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Impact of in vitro embryo culture and transfer on blood pressure regulation in the adolescent lamb

Published online by Cambridge University Press:  13 November 2020

Monalisa Padhee ,
I. Caroline McMillen ,
Song Zhang ,
Severence M. MacLaughlin ,
James A. Armitage ,
Geoffrey A. Head ,
Jack R. T. Darby Open the ORCID record for Jack R. T. Darby [Opens in a new window] ,
Jennifer M. Kelly ,
Skye R. Rudiger  and
David O. Kleemann
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Monalisa Padhee
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
I. Caroline McMillen
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
Song Zhang
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
Severence M. MacLaughlin
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
James A. Armitage
Affiliation:
School of Medicine (Optometry), Deakin University, Waurn Ponds, Victoria, Australia
Geoffrey A. Head
Affiliation:
Neuropharmacology Lab, Baker IDI Heart and Diabetes Institute, Melbourne, Victoria, Australia
Jack R. T. Darby
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
Jennifer M. Kelly
Affiliation:
South Australian Research and Development Institute, Turretfield, South Australia, Australia
Skye R. Rudiger
Affiliation:
South Australian Research and Development Institute, Turretfield, South Australia, Australia
David O. Kleemann
Affiliation:
South Australian Research and Development Institute, Turretfield, South Australia, Australia
Simon K. Walker
Affiliation:
South Australian Research and Development Institute, Turretfield, South Australia, Australia
Janna L. Morrison*
Affiliation:
Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia
*
Address for correspondence: Janna L. Morrison, Australian Research Council Future Fellow (Level 3), Early Origins of Adult Health Research Group, Health and Biomedical Innovation, UniSA: Clinical and Health Sciences, University of South Australia, GPO Box 2471, Adelaide, South Australia 5001, Australia. Email: Janna. [email protected]
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Abstract

Nutrition during the periconceptional period influences postnatal cardiovascular health. We determined whether in vitro embryo culture and transfer, which are manipulations of the nutritional environment during the periconceptional period, dysregulate postnatal blood pressure and blood pressure regulatory mechanisms. Embryos were either transferred to an intermediate recipient ewe (ET) or cultured in vitro in the absence (IVC) or presence of human serum (IVCHS) and a methyl donor (IVCHS+M) for 6 days. Basal blood pressure was recorded at 19–20 weeks after birth. Mean arterial pressure (MAP) and heart rate (HR) were measured before and after varying doses of phenylephrine (PE). mRNA expression of signaling molecules involved in blood pressure regulation was measured in the renal artery. Basal MAP did not differ between groups. Baroreflex sensitivity, set point, and upper plateau were also maintained in all groups after PE stimulation. Adrenergic receptors alpha-1A (αAR1A), alpha-1B (αAR1B), and angiotensin II receptor type 1 (AT1R) mRNA expression were not different from controls in the renal artery. These results suggest there is no programmed effect of ET or IVC on basal blood pressure or the baroreflex control mechanisms in adolescence, but future studies are required to determine the impact of ET and IVC on these mechanisms later in the life course when developmental programming effects may be unmasked by age.

