Potential effect of maternal dietary sucrose or fructose syrup on CD36, leptin, and ghrelin-mediated fetal programming of obesity

References

• Padmanabhan V, Cardoso RC, Puttabyatappa M. Developmental programming, a pathway to disease. Endocrinology. 2016;157(4):1328–40. Epub 2016/02/10. doi:10.1210/en.2016-1003. PubMed PMID: 26859334; PubMed Central PMCID: PMCPMC4816734.
   PubMed Web of Science ®Google Scholar
• Whisner CM, Young BE, Pressman EK, Queenan RA, Cooper EM, O’Brien KO. Maternal diet but not gestational weight gain predicts central adiposity accretion in utero among pregnant adolescents. Int J Obes. 2015;39(4):565–70. doi: 10.1038/ijo.2014.202
   Web of Science ®Google Scholar
• Prior LJ, Davern PJ, Burke SL, Lim K, Armitage JA, Head GA. Exposure to a high-fat diet during development alters leptin and ghrelin sensitivity and elevates renal sympathetic nerve activity and arterial pressure in rabbits. Hypertension (Dallas, Tex: 1979) 2014;63(2):338–45. Epub 2013/11/06. doi: 10.1161/hypertensionaha.113.02498. PubMed PMID: 24191287.
   PubMed Web of Science ®Google Scholar
• Tappy L, Lê KA, Tran C, Paquot N. Fructose and metabolic diseases: New findings, new questions. Nutrition. 2010;26(11–12):1044–9. doi: 10.1016/j.nut.2010.02.014
   PubMed Web of Science ®Google Scholar
• Page KA, Melrose AJ. Brain, hormone and appetite responses to glucose versus fructose. Curr Opin Behav Sci. 2016;9:111–7. doi: 10.1016/j.cobeha.2016.03.002
   Web of Science ®Google Scholar
• Lempradl A, Pospisilik JA, Penninger JM. Exploring the emerging complexity in transcriptional regulation of energy homeostasis. Nat Rev Genet. 2015;16(11):665–81. doi: 10.1038/nrg3941
   PubMed Web of Science ®Google Scholar
• Batista LO, Ramos VW, Rosas Fernández MA, Concha Vilca CM, Albuquerque KTd. Oral solution of fructose promotes SREBP-1c high-expression in the hypothalamus of wistar rats. Nutr Neurosci. 2018:1–7. doi: 10.1080/1028415X.2018.1427659.
   Web of Science ®Google Scholar
• Djordjevic A, Bursać B, Veličković N, Vasiljević A, Matić G. The impact of different fructose loads on insulin sensitivity, inflammation, and PSA-NCAM-mediated plasticity in the hippocampus of fructose-fed male rats. Nutr Neurosci. 2015;18(2):66–75. doi: 10.1179/1476830513Y.0000000098
   PubMed Web of Science ®Google Scholar
• Wu HW, Ren LF, Zhou X, Han DW. A high-fructose diet induces hippocampal insulin resistance and exacerbates memory deficits in male sprague-dawley rats. Nutr Neurosci. 2015;18(7):323–8. Epub 2014/05/27. doi:10.1179/1476830514y.0000000133. PubMed PMID: 24856097.
   PubMed Web of Science ®Google Scholar
• Nergiz-Unal R, Rademakers T, Cosemans JM, Heemskerk JW. CD36 as a multiple-ligand signaling receptor in atherothrombosis. Cardiovasc Hematol Agents Med Chem. 2011;9(1):42–55. PubMed PMID: 20939828. doi: 10.2174/187152511794182855
   PubMedGoogle Scholar
• Alkhatatbeh M, Mhaidat N, Enjeti A, Lincz L, Thorne R. The putative diabetic plasma marker, soluble CD36, is non-cleaved, non-soluble and entirely associated with microparticles. J Thromb Haemostasis. 2011;9(4):844–51. doi: 10.1111/j.1538-7836.2011.04220.x
   PubMed Web of Science ®Google Scholar
• Ekici M, Kisa U, Arikan Durmaz S, Ugur E, Nergiz-Unal R. Fatty acid transport receptor sCD36 and dietary fatty acid pattern in type 2 diabetic patients: A comparative study. Br J Nutr. 2017; (epub ahead of print). doi:10.1017/S0007114517003269.
   Web of Science ®Google Scholar
• Yuruk AA, Nergiz-Unal R. Maternal dietary free or bound fructose diversely influence developmental programming of lipogenesis. Lipids Health Dis. 2017; (epub ahead of print). doi:10.1186/s12944-017-0618-z.
