High fructose consumption in pregnancy alters the perinatal environment without increasing metabolic disease in the offspring

Reproduction, Fertility and Development

Volumn 28, Issue 12, 2016, Pages 2007-2015

  Lineker, Christopher ^a   Kerr, Paul M ^a,c   Nguyen, Patricia ^a   Bloor, Ian ^b   Astbury, Stuart ^a,b   Patel, Nikhil ^a,b   Budge, Helen ^b   Hemmings, Denise G ^a   Plane, Frances ^a   Symonds, Michael E ^b   Bell, Rhonda C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c MACEWAN UNIVERSITY   (Canada)

Author keywords

developmental origins; fetal programming; metabolism; vascular function

Indexed keywords

AMINO ACID TRANSPORTER; GLUCOSE; INSULIN; TRIACYLGLYCEROL; FRUCTOSE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE REGULATION; BLOOD VESSEL REACTIVITY; BODY WEIGHT; CARBOHYDRATE INTAKE; CONTROLLED STUDY; FAT MASS; FEMALE; FETUS; FETUS DEVELOPMENT; GENE EXPRESSION; GLUCOSE TRANSPORTER 1 GENE; GROWTH RATE; INSULIN BLOOD LEVEL; MARKER GENE; MATERNAL OBESITY; METABOLIC DISORDER; NONHUMAN; PERINATAL PERIOD; PLACENTA WEIGHT; PREGNANCY; PROGENY; RAT; REPRODUCTION; TISSUE PERFUSION; TRIACYLGLYCEROL BLOOD LEVEL; WEANING; ANIMAL; DIET; GROWTH, DEVELOPMENT AND AGING; NEWBORN; PLACENTA; PRENATAL EXPOSURE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BODY WEIGHT; DIET; FEMALE; FRUCTOSE; METABOLIC DISEASES; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS, WISTAR;

EID: 84991490671     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD15119     Document Type: Article

References (44)

