Pregnancy-associated homeostasis and dysregulation: Lessons from genetically modified animal models

Journal of Biochemistry

Volumn 150, Issue 1, 2011, Pages 5-14

  Ishida, Junji ^a   Matsuoka, Toshiki ^a   Saito Fujita, Tomoko ^a   Inaba, Saki ^a   Kunita, Satoshi ^a   Sugiyama, Fumihiro ^a   Yagami, Ken Ichi ^a   Fukamizu, Akiyoshi ^a  

^a UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Genetically modified animal models; placenta; pre eclampsia; pregnancy associated homeostasis; renin angiotensin system

Indexed keywords

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; CONTROLLED STUDY; FEMALE; FETOPLACENTAL UNIT; GENE EXPRESSION REGULATION; HOMEOSTASIS AND REGULATION; MOUSE; NONHUMAN; PLACENTA FUNCTION; PREECLAMPSIA; PREGNANCY; PREGNANCY DISORDER; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOMEOSTASIS; HUMANS; MICE; PLACENTA; PRE-ECLAMPSIA; PREGNANCY; RENIN-ANGIOTENSIN SYSTEM;

ANIMALIA;

EID: 79960086044     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvr069     Document Type: Review

References (66)

1. WHO, UNICEF, UNFPA, and World Bank. (2007) Maternal mortality in 2005: estimates developed by WHO, UNICEF, UNFPA and the World Bank. Geneva: WHO.
2. Weinstein, L. (1982) Syndrome of hemolysis, elevated liver enzymes, and low platelet count: a severe consequence of hypertension in pregnancy. Am. J. Obstet. Gynecol. 142, 159-167 (Pubitemid 12222094)
3. Sibai, B.M., Ramadan, M.K., Usta, I., Salama, M., Mercer, B.M., and Friedman, S.A. (1993) Maternal morbidity and mortality in 442 pregnancies with hemolysis, elevated liver enzymes and low platelets (HELLP syndrome). Am. J. Obstet. Gynecol. 169, 1000-1006 (Pubitemid 23317544)
4. Gracia, P.V. (2009) Maternal deaths due to eclampsia and HELLP syndrome. Int. J. Gynecol. Obstet. 104, 90-94
5. Pritchard, J.A. (1965) Changes in the blood volume during pregnancy and delivery. Anesthesiology 26, 393-399
6. Whittaker, P.G., Macphail, S., and Lind, T. (1996) Serial hematologic changes and pregnancy outcome. Obstet. Gynecol. 88, 33-39 (Pubitemid 26197273)
7. Phelps, R.L., Metzger, B.E., and Freinkel, N. (1981) Carbohydrate metabolism in pregnancy, XVII. Diurnal profiles of plasma glucose, insulin, free fatty acids, triglycerides, cholesterol, and individual amino acids in late normal pregnancy. Am. J. Obstet. Gynecol. 140, 730-736 (Pubitemid 11046636)
8. Butte, N.F. (2000) Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus. Am. J. Clin. Nutr. 7, 1256S-1261S (Pubitemid 30230526)
9. Freinkel, N. (1980) Banting lecture 1980: of pregnancy and progeny. Diabetes 29, 1023-1035
10. Guleria, I. and Pollard, J.W. (2000) The trophoblast is a component of the innate immune system during pregnancy. Nat. Med. 6, 589-593 (Pubitemid 30305912)
11. Khan, S., Khan, S., Katabuchi, H., Araki, M., Nishimura, R., and Okamura, H. (2000) Human villous macrophage-conditioned media enhance human trophoblast growth and differentiation in vitro. Biol. Reprod. 62, 1075-1083 (Pubitemid 30173824)
12. Robertson, S.A., Roberts, C.T., Farr, K.L., Dunn, A.R., and Seamark, R.F. (1999) Fertility impairment in granulocyte-macrophage colony-stimulating factordeficient mice. Biol. Reprod. 60, 251-261 (Pubitemid 29063863)
13. Cianfarani, F., Tommasi, R., Failla, C.M., Viviano, M.T., Annessi, G., Papi, M., Zambruno, G., and Odorisio, T. (2006) Granulocyte/macrophage colonystimulating factor treatment of human chronic ulcers promotes angiogenesis associated with de novo vascular endothelial growth factor transcription in the ulcer bed. Br. J. Dermatol. 154, 34-41 (Pubitemid 43381317)
14. Cope, I. (1961) Plasma and blood volume changes in pregnancies complicated by pre-eclampsia. J. Obstet. Gynaecol. Br. Commonw. 68, 413-416
15. MacGillivray, I., Rose, G.A., and Rowe, B. (1969) Blood pressure survey in pregnancy. Clin. Sci. 37, 395-407
