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Am J Physiol Regul Integr Comp Physiol 283: R1289-R1292, 2002; doi:10.1152/ajpregu.00562.2002
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Vol. 283, Issue 6, R1289-R1292, December 2002

IN FOCUS
Maternal and fetal adaptations during pregnancy: lessons in regulatory and integrative physiology

Joey P. Granger

Department of Physiology and Biophysics, University of Mississippi, Jackson, Mississippi 39216


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PREGNANCY IS A COMPLEX PHYSIOLOGICAL condition that involves the integration of a variety of regulatory and organ systems. Many aspects of maternal and fetal adaptations during pregnancy have been addressed by recent publications in the American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. Articles include investigations on cardiac, vascular, endothelial (1, 7), renal (17), respiratory, gastrointestinal (39), uteroplacental (12, 36, 38, 48, 55, 56, 63, 68, 71-74), and neuroendocrine changes during pregnancy. Cardiovascular (19) and neurohumoral (41, 49, 66) and metabolic (3, 4, 8, 18) adaptations in the fetus have also been a subject of great interest. Much attention has also been given to the impact of hypoxia, glucocorticoids, and other stressors on the development of the fetus and newborn.

Normal pregnancy is associated with marked hemodynamic alterations within the maternal circulation, including increases in cardiac output and plasma volume and reductions in vascular resistance and arterial pressure. Associated with these changes are marked alterations in the activity of various neurohumoral systems and in vascular and endothelial function. Hines and colleagues (33-35) recently reported that stimulation of volume-sensitive cardiac mechanoreceptors elicits an attenuated reflex effect on blood pressure and renal function. Furthermore, these investigators reported baroreceptor afferent as well as cardiac receptor afferent discharge is reduced during pregnancy (33-35). These investigators postulate these changes in reflex function are an important adaptation that allows plasma volume expansion during pregnancy.

The reduction in arterial pressure in the face of marked increases in cardiac output during pregnancy is due to a considerable decrease in vascular tone. An increase in nitric oxide (NO) during normal pregnancy has been suggested to mediate decreases in vascular resistance by direct actions and by blunting the vascular responsiveness to vasoconstrictors such as angiotensin II and norepinephrine (16, 57). This concept is supported by recent reports that the expression (2) and activity of NO synthases are elevated during normal pregnancy and that the plasma level and urinary excretion of cGMP, a second messenger of NO and a mediator of vascular smooth muscle relaxation, are increased during pregnancy. Moreover, pharmacological blockade or targeted disruption of NO synthases markedly attenuates the reduction in vascular resistance and blood pressure during pregnancy (11, 32). Inhibition of NO synthesis has also been recently shown to modulate the reduction in vascular smooth muscle intracellular calcium concentration (52) and protein kinase C activity (40) that normally occurs during pregnancy. Furthermore, the vascular responsiveness to vasoconstrictors such as angiotensin II is markedly enhanced during pregnancy when NO synthase is inhibited. Finally, recent studies in American Journal of Physiology-Regulatory, Integrative and Comparative Physiology have reported that the vascular actions of NO during pregnancy are attenuated by hyperlipidemia (53) and alcohol intake (15).

The renal circulation is particularly affected during normal pregnancy. Both renal plasma flow and glomerular filtration rate increase to 40-80% above normal in humans and 20-40% in pregnant rats. Mechanisms underlying the marked renal vasodilation during pregnancy have been a subject of intensive investigation. Although numerous factors may be involved in this renal hyperemia, recent studies have implicated NO as an important mediator of the renal hyperfiltration during pregnancy (27, 45). Pregnancy is associated with enhanced renal expression and activation of NO synthase (2). Nonselective and selective inhibition of NO synthase isoforms also attenuate the renal hemodynamic changes during pregnancy (1). Recent studies have suggested that the hormone relaxin is an important factor that mediates the enhanced renal hyperemia and production of NO during pregnancy (17). It also appears that relaxin enhances NO production by an endothelin B receptor-mediated mechanism (17). The interaction between relaxin and the renal endothelin system remains to be an important area of investigation.