1. Ainge, H., Thompson, C., Ozanne, S. E., and Rooney, K. B. (2011). A systematic review on animal models of maternal high fat feeding, and offspring glycaemic control. Int. J. Obes. 35, 325-335. doi: 10.1038/IJO.2010.149
2. Alzamendi, A., Castrogiovanni, D., Gaillard, R. C., Spinedi, E., and Giovambattista, A. (2010). Increased male offspring's risk of metabolicneuroendocrine dysfunction, and overweight after fructose-rich diet intake by the lactating mother. Endocrinology 151, 4214-4223. doi: 10.1210/EN.2009-1353
3. Armitage, J. A., Taylor, P. D., and Poston, L. (2005). Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J. Physiol. 565, 3-8. doi: 10.1113/JPHYSIOL.2004.079756
4. Battaglia, F. C., and Meschia, G. (1978). Principal substrates of fetal metabolism. Physiol. Rev. 58, 499-527
5. Bloor, I. D., and Symonds, M. E. (2014). Sexual dimorphism in white, and brown adipose tissue with obesity, and inflammation. Horm. Behav. 66, 95-103. doi: 10.1016/J.YHBEH.2014.02.007
6. Bruun, J. M., Stallknecht, B., Helge, J. W., and Richelsen, B. (2007). Interleukin-18 in plasma, and adipose tissue: effects of obesity, insulin resistance, and weight loss. Eur. J. Endocrinol. 157, 465-471. doi: 10.1530/EJE-07-0206
7. Catena, C., Giacchetti, G., Novello, M., Colussi, G., Cavarape, A., and Sechi, L. A. (2003). Cellular mechanisms of insulin resistance in rats with fructose-induced hypertension. Am. J. Hypertens. 16, 973-978. doi: 10.1016/S0895-7061(03)01002-1
8. Chesley, L. C., Talledo, E., Bohler, C. S., and Zuspan, F. P. (1965). Vascular reactivity to angiotensin II, and norepinephrine in pregnant women. Am. J. Obstet. Gynecol. 91, 837-842
9. Despreís, J.-P., and Lemieux, I. (2006). Abdominal obesity, and metabolic syndrome. Nature 444, 881-887. doi: 10.1038/NATURE05488
10. Duvekot, J. J., and Peeters, L. L. (1994). Maternal cardiovascular hemodynamic adaptation to pregnancy. Obstet. Gynecol. Surv. 49(12 Suppl), S1-S14. doi: 10.1097/00006254-199412011-00001
11. Ericsson, A., Säljö, K., Sjöstrand, E., Jansson, N., Prasad, P. D., Powell, T. L., and Jansson, T. (2007). Brief hyperglycaemia in the early pregnant rat increases fetal weight at term by stimulating placental growth, and affecting placental nutrient transport. J. Physiol. 581, 1323-1332. doi: 10.1113/JPHYSIOL.2007.131185
12. Friis, C. M., Paasche Roland, M. C., Godang, K., Ueland, T., Tanbo, T., Bollerslev, J., and Henriksen, T. (2013). Adiposity-related inflammation: effects of pregnancy. Obesity (Silver Spring) 21, E124-E130. doi: 10.1002/OBY.20120
13. Gaither, K., Quraishi, A. N., and Illsley, N. P. (1999). Diabetes alters the expression, and activity of the human placental GLUT1 glucose transporter. J. Clin. Endocrinol. Metab. 84, 695-701
14. Gerber, R. T., Anwar, M. A., and Poston, L. (1998). Enhanced acetylcholine induced relaxation in small mesenteric arteries from pregnant rats: an important role for endothelium-derived hyperpolarizing factor (EDHF). Br. J. Pharmacol. 125, 455-460. doi: 10.1038/SJ.BJP.0702099
15. Gombos, R. B., and Hemmings, D. G. (2010). Differential effects on nitric oxide-mediated vasodilation in mesenteric, and uterine arteries from cytomegalovirus-infected mice. Am. J. Physiol. Heart Circ. Physiol. 299, H1124-H1134. doi: 10.1152/AJPHEART.01113.2009
16. Goran, M. I., Ulijaszek, S. J., and Ventura, E. E. (2013). High fructose corn syrup, and diabetes prevalence: a global perspective. Glob. Public Health 8, 55-64. doi: 10.1080/17441692.2012.736257
17. Hemmings, D. G., Williams, S. J., and Davidge, S. T. (2005). Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. Am. J. Physiol. Heart Circ. Physiol. 289, H674-H682. doi: 10.1152/AJPHEART.00191.2005
18. Hwang, I. S., Ho, H., Hoffman, B. B., and Reaven, G. M. (1987). Fructoseinduced insulin resistance, and hypertension in rats. Hypertension 10, 512-516. doi: 10.1161/01.HYP.10.5.512
19. Jansson, T., Wennergren, M., and Powell, T. L. (1999). Placental glucose transport, and GLUT 1 expression in insulin-dependent diabetes. Am. J. Obstet. Gynecol. 180, 163-168. doi: 10.1016/S0002-9378(99)70169-9
20. Johnson, R. J., Segal, M. S., Sautin, Y., Nakagawa, T., Feig, D. I., Kang, D.-H., Gersch, M. S., Benner, S., and Saínchez-Lozada, L. G. (2007). Potential role of sugar (fructose) in the epidemic of hypertension, obesity, and the metabolic syndrome, diabetes, kidney disease, and cardiovascular disease. Am. J. Clin. Nutr. 86, 899-906
21. Julian, C. G., Galan, H. L., Wilson, M. J., DeSilva, W., Cioffi-Ragan, D., Schwartz, J., and Moore, L. G. (2008). Lower uterine artery blood flow, and higher endothelin relative to nitric oxide metabolite levels are associated with reductions in birth weight at high altitude. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R906-R915. doi: 10.1152/AJPREGU.00164.2008
22. Kaaja, R., Tikkanen, M. J., Viinikka, L., and Ylikorkala, O. (1995). Serum lipoproteins, insulin, and urinary prostanoid metabolites in normal, and hypertensive pregnant women. Obstet. Gynecol. 85, 353-356. doi: 10.1016/0029-7844(94)00380-V