Keywords

In vitro embryo cultureembryo transferartificial reproductive technologiesbaroreflexhypertensioncardiacDOHaD
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 5 , October 2021 , pp. 731 - 737
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Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Kannel, WB. Blood pressure as a cardiovascular risk factor: prevention and treatment. JAMA. 1996; 275, 1571–1576.CrossRefGoogle ScholarPubMed
Nicholls, MG. Hypertension, hypertrophy, heart failure. Heart. 1996; 76, 92.CrossRefGoogle Scholar
Iqbal, R, Ahmad, Z, Malik, F, et al. A statistical analysis of hypertension as cardiovascular risk factor. Middle-East J Sci Res. 2012; 12, 19–22.Google Scholar
Kougias, P, Weakley, SM, Yao, Q, Lin, PH, Chen, C. Arterial baroreceptors in the management of systemic hypertension. Med Sci Monit. 2010; 16, RA1–RA8.Google ScholarPubMed
Dampney, RAL, Coleman, MJ, Fontes, MAP, et al. Central mechanisms underlying short- and long-term regulation of the cardiovascular system. Clin Exp Pharmacol Physiol. 2002; 29, 261–268.CrossRefGoogle Scholar
Izzo, J, Jr., Taylor, A. The sympathetic nervous system and baroreflexes in hypertension and hypotension. Current Science Inc. 1999; 1, 254–263.CrossRefGoogle ScholarPubMed
Hein, L, Altman, JD, Kobilka, BK. Two functionally distinct alpha2-adrenergic receptors regulate sympathetic neurotransmission. Nature. 1999; 402, 181–184.CrossRefGoogle ScholarPubMed
Shannon, R, Chaudhry, M. Effect of α1-adrenergic receptors in cardiac pathophysiology. Am Heart J. 2006; 152, 842–850.CrossRefGoogle ScholarPubMed
Wang, GY, McCloskey, DT, Turcato, S, Swigart, PM, Simpson, PC, Baker, AJ. Contrasting inotropic responses to α1-adrenergic receptor stimulation in left versus right ventricular myocardium. Am J Physiol Heart Circ Physiol. 2006; 291, H2013–H2017.Google Scholar
Kedzierski, RM, Yanagisawa, M. Endothelin system: the double-edged sword in health and disease. Ann Rev Pharmacol Toxicol. 2001; 41, 851–876.CrossRefGoogle ScholarPubMed
De Mello, WC, Danser, AHJ. Angiotensin II and the heart: on the intracrine renin-angiotensin system. Hypertension. 2000; 35, 1183–1188.CrossRefGoogle ScholarPubMed
Baker, KM, Booz, GW, Dostal, DE. Cardiac actions of angiotensin II: role of an intracardiac renin-angiotensin system. Ann Rev Physiol. 1992; 54, 227–241.CrossRefGoogle ScholarPubMed
Kohan, DE, Rossi, NF, Inscho, EW, Pollock, DM. Regulation of blood pressure and salt homeostasis by endothelin. Physiol Rev. 2011; 91, 1–77.CrossRefGoogle ScholarPubMed
Smith, FG, van der Velde, L, Sener, A. Nitric oxide modulates renal vasoconstrictor effect of endothelin-1 in conscious lambs. Pediatr Nephrol. 2005; 20, 1545–1551.CrossRefGoogle ScholarPubMed
Curhan, GC, Willett, WC, Rimm, EB, Spiegelman, D, Ascherio, AL, Stampfer, MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996; 94, 3246–3250.CrossRefGoogle ScholarPubMed
Mu, M, Wang, SF, Sheng, J, et al. Birth weight and subsequent blood pressure: a meta-analysis. Arch Cardiovasc Dis. 2012; 105, 99–113.CrossRefGoogle ScholarPubMed
Lackland, DT, Egan, BM, Ferguson, PL. Low birth weight as a risk factor for hypertension. he J Clin Hypertens. 2003; 5, 133–136.CrossRefGoogle ScholarPubMed
McMillen, IC, MacLaughlin, SM, Muhlhausler, BS, Gentili, S, Duffield, JL, Morrison, JL. Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin Pharmacol Toxicol. 2008; 102, 82–89.CrossRefGoogle ScholarPubMed
Edwards, LJ, McMillen, IC. Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2002; 283, R669–R679.CrossRefGoogle ScholarPubMed
Ceelen, M, van Weissenbruch, MM, Vermeiden, JPW, van Leeuwen, FE, Delemarre-van de Waal, HA. Cardiometabolic differences in children born after in vitro fertilization: follow-up study. J Clin Endocrinol Metab. 2008; 93, 1682–1688.CrossRefGoogle ScholarPubMed