The influence of various neurohumoral and metabolic factors on fetal physiology and development of the cardiovascular (7, 46, 60, 64, 69), renal, gastrointestinal (14, 61, 62), neuroendocrine (42), hemopoietic (10, 65), and pulmonary (37, 54) systems has also been an important area of investigation. In particular, much attention has been directed toward studying the impact of various stressors such as hypoxia (5, 13, 28, 30, 43, 44, 70), malnutrition (25, 31, 67), glucocorticoids, infection (23, 29), alcohol, nicotine (26), and other factors (6) on the mother and the fetus. This is a clinically important area of investigation because maternal-fetal stress is a major factor for poor obstetric and infant outcomes, including spontaneous abortion, prematurity, and intrauterine growth restriction as well as susceptibility to cardiovascular and metabolic disease throughout life. Numerous epidemiological studies have reported an association between low birth weight and the risk of hypertension. The inverse relationship between low birth weight and hypertension suggests that factors present in the prenatal environment that affect fetal growth are responsible for the in utero programming of arterial blood pressure control.

A number of studies published in American Journal of Physiology-Regulatory, Integrative and Comparative Physiology have focused on the effect of glucocorticoids and other stressors on fetal development and its impact on blood pressure regulation later in life. Although antenatal glucocorticoid administration is used to improve lung function in human premature newborns, data emerging from humans and animal studies indicate antenatal glucocorticoid administration can significantly affect the cardiovascular, renal, and metabolic alterations essential to postnatal adaptation at birth. Although the mechanisms by which antenatal glucocorticoids impact postnatal circulatory function are unclear, abnormalities in vascular, cardiac, neurohumoral, and autacoid functions appear to be involved (20, 21, 51). Segar et al. (59) recently reported that postnatal increases in arterial pressure and renal sympathetic nerve activity seen with glucocorticoid treatment are not mediated by stimulation of peripherally accessible angiotensin type 1 receptors. They also suggest that augmented cardiovascular function in glucocorticoid-treated premature lambs is dependent, in part, on a generalized sympathetic excitatory response that is mediated by central mechanisms (59). Ervin and colleagues (24) reported that the alterations in postnatal blood pressure regulation in lambs exposed to glucocorticoids preterm occurs despite reductions in plasma cortisol, catecholamines, and circulating levels of angiotensin II. Interestingly, in another study by Brabham et al. (9), it was reported that the environment provided by a healthy mother during postnatal period can prevent the detrimental effects of prenatal glucocorticoid administration on cognitive function. Because of its significant clinical implications, it is quite obvious that more studies are needed to determine the underlying mechanisms whereby antenatal exposure to glucocorticoids and other stressors such as malnutrition and hypoxia affect the physiology of the fetus and the newborn.

Because the renin-angiotensin system has been implicated in the morphogenesis and growth of the kidney throughout fetal development, investigators have also been interested in studying factors that regulate renin secretion in the developing fetus (22, 47, 50). Draper et al. (22) recently examined the role of renal nerves on renal secretion in the mature ovine fetus. They reported that renal nerves are required for the renin secretory mechanisms and responsiveness of renin mRNA to beta -adrenergic stimulation but not for the basal expression of renin in the fetal kidney. In another study by Marsh and colleagues (47), insulin-like growth factor (IGF) was found to chronically enhance plasma renin activity and concentration, implicating IGF as another modulator of renin secretion during fetal development.


    FOOTNOTES

Address for reprint requests and other correspondence: J. P. Granger, Department of Physiology and Biophysics, University of Mississippi Medical Center, 2500 N. State St., Jackson, MS (E-mail: jgranger{at}physiology.umsmed.edu).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

10.1152/ajpregu.00562.2002


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1.   Abram, SR, Alexander BT, Bennett WA, and Granger JP. Role of neuronal nitric oxide synthase in mediating renal hemodynamic changes during pregnancy. Am J Physiol Regul Integr Comp Physiol 281: R1390-R1393, 2001[Abstract/Free Full Text].

2.   Alexander, BT, Reckelhoff JF, Kassab S, and Granger JP. Differential expression of renal nitric oxide synthase isoforms during pregnancy in rats. Hypertension 33: 435-439, 1999[Abstract/Free Full Text].

3.   Anderson, MS, Flowers-Ziegler J, Das UG, Hay WW, Jr, and Devaskar SU. Glucose transporter protein responses to selective hyperglycemia or hyperinsulinemia in fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R1545-R1552, 2001[Abstract/Free Full Text].