16. Visser, W. and Wallenburg, H.C. (1995) Maternal and perinatal outcome of temporizing management in 254 consecutive patients with severe pre-eclampsia remote from term. Eur. J. Obstet. Gynecol. Reprod. Biol. 63, 147-154 (Pubitemid 26008826)
17. Redman, C.W. (1984) Maternal plasma volume and disorders of pregnancy. Br. Med. J. (Clin Res Ed) 288, 955-956 (Pubitemid 14115346)
18. Gant, N.F., Daley, G.L., Chand, S., Whalley, P.J., and MacDonald, P.C. (1973) A study of angiotensin II pressor response throughout primigravid pregnancy. J. Clin. Invest. 52, 2682-2689
19. Cross, J.C., Werb, Z., and Fisher, S.J. (1994) Implantation and the placenta: key pieces of the development puzzle. Science 266, 1508-1518
20. Zhou, Y., Fisher, S.J., Janatpour, M., Genbacev, O., Dejana, E., Wheelock, M., and Damsky, C.H. (1997) Human cytotrophoblasts adopt a vascular phenotype as they differentiate. A strategy for successful endovascular invasion? J. Clin. Invest. 99, 2139-2151 (Pubitemid 27203770)
21. Meekins, J.W., Pijnenborg, R., Hanssens, M., McFadyen, I.R., and van Asshe, A. (1994) A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br. J. Obstet. Gynaecol. 101, 669-674 (Pubitemid 24251519)
22. Lunell, N.O., Nylund, L.E., Lewander, R., and Sarby, B. (1982) Uteroplacental blood flow in preeclampsia measurements with indium-113m and a computer-linked gamma camera. Clin. Exp. Hypertens. B 1, 105-117 (Pubitemid 12066050)
23. Genbacev, O., Joslin, R., Damsky, C.H., Polliotti, B.M., and Fisher, S.J. (1996) Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J. Clin. Invest. 97, 540-550 (Pubitemid 26039422)
24. Roberts, J.M. and Lain, K.Y. (2002) Recent insights into the pathogenesis of preeclampsia. Placenta 23, 359-372
25. Redline, R.W. and Patterson, P. (1995) Pre-eclampsia is associated with an excess of proliferative immature intermediate trophoblast. Hum. Pathol. 26, 594-600
26. Reynolds, L.P. and Redmer, D.A. (2001) Angiogenesis in the placenta. Biol. Reprod. 64, 1033-1040 (Pubitemid 32239172)
27. Zygmunt, M., Herr, F., Münstedt, K., Lang, U., and Liang, O.D. (2003) Angiogenesis and vasculogenesis in pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol. 22, S10-18 (Pubitemid 37074857)
28. Kendall, R.L. and Thomas, K.A. (1993) Inhibition of vascular endothelial cell growth factor activity by an endogenously encoded soluble receptor. Proc. Natl Acad. Sci. USA 90, 10705-10709
29. Stepan, H., Faber, R., Dornhöfer, N., Huppertz, B., Robitzki, A., and Walther, T. (2006) New insights into the biology of preeclampsia. Biol. Reprod. 74, 772-776
30. 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 (Pubitemid 36278583)
31. Cudmore, M., Ahmad, S., Al-Ani, B., Fujisawa, T., Coxall, H., Chudasama, K., Devey, L.R., Wigmore, S.J., Abbas, A., Hewett, P.W., and Ahmed, A. (2007) Negative regulation of soluble Flt-1 and soluble endoglin release by heme oxygenase-1. Circulation 115, 1789-1797
32. Venkatesha, S., Toporsian, M., Lam, C., Hanai, J., Mammoto, T., Kim, Y.M., Bdolah, Y., Lim, K.H., Yuan, H.T., Libermann, T.A., Stillman, I.E., Roberts, D., DAmore, P.A., Epstein, F.H., Sellke, F.W., Romero, R., Sukhatme, V.P., Letarte, M., and Karumanchi, S.A. (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 12, 642-649 (Pubitemid 43865232)
33. Jerkic, M., Rivas-Elena, J.V., Prieto, M., Carrón, R., Sanz-Rodríguez, F., Pérez-Barriocanal, F., Rodríguez- Barbero, A., Bernabéu, C., and López- Novoa, J.M. (2004) Endoglin regulates nitric oxidedependent vasodilatation. FASEB J. 18, 609-611
34. Santibanez, J.F., Letamendia, A., Perez-Barriocanal, F., Silvestri, C., Saura, M., Vary, C.P., Lopez-Novoa, J.M., Attisano, L., and Bernabeu, C. (2007) Endoglin increases eNOS expression by modulating Smad2 protein levels and Smad2-dependent TGF-b signaling. J. Cell. Physiol. 210, 456-468 (Pubitemid 44956891)