Padhee, M, Zhang, S, Lie, S, et al. The periconceptional environment and cardiovascular disease: does in vitro embryo culture and transfer influence cardiovascular development and health? Nutrients. 2015; 7, 1378–1425.CrossRefGoogle ScholarPubMed
Scherrer, U, Rimoldi, SF, Rexhaj, E, et al. Systemic and pulmonary vascular dysfunction in children conceived by assisted reproductive technologies. Circulation. 2012; doi: 10.1161/circulationaha.111.071183 CrossRefGoogle ScholarPubMed
Watkins, AJ, Fleming, TP. Blastocyst environment and its influence on offspring cardiovascular health: the heart of the matter. J Anat. 2009; 215, 52–59.CrossRefGoogle ScholarPubMed
Morrison, JL, Berry, MJ, Botting, KJ, et al. Improving pregnancy outcomes in humans through studies in sheep. Am J Physiol Regul Integr Comp Physiol. 2018; 315, R1123–R1153.CrossRefGoogle ScholarPubMed
Segar, JL. Ontogeny of the arterial and cardiopulmonary baroreflex during fetal and postnatal life. Am J Physiol Regul Integr Comp Physiol. 1997; 273, R457–R471.CrossRefGoogle ScholarPubMed
Segar, JL, Hajduczok, G, Smith, BA, Merrill, DC, Robillard, JE. Ontogeny of baroreflex control of renal sympathetic nerve activity and heart rate. Am J Physiol Heart Circ Physiol. 1992; 263, H1819–H1826.CrossRefGoogle ScholarPubMed
Yu, ZY, Lumbers, ER. Measurement of baroreceptor-mediated effects on heart rate variability in fetal sheep. Pediatr Res. 2000; 47, 233–239.CrossRefGoogle ScholarPubMed
Yu, ZY, Lumbers, ER. Effects of birth on baroreceptor-mediated changes in heart rate variability in lambs and fetal sheep. Clin Exp Pharmacol Physiol. 2002; 29, 455–463.CrossRefGoogle ScholarPubMed
Lee, WB, Ismay, MJ, Lumbers, ER. Mechanisms by which angiotensin II affects the heart rate of the conscious sheep. Circ Res. 1980; 47, 286–292.CrossRefGoogle ScholarPubMed
Lumbers, ER, Yu, ZY. A method for determining baroreflex-mediated sympathetic and parasympathetic control of the heart in pregnant and non-pregnant sheep. J Physiol. 1999; 515, 555–566.CrossRefGoogle ScholarPubMed
Lumbers, ER, Potter, EK. Inhibition of the vagal component of the baroreceptor-cardioinhibitory reflex by angiotensin III in dogs and sheep. J Physiol. 1983; 336, 83–89.CrossRefGoogle ScholarPubMed
Ismay, MJ, Lumbers, ER, Stevens, AD. The action of angiotensin II on the baroreflex response of the conscious ewe and the conscious fetus. J Physiol. 1979; 288, 467–479.Google ScholarPubMed
Gardner, DS, Pearce, S, Dandrea, J, et al. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension. 2004; 43, 1290–1296.CrossRefGoogle ScholarPubMed
Hawkins, P, Steyn, C, Ozaki, T, Saito, T, Noakes, D, Hanson, M. Effect of maternal undernutrition in early gestation on ovine fetal blood pressure and cardiovascular reflexes. Am J Physiol Regul Integr Comp Physiol. 2000; 279, R340–R348.CrossRefGoogle ScholarPubMed
Gopalakrishnan, GS, Gardner, DS, Rhind, SM, et al. Programming of adult cardiovascular function after early maternal undernutrition in sheep. Am J Physiol Regul Integr Comp Physiol. 2004; 287, R12–R20.CrossRefGoogle ScholarPubMed
Gardner, DK. In Vitro Fertilization: A Practical Approach, 2007. Informa Healthcare, London.Google Scholar
Grundy, D. Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. J Physiol. 2015; 593, 2547–2549.CrossRefGoogle ScholarPubMed
Tervit, HR, Whittingham, DG, Rowson, LE. Successful culture in vitro of sheep and cattle ova. J Reprod Fertil. 1972; 30, 493–497.CrossRefGoogle ScholarPubMed
Walker, SK, Hill, JL, Kleemann, DO, Nancarrow, CD. Development of ovine embryos in synthetic oviductal fluid containing amino acids at oviductal fluid concentrations. Biol Reprod. 1996; 55, 703–708.CrossRefGoogle ScholarPubMed
Edwards, LJ, McMillen, IC. Periconceptional nutrition programs development of the cardiovascular system in the fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2002; 283, R669–R679.CrossRefGoogle ScholarPubMed