4.   Anderson, MS, He J, Flowers-Ziegler J, Devaskar SU, and Hay WW, Jr. Effects of selective hyperglycemia and hyperinsulinemia on glucose transporters in fetal ovine skeletal muscle. Am J Physiol Regul Integr Comp Physiol 281: R1256-R1263, 2001[Abstract/Free Full Text].

5.   Angeles, DM, Williams J, Purdy RE, Zhang L, and Pearce WJ. Effects of maturation and acute hypoxia on receptor-IP(3) coupling in ovine common carotid arteries. Am J Physiol Regul Integr Comp Physiol 280: R410-R417, 2001[Abstract/Free Full Text].

6.   Auman, JT, Seidler FJ, and Slotkin TA. Regulation of fetal cardiac and hepatic beta-adrenoceptors and adenylyl cyclase signaling: terbutaline effects. Am J Physiol Regul Integr Comp Physiol 281: R1079-R1089, 2001[Abstract/Free Full Text].

7.   Barbera, A, Giraud GD, Reller MD, Maylie J, Morton MJ, and Thornburg KL. Right ventricular systolic pressure load alters myocyte maturation in fetal sheep. Am J Physiol Regul Integr Comp Physiol 279: R1157-R1164, 2000[Abstract/Free Full Text].

8.   Bassett, JM, and Hanson C. Prevention of hypoinsulinemia modifies catecholamine effects in fetal sheep. Am J Physiol Regul Integr Comp Physiol 278: R1171-R1181, 2000[Abstract/Free Full Text].

9.   Brabham, T, Phelka A, Zimmer C, Nash A, Lopez JF, and Vazquez DM. Effects of prenatal dexamethasone on spatial learning and response to stress is influenced by maternal factors. Am J Physiol Regul Integr Comp Physiol 279: R1899-R1909, 2000[Abstract/Free Full Text].

10.   Brace, RA, Langendorfer C, Song TB, and Mock DM. Red blood cell life span in the ovine fetus. Am J Physiol Regul Integr Comp Physiol 279: R1196-R1204, 2000[Abstract/Free Full Text].

11.   Brooks, VL, Clow KA, Welch LS, and Giraud GD. Does nitric oxide contribute to the basal vasodilation of pregnancy in conscious rabbits? Am J Physiol Regul Integr Comp Physiol 281: R1624-R1632, 2001[Abstract/Free Full Text].

12.   Brownbill, P, Mahendran D, Owen D, Swanson P, Thornburg KL, Nelson DM, and Sibley CP. Denudations as paracellular routes for alphafetoprotein and creatinine across the human syncytiotrophoblast. Am J Physiol Regul Integr Comp Physiol 278: R677-R683, 2000[Abstract/Free Full Text].

13.   Buchholz, J, and Duckles SP. Chronic hypoxia alters prejunctional alpha 2-receptor function in vascular adrenergic nerves of adult and fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R926-R934, 2001[Abstract/Free Full Text].

14.   Buddington, RK, Elnif J, Puchal-Gardiner AA, and Sangild PT. Intestinal apical amino acid absorption during development of the pig. Am J Physiol Regul Integr Comp Physiol 280: R241-R247, 2001[Abstract/Free Full Text].

15.   Cook, JL, Zhang Y, and Davidge ST. Vascular function in alcohol-treated pregnant and nonpregnant mice. Am J Physiol Regul Integr Comp Physiol 281: R1449-R1455, 2001[Abstract/Free Full Text].

16.   Cox, BE, Williams CE, and Rosenfeld CR. Angiotensin II indirectly vasoconstricts the ovine uterine circulation. Am J Physiol Regul Integr Comp Physiol 278: R337-R344, 2000[Abstract/Free Full Text].

17.   Danielson, LA, Kercher LJ, and Conrad KP. Impact of gender and endothelin on renal vasodilation and hyperfiltration induced by relaxin in conscious rats. Am J Physiol Regul Integr Comp Physiol 279: R1298-R1304, 2000[Abstract/Free Full Text].

