (2000). Apoptosis in rat placenta is zone-dependent and stimulated by glucocorticoids. Biol. Reprod. 63, 1913–1917.
| Apoptosis in rat placenta is zone-dependent and stimulated by glucocorticoids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVKhtbs%3D&md5=501085ff8dae925cd22960717d162d35CAS | 11090465PubMed |
Wisborg, K., Barklin, A., Hedegaard, M., and Henriksen, T. B. (2008). Psychological stress during pregnancy and stillbirth: prospective study. BJOG 115, 882–885.
| Psychological stress during pregnancy and stillbirth: prospective study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1czitlaqtA%3D%3D&md5=e21b1fae9ff51325d7b06c4f295bf4b8CAS | 18485167PubMed |
Wong, M. L., Dong, C., Esposito, K., Thakur, S., Liu, W., Elashoff, R. M., and Licinio, J. (2008). Elevated stress hemoconcentration in major depression is normalized by antidepressant treatment: secondary analysis from a randomized, double-blind clinical trial and relevance to cardiovascular disease risk. PLoS ONE 3, e2350.
| Elevated stress hemoconcentration in major depression is normalized by antidepressant treatment: secondary analysis from a randomized, double-blind clinical trial and relevance to cardiovascular disease risk.Crossref | GoogleScholarGoogle Scholar | 18985146PubMed |
Yamazaki, Y., Nakano, Y., Imamura, T., and Morita, T. (2007). Augmentation of vascular permeability of VEGF is enhanced by KDR-binding proteins. Biochem. Biophys. Res. Commun. 355, 693–699.
| Augmentation of vascular permeability of VEGF is enhanced by KDR-binding proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVWju7o%3D&md5=13419abc511947cc71f51ae1a0906c66CAS | 17320821PubMed |
Yang, R., Thomas, G. R., Bunting, S., Ko, A., Ferrara, N., Keyt, B., Ross, J., and Jin, H. (1996). Effects of vascular endothelial growth factor on hemodynamics and cardiac performance. J. Cardiovasc. Pharmacol. 27, 838–844.
| Effects of vascular endothelial growth factor on hemodynamics and cardiac performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjsVOit7w%3D&md5=d802c18e04d039bdfc1571cec0e035ccCAS | 8761851PubMed |
Zhou, Y., Bourcy, K., and Kang, Y. J. (2009). Copper-induced regression of cardiomyocyte hypertrophy is associated with enhanced vascular endothelial growth factor receptor-1 signalling pathway. Cardiovasc. Res. 84, 54–63.
| Copper-induced regression of cardiomyocyte hypertrophy is associated with enhanced vascular endothelial growth factor receptor-1 signalling pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFarsbvF&md5=df93bd674882d7cd6d6e3a553ac6a5feCAS | 19542178PubMed |