   PubMed Web of Science ®Google Scholar
• Calvo SS-C, Egan JM. The endocrinology of taste receptors. Nature Reviews Endocrinology. 2015;11(4):213–27. doi: 10.1038/nrendo.2015.7
   PubMed Web of Science ®Google Scholar
• Moullé VS, Le Foll C, Philippe E, Kassis N, Rouch C, Marsollier N, et al. Fatty acid transporter CD36 mediates hypothalamic effect of fatty acids on food intake in rats. PLOS ONE. 2013;8(9):e74021. doi: 10.1371/journal.pone.0074021
   PubMed Web of Science ®Google Scholar
• Niot I, Besnard P. Appetite control by the tongue-gut axis and evaluation of the role of CD36/SR-B2. Biochimie. 2017;136:27–32. doi: 10.1016/j.biochi.2017.02.011
   PubMed Web of Science ®Google Scholar
• Zhao C, Castonguay TW. Effects of free access to sugar solutions on the control of energy intake. Food Rev Int. 2017;33(2):105–22. doi: 10.1080/87559129.2016.1149863
   Web of Science ®Google Scholar
• Madero M, Arriaga JC, Jalal D, Rivard C, McFann K, Perez-Mendez O, et al. The effect of two energy-restricted diets, a low-fructose diet versus a moderate natural fructose diet, on weight loss and metabolic syndrome parameters: a randomized controlled trial. Metabolism. 2011;60(11):1551–9. doi: 10.1016/j.metabol.2011.04.001. PubMed PMID: 21621801.
   PubMed Web of Science ®Google Scholar
• Nemoseck TM, Carmody EG, Furchner-Evanson A, Gleason M, Li A, Potter H, et al. Honey promotes lower weight gain, adiposity, and triglycerides than sucrose in rats. Nutr Res. 2011;31(1):55–60. doi: 10.1016/j.nutres.2010.11.002
   PubMed Web of Science ®Google Scholar
• Dekker MJ, Su Q, Baker C, Rutledge AC, Adeli K. Fructose: a highly lipogenic nutrient implicated in insulin resistance, hepatic steatosis, and the metabolic syndrome. American Journal of Physiology-Endocrinology and Metabolism. 2010;299(5):E685–E694. Epub 2010/09/09. doi: 10.1152/ajpendo.00283.2010. PubMed PMID: 20823452.
   PubMed Web of Science ®Google Scholar
• Havel PJ. Dietary fructose: implications for dysregulation of energy homeostasis and lipid/carbohydrate metabolism. Nutr Rev. 2005;63(5):133–57. doi: 10.1111/j.1753-4887.2005.tb00132.x
   PubMed Web of Science ®Google Scholar
• Lowndes J, Kawiecki D, Pardo S, Nguyen V, Melanson KJ, Yu Z, et al. The effects of four hypocaloric diets containing different levels of sucrose or high fructose corn syrup on weight loss and related parameters. Nutr J. 2012;11(1):55. doi: 10.1186/1475-2891-11-55
   PubMed Web of Science ®Google Scholar
• Bocarsly ME, Powell ES, Avena NM, Hoebel BG. High-fructose corn syrup causes characteristics of obesity in rats: increased body weight, body fat and triglyceride levels. Pharmacol Biochem Behav. 2010;97(1):101–6. doi: 10.1016/j.pbb.2010.02.012
   PubMed Web of Science ®Google Scholar
• Bowen J, Noakes M, Clifton P. Appetite hormones and energy intake in obese men after consumption of fructose, glucose and whey protein beverages. Int J Obes. 2007;31(11):1696–1703. doi: 10.1038/sj.ijo.0803665
   Web of Science ®Google Scholar
• Sampson DA, Jansen GR. Measurement of milk yield in the lactating rat from pup weight and weight gain. J Pediatr Gastroenterol Nutr. 1984;3(4):613–7. doi: 10.1097/00005176-198409000-00023
   PubMed Web of Science ®Google Scholar
• Nergiz-Unal R, Kuijpers MJ, de Witt SM, Heeneman S, Feijge MA, Garcia Caraballo SC, et al. Atheroprotective effect of dietary walnut intake in ApoE-deficient mice: involvement of lipids and coagulation factors. Thromb Res. 2013;131(5):411–7. PubMed PMID: 23347681. doi: 10.1016/j.thromres.2013.01.003
   PubMed Web of Science ®Google Scholar
• Lindqvist A, Baelemans A, Erlanson-Albertsson C. Effects of sucrose, glucose and fructose on peripheral and central appetite signals. Regulatory Peptides. 2008;150(1–3):26–32. Epub 2008/07/17. doi: 10.1016/j.regpep.2008.06.008. PubMed PMID: 18627777.