18.   Das, UG, He J, Ehrhardt RA, Hay WW, Jr, and Devaskar SU. Time-dependent physiological regulation of ovine placental GLUT-3 glucose transporter protein. Am J Physiol Regul Integr Comp Physiol 279: R2252-R2261, 2000[Abstract/Free Full Text].

19.   Di Maso, NA, Caiozzo VJ, and Baldwin KM. Single-fiber myosin heavy chain polymorphism during postnatal development: modulation by hypothyroidism. Am J Physiol Regul Integr Comp Physiol 278: R1099-R1106, 2000[Abstract/Free Full Text].

20.   Docherty, CC, Kalmar-Nagy J, Engelen M, Koenen SV, Nijland M, Kuc RE, Davenport AP, and Nathanielsz PW. Effect of in vivo fetal infusion of dexamethasone at 0.75 GA on fetal ovine resistance artery responses to ET-1. Am J Physiol Regul Integr Comp Physiol 281: R261-R268, 2001[Abstract/Free Full Text].

21.   Docherty, CC, Kalmar-Nagy J, Engelen M, and Nathanielsz PW. Development of fetal vascular responses to endothelin-1 and acetylcholine in the sheep. Am J Physiol Regul Integr Comp Physiol 280: R554-R562, 2001[Abstract/Free Full Text].

22.   Draper, ML, Wang J, Valego N, Block WA, Jr, and Rose JC. Effect of renal denervation on renin gene expression, concentration, and secretion in mature ovine fetus. Am J Physiol Regul Integr Comp Physiol 279: R263-R270, 2000[Abstract/Free Full Text].

23.   Fang, L, Nowicki B, and Yallampalli C. Differential expression of uterine NO in pregnant and nonpregnant rats with intrauterine bacterial infection. Am J Physiol Regul Integr Comp Physiol 280: R1356-R1363, 2001[Abstract/Free Full Text].

24.   Ervin, MG, Padbury JF, Polk DH, Ikegami M, Berry LM, and Jobe AH. Antenatal glucocorticoids alter premature newborn lamb neuroendocrine and endocrine responses to hypoxia. Am J Physiol Regul Integr Comp Physiol 279: R830-R838, 2000[Abstract/Free Full Text].

25.   Fiorotto, ML, Davis TA, and Reeds PJ. Regulation of myofibrillar protein turnover during maturation in normal and undernourished rat pups. Am J Physiol Regul Integr Comp Physiol 278: R845-R854, 2000[Abstract/Free Full Text].

26.   Frank, MG, Srere H, Ledezma C, O'Hara B, and Heller HC. Prenatal nicotine alters vigilance states and AchR gene expression in the neonatal rat: implications for SIDS. Am J Physiol Regul Integr Comp Physiol 280: R1134-R1140, 2001[Abstract/Free Full Text].

27.   Gandley, RE, Conrad KP, and McLaughlin MK. Endothelin and nitric oxide mediate reduced myogenic reactivity of small renal arteries from pregnant rats. Am J Physiol Regul Integr Comp Physiol 280: R1-R7, 2001[Abstract/Free Full Text].

28.   Giussani, DA, Gardner DS, Cox DT, and Fletcher AJ. Purinergic contribution to circulatory, metabolic, and adrenergic responses to acute hypoxemia in fetal sheep. Am J Physiol Regul Integr Comp Physiol 280: R678-R685, 2001[Abstract/Free Full Text].

29.   Gross, G, Imamura T, Vogt SK, Wozniak DF, Nelson DM, Sadovsky Y, and Muglia LJ. Inhibition of cyclooxygenase-2 prevents inflammation-mediated preterm labor in the mouse. Am J Physiol Regul Integr Comp Physiol 278: R1415-R1423, 2000[Abstract/Free Full Text].

30.   Harris, AP, Helou S, Gleason CA, Traystman RJ, and Koehler RC. Fetal cerebral and peripheral circulatory responses to hypoxia after nitric oxide synthase inhibition. Am J Physiol Regul Integr Comp Physiol 281: R381-R390, 2001[Abstract/Free Full Text].

31.   Hawkins, P, Steyn C, Ozaki T, Saito T, Noakes DE, and Hanson MA. Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes. Am J Physiol Regul Integr Comp Physiol 279: R340-R348, 2000[Abstract/Free Full Text].