Bustin, SA, Benes, V, Garson, JA, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55, 611–622.CrossRefGoogle ScholarPubMed
Wang, KC, Lim, CH, McMillen, IC, Duffield, JA, Brooks, DA, Morrison, JL. Alteration of cardiac glucose metabolism in association to low birth weight: Experimental evidence in lambs with left ventricular hypertrophy. Metabolism. 2013. doi: 10.1016/j.metabol.2013.06.013 CrossRefGoogle ScholarPubMed
Passmore, M, Nataatmadja, M, Fraser, JF. Selection of reference genes for normalisation of real-time RT-PCR in brain-stem death injury in Ovis aries. BMC Mol Biol. 2009; 10, 72.CrossRefGoogle ScholarPubMed
Wang, KC, Lim, CH, McMillen, IC, Duffield, JA, Brooks, DA, Morrison, JL. Alteration of cardiac glucose metabolism in association to low birth weight: experimental evidence in lambs with left ventricular hypertrophy. Metabolism. 2013; 62, 1662–1672.CrossRefGoogle ScholarPubMed
Hellemans, J, Vandesompele, J. Selection of reliable reference genes for RT-qPCR analysis. Methods Mol Biol. 2014; 1160, 19–26.CrossRefGoogle ScholarPubMed
Hellemans, J, Mortier, G, De Paepe, A, Speleman, F, Vandesompele, J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 2007; 8, 1–14.CrossRefGoogle ScholarPubMed
Soo, PS, Hiscock, J, Botting, KJ, Roberts, CT, Davey, AK, Morrison, JL. Maternal undernutrition reduces P-glycoprotein in guinea pig placenta and developing brain in late gestation. Reprod Toxicol. 2012; 33, 374–381.CrossRefGoogle ScholarPubMed
McGillick, EV, Orgeig, S, McMillen, IC, Morrison, JL. The fetal sheep lung does not respond to cortisol infusion during the late canalicular phase of development. Physiol Rep. 2013; 1, e00130.CrossRefGoogle Scholar
Ricketts, JH, Head, GA. A five-parameter logistic equation for investigating asymmetry of curvature in baroreflex studies. Am J Physiol. 1999; 277, R441–R454.Google ScholarPubMed
Head, GA, McCarty, R. Vagal and sympathetic components of the heart rate range and gain of the baroreceptor-heart rate reflex in conscious rats. J Auton Nerv Syst. 1987; 21, 203–213.CrossRefGoogle ScholarPubMed
Lim, GB. Assisted reproductive technologies increase risk of hypertension in offspring. Nat Rev Cardiol. 2018; 15, 656.CrossRefGoogle ScholarPubMed
Meister, TA, Rimoldi, SF, Soria, R, et al. Association of assisted reproductive technologies with arterial hypertension during adolescence. J Am Coll Cardiol. 2018; 72, 1267–1274.CrossRefGoogle ScholarPubMed
Padhee, M, Zhang, S, Lie, S, et al. The periconceptional environment and cardiovascular disease: does in vitro embryo culture and transfer influence cardiovascular development and health? Nutrients. 2015; 7, 1378–1425.CrossRefGoogle ScholarPubMed
Sakka, SD, Loutradis, D, Kanaka-Gantenbein, C, et al. Absence of insulin resistance and low-grade inflammation despite early metabolic syndrome manifestations in children born after in vitro fertilization. Fertil Steril. 2010; 94, 1693–1699.CrossRefGoogle ScholarPubMed
Thomas, GD. Neural control of the circulation. Adv Physiol Educ. 2011; 35, 28–32.CrossRefGoogle ScholarPubMed
Pernow, J, Boutier, JF, Franco-Cereceda, A, et al. Potent selective vasoconstrictor effects of endothelin in the pig kidney in vivo. Acta Physiol Scand. 1998; 134, 573–574.CrossRefGoogle Scholar
Lanese, DM, Yuan, BH, McMurtry, IF, Conger, JD. Comparative sensitivities of isolated rat renal arterioles to endothelin. Am J Physiol Renal Physiol. 1992; 263, F894–F899.CrossRefGoogle ScholarPubMed
Kohan, DE. Endothelins in the kidney: physiology and pathophysiology. Am J Kidney Dis. 1993; 22, 493–510.CrossRefGoogle ScholarPubMed
Billet, S, Aguilar, F, Baudry, C, Clauser, E. Role of angiotensin II AT sub(1) receptor activation in cardiovascular diseases. Kidney Int. 2008; 74, 1379–1384.CrossRefGoogle Scholar