35. Berg, D., Sonsalla, R., and Kuss, E. (1983) Concentrations of 2-methoxyoestrogens in human serum measured by a heterologous immunoassay with an 125I-labelled ligand. Acta Endocrinol. 103, 282-288.
36. Redman, C.W. and Sargent, I.L. (2005) Latest advances in understanding preeclampsia. Science 308, 1592-1594
37. Davisson, R.L., Hoffmann, D.S., Butz, G.M., Aldape, G., Schlager, G., Merrill, D.C., Sethi, S., Weiss, R.M., and Bates, J.N. (2002) Discovery of a spontaneous genetic mouse model of preeclampsia. Hypertension 39, 337-342
38. Hoffmann, D.S., Weydert, C.J., Lazartigues, E., Kutschke, W.J., Kienzle, M.F., Leach, J.E., Sharma, J.A., Sharma, R.V., and Davisson, R.L. (2008) Chronic tempol prevents hypertension, proteinuria and poor feto-placental outcomes in BPH/5 mouse model of preeclampsia. Hypertension 51, 1058-1065
39. Sharkey, L.C., McCune, S.A., Yuan, O., Lange, C., and Fray, J. (2001) Spontaneous pregnancy-induced hypertension and intrauterine growth restriction in rats. Am. J. Hypertens. 14, 1058-1066 (Pubitemid 32978080)
40. Kanayama, N., Takahashi, K., Matsuura, T., Sugimura, M., Kobayashi, T., Moniwa, N., Tomita, M., and Nakayama, K. (2002) Deficiency in p57Kip2 expression induces preeclampsia-like symptoms in mice. Mol. Hum. Reprod. 8, 1129-1135 (Pubitemid 36032852)
41. Hefler, L.A., Tempfer, C.B., Moreno, R.M., OBrien, W.E., and Gregg, A.R. (2001) Endothelial-derived nitric oxide and angiotensinogen: blood pressure and metabolism during mouse pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R174-R182
42. Chan, J.C., Knudson, O., Wu, F., Morser, J., Dole, W.P., and Wu, Q. (2005) Hypertension in mice lacking the pro-atrial natriuretic peptide convertase corin. Proc. Natl Acad. Sci. USA. 102, 785-790 (Pubitemid 40282743)
43. Kanasaki, K., Palmsten, K., Sugimoto, H., Ahmad, S., Hamano, Y., Xie, L., Parry, S., Augustin, H.G., Gattone, V.H., Folkman, J., Strauss, J.F., and Kalluri, R. (2008) Deficiency in catechol-O-methyltransferase and 2-methoxyoestradiol is associated with pre-eclampsia. Nature 453, 1117-11121
44. August, P., Lenz, T., Ales, K. L., Druzin, M. L., Edersheim, T. G., Hutson, J. M., Muller, F. B., Laragh, J. H., and Sealey, J. E. (1990) Longitudinal study of the renin-angiotensin-aldosterone system in hypertensive pregnant women: deviations related to the development of superimposed preeclampsia. Am. J. Obstet. Gynecol. 163, 1612-1621
45. Brown, M. A., Nicholson, E., and Gallery, E. D. (1988) Sodium-renin-aldosterone relations in normal and hypertensive pregnancy. Br. J. Obstet. Gynaecol. 95, 1237-1246 (Pubitemid 19032903)
46. Oparil, S. and Haber, E. (1974) The renin-angiotensin system (first of two parts). N. Engl. J. Med. 291, 389-401
47. Crowley, S.D., Tharaux, P.L., Audoly, L.P., and Coffman, T.M. (2004) Exploring type I angiotensin (AT1) receptor functions through gene targeting. Acta Physiol. Scand. 181, 561-570 (Pubitemid 39078855)
48. Kim, S. and Iwao, H. (2000) Molecular and cellular mechanisms of angiotensin II-mediated cardiovascular and renal diseases. Pharmacol. Rev. 52, 11-34 (Pubitemid 30127593)
49. Brown, M.A., Wang, J., and Whitworth, J.A. (1997) The renin-angiotensin-aldosterone system in pre-eclampsia. Clin. Exp. Hypertens. 19, 713-726 (Pubitemid 27321699)
50. Baker, P.N., Pipkin, F.B., and Symonds, E.M. (1990) Platelet angiotensin II binding and plasma renin concentration, plasma renin substrate and plasma angiotensin II in human pregnancy. Clin. Sci. 79, 403-408 (Pubitemid 20331479)
51. Chesley, L.C., Talledo, E., Bohler, C.S., and Zuspan, F.P. (1965) Vascular reactivity to angiotensin II and norepinephrine in pregnant and nonpregnant women. Am. J. Obstetr. Gynecol. 91, 837-842