32.   Hefler, LA, Tempfer CB, Moreno RM, O'Brien WE, and Gregg AR. Endothelial-derived nitric oxide and angiotensinogen: blood pressure and metabolism during mouse pregnancy. Am J Physiol Regul Integr Comp Physiol 280: R174-R182, 2001[Abstract/Free Full Text].

33.   Hines, T. Baroreceptor afferent discharge in the pregnant rat. Am J Physiol Regul Integr Comp Physiol 278: R1433-R1440, 2000[Abstract/Free Full Text].

34.   Hines, T, and Herzer WA. Effect of cardiac receptor stimulation on renal vascular resistance in the pregnant rat. Am J Physiol Regul Integr Comp Physiol 278: R171-R178, 2000[Abstract/Free Full Text].

35.   Hines, T, and Hodgson TM. Pregnancy alters cardiac receptor afferent discharge in rats. Am J Physiol Regul Integr Comp Physiol 278: R149-R156, 2000[Abstract/Free Full Text].

36.   Imamura, T, Luedke CE, Vogt SK, and Muglia LJ. Oxytocin modulates the onset of murine parturition by competing ovarian and uterine effects. Am J Physiol Regul Integr Comp Physiol 279: R1061-R1067, 2000[Abstract/Free Full Text].

37.   Jaillard, S, Houfflin-Debarge V, Riou Y, Rakza T, Klosowski S, Lequien P, and Storme L. Effects of catecholamines on the pulmonary circulation in the ovine fetus. Am J Physiol Regul Integr Comp Physiol 281: R607-R614, 2001[Abstract/Free Full Text].

38.   Johansson, M, Jansson T, and Powell TL. Na+-K+-ATPase is distributed to microvillous and basal membrane of the syncytiotrophoblast in human placenta. Am J Physiol Regul Integr Comp Physiol 279: R287-R294, 2000[Abstract/Free Full Text].

39.   Petersen, YM, Burrin DG, and Sangild PT. GLP-2 has differential effects on small intestine growth and function in fetal and neonatal pigs. Am J Physiol Regul Integr Comp Physiol 281: R1986-R1993, 2001[Abstract/Free Full Text].

40.   Kanashiro, CA, Cockrell KL, Alexander BT, Granger JP, and Khalil RA. Pregnancy-associated reduction in vascular protein kinase C activity rebounds during inhibition of NO synthesis. Am J Physiol Regul Integr Comp Physiol 278: R295-R303, 2000[Abstract/Free Full Text].

41.   Keller-Wood, M, and Wood CE. Pregnancy alters cortisol feedback inhibition of stimulated ACTH: studies in adrenalectomized ewes. Am J Physiol Regul Integr Comp Physiol 280: R1790-R1798, 2001[Abstract/Free Full Text].

42.   Koos, BJ, Chau A, Matsuura M, Punla O, and Kruger L. Thalamic lesions dissociate breathing inhibition by hypoxia and adenosine in fetal sheep. Am J Physiol Regul Integr Comp Physiol 278: R831-R837, 2000[Abstract/Free Full Text].

43.   Lane, RH, Kelley DE, Gruetzmacher EM, and Devaskar SU. Uteroplacental insufficiency alters hepatic fatty acid-metabolizing enzymes in juvenile and adult rats. Am J Physiol Regul Integr Comp Physiol 280: R183-R190, 2001[Abstract/Free Full Text].

44.   Lang, U, Baker RS, Khoury J, and Clark KE. Effects of chronic reduction in uterine blood flow on fetal and placental growth in the sheep. Am J Physiol Regul Integr Comp Physiol 279: R53-R59, 2000[Abstract/Free Full Text].

45.   Lo, F, and Kaufman S. Effect of 5alpha -pregnan-3alpha -ol-20-one on nitric oxide biosynthesis and plasma volume in rats. Am J Physiol Regul Integr Comp Physiol 280: R1902-R1905, 2001[Abstract/Free Full Text].

46.   Long, W, Zhang L, and Longo LD. Cerebral artery sarcoplasmic reticulum Ca2+ stores and contractility: changes with development. Am J Physiol Regul Integr Comp Physiol 279: R860-R873, 2000[Abstract/Free Full Text].