23. Kashiwagi, H., Yamazaki, K., Takekuma, Y., Ganapathy, V., and Sugawara, M. (2009). Regulatory mechanisms of SNAT2, an amino acid transporter, in L6 rat skeletal muscle cells by insulin, osmotic shock, and amino acid deprivation. Amino Acids 36, 219-230. doi: 10.1007/S00726-008-0050-9
24. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR, and the 2 DDCT method. Methods 25, 402-408. doi: 10.1006/METH.2001.1262
25. McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571-633. doi: 10.1152/PHYSREV.00053.2003
26. Metcalfe, J., McAnulty, J. H., and Ueland, K. (1981). Cardiovascular physiology. Clin. Obstet. Gynecol. 24, 693-710. doi: 10.1097/00003081-198109000-00002
27. Meznarich, H. K., Hay, W. W., Sparks, J. W., Meschia, G., and Battaglia, F. C. (1987). Fructose disposal, and oxidation rates in the ovine fetus. Q. J. Exp. Physiol. 72, 617-625. doi: 10.1113/EXPPHYSIOL.1987. SP003102
28. Nyby, M. D., Abedi, K., Smutko, V., Eslami, P., and Tuck, M. L. (2007). Vascular angiotensin type 1 receptor expression is associated with vascular dysfunction, oxidative stress, and inflammation in fructosefed rats. Hypertens. Res. 30, 451-457. doi: 10.1291/HYPRES.30.451
29. Ogura, K., Sakata, M., Yamaguchi, M., Kurachi, H., and Murata, Y. (1999). High concentration of glucose decreases glucose transporter-1 expression in mouse placenta in vitro, and in vivo. J. Endocrinol. 160, 443-452. doi: 10.1677/JOE.0.1600443
30. Ojha, S., Saroha, V., Symonds, M. E., and Budge, H. (2013). Excess nutrient supply in early life, and its later metabolic consequences. Clin. Exp. Pharmacol. Physiol. 40, 817-823. doi: 10.1111/1440-1681.12061
31. Osmond, D. T., King, R. G., Brennecke, S. P., and Gude, N. M. (2001). Placental glucose transport, and utilisation is altered at term in insulintreated, gestational-diabetic patients. Diabetologia 44, 1133-1139. doi: 10.1007/S001250100609
32. Park, K.-G., Park, K. S., Kim, M.-J., Kim, H.-S., Suh, Y.-S., Ahn, J. D., Park, K.-K., Chang, Y.-C., and Lee, I.-K. (2004). Relationship between serum adiponectin, and leptin concentrations, and body fat distribution. Diabetes Res. Clin. Pract. 63, 135-142. doi: 10.1016/J.DIABRES. 2003.09.010
33. Plane, F., Hurrell, A., Jeremy, J. Y., and Garland, C. J. (1996). Evidence that potassium channels make a major contribution to SIN-1-evoked relaxation of rat isolated mesenteric artery. Br. J. Pharmacol. 119, 1557-1562. doi: 10.1111/J.1476-5381.1996.TB16072.X
34. Powe, C. E., Levine, R. J., and Karumanchi, S. A. (2011). Preeclampsia, a disease of the maternal endothelium: the role of antiangiogenic factors, and implications for later cardiovascular disease. Circulation 123, 2856-2869. doi: 10.1161/CIRCULATIONAHA.109.853127
35. Rich-Edwards, J. W., Fraser, A., Lawlor, D. A., and Catov, J. M. (2014). Pregnancy characteristics, and women's future cardiovascular health: an underused opportunity to improve women's health? Epidemiol. Rev. 36, 57-70. doi: 10.1093/EPIREV/MXT006
36. Romacho, T., Elsen, M., Röhrborn, D., and Eckel, J. (2014). Adipose tissue, and its role in organ crosstalk. Acta Physiol. (Oxf.) 210, 733-753. doi: 10.1111/APHA.12246
37. Sebert, S., Salonurmi, T., Keinänen-Kiukaanniemi, S., Savolainen, M., Herzig, K.-H., Symonds, M. E., and Järvelin, M.-R. (2014). Programming effects of FTO in the development of obesity. Acta Physiol. (Oxf.) 210, 58-69. doi: 10.1111/APHA.12196
38. Sun, S. Z., Anderson, G. H., Flickinger, B. D., Williamson-Hughes, P. S., and Empie, M. W. (2011). Fructose, and non-fructose sugar intakes in the US population, and their associations with indicators of metabolic syndrome. Food Chem. Toxicol. 49, 2875-2882. doi: 10.1016/J.FCT. 2011.07.068
39. Takagawa, Y., Berger, M. E., Hori, M. T., Tuck, M. L., and Golub, M. S. (2001). Long-term fructose feeding impairs vascular relaxation in rat mesenteric arteries. Am. J. Hypertens. 14, 811-817. doi: 10.1016/S0895-7061(01)01298-5
40. Veerareddy, S., Cooke, C.-L. M., Baker, P. N., and Davidge, S. T. (2002). Vascular adaptations to pregnancy in mice: effects on myogenic tone. Am. J. Physiol. Heart Circ. Physiol. 283, H2226-H2233. doi: 10.1152/AJPHEART.00593.2002
41. Vickers, M. H., Clayton, Z. E., Yap, C., and Sloboda, D. M. (2011). Maternal fructose intake during pregnancy, and lactation alters placental growth, and leads to sex-specific changes in fetal, and neonatal endocrine function. Endocrinology 152, 1378-1387. doi: 10.1210/EN.2010-1093
42. Virdis, A., Ghiadoni, L., Giannarelli, C., and Taddei, S. (2010). Endothelial dysfunction, and vascular disease in later life. Maturitas 67, 20-24. doi: 10.1016/J.MATURITAS.2010.04.006
43. Waldeín, T. B., Hansen, I. R., Timmons, J. A., Cannon, B., and Nedergaard, J. (2012). Recruited vs. nonrecruited molecular signatures of brown, ?brite, ?, and white adipose tissues. Am. J. Physiol. Endocrinol. Metab. 302, E19-E31. doi: 10.1152/AJPENDO.00249.2011
44. Xiao, D., Buchholz, J. N., and Zhang, L. (2006). Pregnancy attenuates uterine artery pressure-dependent vascular tone: role of PKC/ERK pathway. Am. J. Physiol. Heart Circ. Physiol. 290, H2337-H2343. doi: 10.1152/AJPHEART.01238.2005