   PubMedGoogle Scholar
• Kouno T, Akiyama N, Fujieda K, Nanchi I, Okuda T, Iwasaki T, et al. Reduced intake of carbohydrate prevents the development of obesity and impaired glucose metabolism in ghrelin O-acyltransferase knockout mice. Peptides. 2016;86:145–52. doi: 10.1016/j.peptides.2016.11.003
   PubMed Web of Science ®Google Scholar
• Glintborg D, Højlund K, Andersen M, Henriksen JE, Beck-Nielsen H, Handberg A. Soluble CD36 and risk markers of insulin resistance and atherosclerosis are elevated in polycystic ovary syndrome and significantly reduced during pioglitazone treatment. Diabetes Care. 2008;31(2):328–34. doi: 10.2337/dc07-1424
   PubMed Web of Science ®Google Scholar
• Nagy TR, Clair AL. Precision and accuracy of dual-energy X-ray absorptiometry for determining in vivo body composition of mice. Obes Res. 2000;8(5):392–8. Epub 2000/09/01. doi: 10.1038/oby.2000.47. PubMed PMID: 10968731.
   PubMedGoogle Scholar
• Dobush GR, Ankney CD, Krementz DG. The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Can J Zool. 1985;63(8):1917–20. doi: 10.1139/z85-285
   Web of Science ®Google Scholar
• Chen CS-Y, Bench EM, Allerton TD, Schreiber AL, Arceneaux KP, Primeaux SD. Preference for linoleic acid in obesity-prone and obesity-resistant rats is attenuated by the reduction of CD36 on the tongue. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology. 2013;305(11):R1346–R1R55. doi: 10.1152/ajpregu.00582.2012
   PubMed Web of Science ®Google Scholar
• Su ML, He Y, Li QS, Zhu BH. Efficacy of acetylshikonin in preventing obesity and hepatic steatosis in db/db mice. Molecules. 2016;21(8). PubMed PMID: 27483220. doi: 10.3390/molecules21080976
   Web of Science ®Google Scholar
• Nergiz-Unal R, Lamers MM, Van Kruchten R, Luiken JJ, Cosemans JM, Glatz JF, et al. Signaling role of CD36 in platelet activation and thrombus formation on immobilized thrombospondin or oxidized low-density lipoprotein. J Thromb Haemostasis. 2011;9(9):1835–46. PubMed PMID: 21696539. doi: 10.1111/j.1538-7836.2011.04416.x
   PubMed Web of Science ®Google Scholar
• Tetri LH, Basaranoglu M, Brunt EM, Yerian LM, Neuschwander-Tetri BA. Severe NAFLD with hepatic necroinflammatory changes in mice fed trans fats and a high-fructose corn syrup equivalent. American Journal of Physiology-Gastrointestinal and Liver Physiology. 2008;295(5):G987–G995. doi: 10.1152/ajpgi.90272.2008
   PubMed Web of Science ®Google Scholar
• Mock K, Lateef S, Benedito VA, Tou JC. High-fructose corn syrup-55 consumption alters hepatic lipid metabolism and promotes triglyceride accumulation. J Nutr Biochem. 2017;39:32–39. doi: 10.1016/j.jnutbio.2016.09.010
   PubMed Web of Science ®Google Scholar
• Toop CR, Muhlhausler BS, O’Dea K, Gentili S. Consumption of sucrose, but not high fructose corn syrup, leads to increased adiposity and dyslipidaemia in the pregnant and lactating rat. J Dev Orig Health Dis. 2015;6(1):38–46. PubMed PMID: 25523154. doi: 10.1017/S2040174414000610
   PubMed Web of Science ®Google Scholar
• Teff KL, Elliott SS, Tschop M, Kieffer TJ, Rader D, Heiman M, et al. Dietary fructose reduces circulating insulin and leptin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. J Clin Endocrinol Metab. 2004;89(6):2963–72. doi: 10.1210/jc.2003-031855
   PubMed Web of Science ®Google Scholar
• Toop CR, Gentili S. Fructose beverage consumption induces a metabolic syndrome phenotype in the Rat: A systematic review and meta-analysis. Nutrients. 2016;8(9). PubMed PMID: 27657120. doi: 10.3390/nu8090577
   PubMed Web of Science ®Google Scholar
• Ackroff K, Sclafani A. Rats’ preferences for high fructose corn syrup vs. sucrose and sugar mixtures. Physiol Behav. 2011;102(5):548–52. PubMed PMID: 21236278; PubMed Central PMCID: PMCPMC3044477. doi: 10.1016/j.physbeh.2011.01.004