47.   Marsh, AC, Gibson KJ, Wu J, Owens PC, Owens JA, and Lumbers ER. Chronic effect of insulin-like growth factor I on renin synthesis, secretion, and renal function in fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R318-R326, 2001[Abstract/Free Full Text].

48.   Melendez, JA, Vinci JM, Jeffrey JJ, and Wilcox BD. Localization and regulation of IL-1alpha in rat myometrium during late pregnancy and the postpartum period. Am J Physiol Regul Integr Comp Physiol 280: R879-R888, 2001[Abstract/Free Full Text].

49.   Mollanji, R, Papaiconomou C, Boulton M, Midha R, and Johnston M. Comparison of cerebrospinal fluid transport in fetal and adult sheep. Am J Physiol Regul Integr Comp Physiol 281: R1215-R1223, 2001[Abstract/Free Full Text].

50.   Moritz, K, Koukoulas I, Albiston A, and Wintour EM. Angiotensin II infusion to the midgestation ovine fetus: effects on the fetal kidney. Am J Physiol Regul Integr Comp Physiol 279: R1290-R1297, 2000[Abstract/Free Full Text].

51.   Moss, TJ, Sloboda DM, Gurrin LC, Harding R, Challis JR, and Newnham JP. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol 281: R960-R970, 2001[Abstract/Free Full Text].

52.   Murphy, JG, Fleming JB, Cockrell KL, Granger JP, and Khalil RA. [Ca2+]i signaling in renal arterial smooth muscle cells of pregnant rat is enhanced during inhibition of NOS. Am J Physiol Regul Integr Comp Physiol 280: R87-R99, 2001[Abstract/Free Full Text].

53.   Ramirez, RJ, Novak J, Johnston TP, Gandley RE, McLaughlin MK, and Hubel CA. Endothelial function and myogenic reactivity in small mesenteric arteries of hyperlipidemic pregnant rats. Am J Physiol Regul Integr Comp Physiol 281: R1330-R1337, 2001[Abstract/Free Full Text].

54.   Renolleau, S, Dauger S, Autret F, Vardon G, Gaultier C, and Gallego J. Maturation of baseline breathing and of hypercapnic and hypoxic ventilatory responses in newborn mice. Am J Physiol Regul Integr Comp Physiol 281: R1746-R1753, 2001[Abstract/Free Full Text].

55.   Reznikov, LL, Shames BD, Barton HA, Selzman CH, Fantuzzi G, Kim SH, Johnson SM, and Dinarello CA. Interleukin-1beta deficiency results in reduced NF-kappa B levels in pregnant mice. Am J Physiol Regul Integr Comp Physiol 278: R263-R270, 2000[Abstract/Free Full Text].

56.   Rosen, O, Suarez C, Schuster VL, and Brion LP. Expression of carbonic anhydrase IV in mouse placenta. Am J Physiol Regul Integr Comp Physiol 280: R365-R375, 2001[Abstract/Free Full Text].

57.   Rosenfeld, CR. Mechanisms regulating angiotensin II responsiveness by the uteroplacental circulation. Am J Physiol Regul Integr Comp Physiol 281: R1025-R1040, 2001[Abstract/Free Full Text].

58.   Sarkar, S, Tsai SW, Nguyen TT, Plevyak M, Padbury JF, and Rubin LP. Inhibition of placental 11beta -hydroxysteroid dehydrogenase type 2 by catecholamines via alpha -adrenergic signaling. Am J Physiol Regul Integr Comp Physiol 281: R1966-R1974, 2001[Abstract/Free Full Text].

59.   Segar, JL, Bedell KA, and Smith OJ. Glucocorticoid modulation of cardiovascular and autonomic function in preterm lambs: role of ANG II. Am J Physiol Regul Integr Comp Physiol 280: R646-R654, 2001[Abstract/Free Full Text].

60.   Segar, JL, Dalshaug GB, Bedell KA, Smith OM, and Scholz TD. Angiotensin II in cardiac pressure-overload hypertrophy in fetal sheep. Am J Physiol Regul Integr Comp Physiol 281: R2037-R2047, 2001[Abstract/Free Full Text].

61.   Shah, S, Hobbs A, Singh R, Cuevas J, Ignarro LJ, and Chaudhuri G. Gastrointestinal motility during pregnancy: role of nitrergic component of NANC nerves. Am J Physiol Regul Integr Comp Physiol 279: R1478-R1485, 2000[Abstract/Free Full Text].