52. Baker, P.N., Pipkin, F.B., and Symonds, E.M. (1992) Comparative study of platelet angiotensin II binding and the angiotensin II sensitivity test as predictors of pregnancy-induced hypertension. Clin. Sci. 83, 89-95
53. Takimoto, E., Ishida, J., Sugiyama, F., Horiguchi, H., Murakami, K., and Fukamizu, A. (1996) Hypertension induced in pregnant mice by placental renin and maternal angiotensinogen. Science 274, 995-998
54. Saito, T., Ishida, J., Takimoto-Ohnishi, E., Takamine, S., Shimizu, T., Sugaya, T., Kato, H., Matsuoka, T., Nangaku, M., Kon, Y., Sugiyama, F., Yagami, K., and Fukamizu, A. (2004) An essential role for angiotensin II type 1a receptor in pregnancy-associated hypertension with intrauterine growth retardation. FASEB J. 18, 388-390
55. Takimoto-Ohnishi, E., Saito, T., Ishida, J., Ohnishi, J., Sugiyama, F., Yagami, K., and Fukamizu, A. (2005) Differential roles of renin and angiotensinogen in the feto-maternal interface to the development of complications of pregnancy. Mol. Endocrinol. 19, 1361-1372 (Pubitemid 40594130)
56. Furuya, M., Ishida, J., Inaba, S., Kasuya, Y., Kimura, S., Nemori, R., and Fukamizu, A. (2008) Impaired placental neovascularization in mice with pregnancy-associated hypertension. Lab. Invest. 88, 416-429 (Pubitemid 351432779)
57. Leung, P. S., Tsai, S. J., Wallukat, G., Leung, T. N., and Lau, T. K. (2001) The upregulation of angiotensin II receptor AT1 in human preeclamptic placenta. Mol. Cell. Endocrinol. 184, 95-102 (Pubitemid 32994800)
58. Doering, T. P., Haller, N. A., Montgomery, M. A., Freeman, E. J., and Hopkins, M. P. (1998) The role of AT1 angiotensin receptor activation in the pathogenesis of preeclampsia. Am. J. Obstet. Gynecol. 178, 1307-1312 (Pubitemid 28304635)
59. Nalogowska-Glosnicka, K., Lacka, B. I., Zychma, M. J., Grzeszczak, W., Zukowska-Szczechowska, E., Poreba, R., Michalski, B., Kniazewski, B., and Rzempoluch, J. (2000) Angiotensin II type 1 receptor gene A1166C polymorphism is associated with the increased risk of pregnancy-induced hypertension. Med. Sci. Monit. 6, 523-529 (Pubitemid 30432139)
60. AbdAlla, S., Lother, H., el Massiery, A., and Quitterer, U. (2001) Increased AT1 receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat. Med. 7, 1003-1009 (Pubitemid 32937379)
61. Wallukat, G., Homuth, V., Fischer, T., Lindschau, C., Horstkamp, B., Jupner, A., Baur, E., Nissen, E., Vetter, K., Neichel, D. et al. (1999) Patients with preeclampsia develop agonistic autoantibodies against the angiotensin AT1 receptor. J. Clin. Invest. 103, 945-952 (Pubitemid 29169601)
62. Zhou, C.C., Zhang, Y., Irani, R.A., Zhang, H., Mi, T., Popek, E.J., Hicks, M.J., Ramin, S.M., Kellems, R.E., and Xia, Y. (2008) Angiotensin receptor agonistic autoantibodies induce pre-eclampsia in pregnant mice. Nat. Med. 14, 855-862
63. Kumasawa, K., Ikawa, M., Kidoya, H., Hasuwa, H., Saito-Fujita, T., Morioka, Y., Takakura, N., Kimura, T., and Okabe, M. (2011) Pravastatin induces placental growth factor (PGF) and ameliorates preeclampsia in a mouse model. Proc. Natl Acad. Sci. USA. 108, 1451-1455
64. Zhou, C.C., Ahmad, S., Mi, T., Xia, L., Abbasi, S., Hewett, P.W., Sun, C., Ahmed, A., Kellems, R.E., and Xia, Y. (2007) Angiotensin II induces soluble fms-like tyrosine kinase-1 release via calcineurin signaling pathway in pregnancy. Circ. Res. 100, 88-95 (Pubitemid 46074969)
65. Zhou, C.C., Ahmad, S., Mi, T., Abbasi, S., Xia, L., Day, M.C., Ramin, S.M., Ahmed, A., Kellems, R.E., and Xia, Y. (2008) Autoantibody from women with preeclampsia induces soluble Fms-like tyrosine kinase-1 production via angiotensin type 1 receptor and calcineurin/nuclear factor of activated T-cells signaling. Hypertension 51, 1010-1019
66. Zhou, A., Carrell, R.W., Murphy, M.P., Wei, Z., Yan, Y., Stanley, P.L., Stein, P.E., Broughton, P.F., and Read, R.J. (2010) A redox switch in angiotensinogen modulates angiotensin release. Nature 468, 108-111