62.   Shah, S, Nathan L, Singh R, Fu YS, and Chaudhuri G. E2 and not P4 increases NO release from NANC nerves of the gastrointestinal tract: implications in pregnancy. Am J Physiol Regul Integr Comp Physiol 280: R1546-R1554, 2001[Abstract/Free Full Text].

63.   Siman, CM, Sibley CP, Jones CJ, Turner MA, and Greenwood SL. The functional regeneration of syncytiotrophoblast in cultured explants of term placenta. Am J Physiol Regul Integr Comp Physiol 280: R1116-R1122, 2001[Abstract/Free Full Text].

64.   Smolich, JJ. NO supports right ventricular flow dominance and whole body O2 utilization in midgestation fetal lambs. Am J Physiol Regul Integr Comp Physiol 280: R1016-R1022, 2001[Abstract/Free Full Text].

65.   Sohl, BD, Cheung CY, Widness JA, and Brace RA. Erythropoietin responses to progressive blood loss over 10 days in the ovine fetus. Am J Physiol Regul Integr Comp Physiol 281: R1051-R1058, 2001[Abstract/Free Full Text].

66.   Speth, RC, Smith MS, and Grove KL. Lactation decreases angiotensinogen mRNA expression in the midcaudal arcuate nucleus of the rat brain. Am J Physiol Regul Integr Comp Physiol 280: R1169-R1176, 2001[Abstract/Free Full Text].

67.   Steiger Burgos, M, Senn M, Sutter F, Kreuzer M, and Langhans W. Effect of water restriction on feeding and metabolism in dairy cows. Am J Physiol Regul Integr Comp Physiol 280: R418-R427, 2001[Abstract/Free Full Text].

68.   St-Pierre, MV, Serrano MA, Macias RI, Dubs U, Hoechli M, Lauper U, Meier PJ, and Marin JJ. Expression of members of the multidrug resistance protein family in human term placenta. Am J Physiol Regul Integr Comp Physiol 279: R1495-R1503, 2000[Abstract/Free Full Text].

69.   Takahashi, Y, Roman C, Chemtob S, Tse MM, Lin E, Heymann MA, and Clyman RI. Cyclooxygenase-2 inhibitors constrict the fetal lamb ductus arteriosus both in vitro and in vivo. Am J Physiol Regul Integr Comp Physiol 278: R1496-R1505, 2000[Abstract/Free Full Text].

70.   Thompson, LP, Aguan K, Pinkas G, and Weiner CP. Chronic hypoxia increases the NO contribution of acetylcholine vasodilation of the fetal guinea pig heart. Am J Physiol Regul Integr Comp Physiol 279: R1813-R1820, 2000[Abstract/Free Full Text].

71.   Thureen, PJ, Anderson SM, and Hay WW, Jr. Regulation of uterine and umbilical amino acid uptakes by maternal amino acid concentrations. Am J Physiol Regul Integr Comp Physiol 279: R849-R859, 2000[Abstract/Free Full Text].

72.   Umur, A, Van Gemert MJ, and Ross MG. Amniotic fluid and hemodynamic model in monochorionic twin pregnancies and twin-twin transfusion syndrome. Am J Physiol Regul Integr Comp Physiol 280: R1499-R1509, 2001[Abstract/Free Full Text].

73.   Wlodek, ME, Westcott KT, Ho PW, Serruto A, Di Nicolantonio R, Farrugia W, and Moseley JM. Reduced fetal, placental, and amniotic fluid PTHrP in the growth-restricted spontaneously hypertensive rat. Am J Physiol Regul Integr Comp Physiol 279: R31-R38, 2000[Abstract/Free Full Text].

74.   Wu, WX, Ma XH, Smith GC, Mecenas CA, Koenen SV, and Nathanielsz PW. Prostaglandin dehydrogenase mRNA in baboon intrauterine tissues in late gestation and spontaneous labor. Am J Physiol Regul Integr Comp Physiol 279: R1082-R1090, 2000[Abstract/Free Full Text].


Am J Physiol Regul Integr Comp Physiol 283(6):R1289-R1292
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