   PubMed Web of Science ®Google Scholar
• Bray GA, Nielsen SJ, Popkin BM. Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity. Am J Clin Nutr. 2004;79(4):537–43. PubMed PMID: 15051594. doi: 10.1093/ajcn/79.4.537
   PubMed Web of Science ®Google Scholar
• Malo E, Saukko M, Santaniemi M, Hietaniemi M, Lammentausta E, Blanco Sequeiros R, et al. Plasma lipid levels and body weight altered by intrauterine growth restriction and postnatal fructose diet in adult rats. Pediatr Res. 2013;73(2):155–62. PubMed PMID: 23174704. doi: 10.1038/pr.2012.173
   PubMed Web of Science ®Google Scholar
• Jürgens H, Haass W, Castañeda TR, Schürmann A, Koebnick C, Dombrowski F, et al. Consuming fructose-sweetened beverages increases body adiposity in mice. Obesity. 2005;13(7):1146–56. doi: 10.1038/oby.2005.136
   Web of Science ®Google Scholar
• Light HR, Tsanzi E, Gigliotti J, Morgan K, Tou JC. The type of caloric sweetener added to water influences weight gain, fat mass, and reproduction in growing sprague-dawley female rats. Exp Biol Med. 2009;234(6):651–61. Epub 2009/04/11. doi:10.3181/0812-rm-368. PubMed PMID: 19359658.
   Web of Science ®Google Scholar
• Melanson KJ, Zukley L, Lowndes J, Nguyen V, Angelopoulos TJ, Rippe JM. Effects of high-fructose corn syrup and sucrose consumption on circulating glucose, insulin, leptin, and ghrelin and on appetite in normal-weight women. Nutrition. 2007;23(2):103–12. Epub 2007/01/20. doi:10.1016/j.nut.2006.11.001. PubMed PMID: 17234503.
   PubMed Web of Science ®Google Scholar
• Yu Z, Lowndes J, Rippe J. High-fructose corn syrup and sucrose have equivalent effects on energy-regulating hormones at normal human consumption levels. Nutr Res. 2013;33(12):1043–52. Epub 2013/11/26. doi:10.1016/j.nutres.2013.07.020. PubMed PMID: 24267044.
   PubMed Web of Science ®Google Scholar
• Shapiro A, Mu W, Roncal C, Cheng K-Y, Johnson RJ, Scarpace PJ. Fructose-induced leptin resistance exacerbates weight gain in response to subsequent high-fat feeding. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2008;295(5):R1370–5. doi: 10.1152/ajpregu.00195.2008
   PubMed Web of Science ®Google Scholar
• Rodríguez L, Otero P, Panadero MI, Rodrigo S, Álvarez-Millán JJ, Bocos C. Maternal fructose intake induces insulin resistance and oxidative stress in male, but not female, offspring. J Nutr Metab. 2015;2015:1–8. doi: 10.1155/2015/158091
   Web of Science ®Google Scholar
• Saad AF, Dickerson J, Kechichian TB, Yin H, Gamble P, Salazar A, et al. High-fructose diet in pregnancy leads to fetal programming of hypertension, insulin resistance, and obesity in adult offspring. J Obstet Gynaecol. 2016. doi:10.1016/j.ajog.2016.03.038. PubMed PMID: 27060421.
   Google Scholar
• Alzamendi A, Castrogiovanni D, Gaillard RC, Spinedi E, Giovambattista A. Increased male offspring’s risk of metabolic-neuroendocrine dysfunction and overweight after fructose-rich diet intake by the lactating mother. Endocrinology. 2010;151(9):4214–23. PubMed PMID: 20660072. doi: 10.1210/en.2009-1353
   PubMed Web of Science ®Google Scholar
• Simopoulos A. Dietary omega-3 fatty acid deficiency and high fructose intake in the development of metabolic syndrome, Brain Metabolic Abnormalities, and Non-Alcoholic Fatty Liver Disease. Nutrients. 2013;5(8):2901. PubMed PMID: doi:10.3390/nu5082901.
   Web of Science ®Google Scholar
• Stoianov A, Adeli K. Central and metabolic effects of high fructose consumption: evidence from animal and human studies. Nutrition and Food Sciences Research. 2014;1(2):3–9.
   Google Scholar
• Teff KL, Grudziak J, Townsend RR, Dunn TN, Grant RW, Adams SH, et al. Endocrine and metabolic effects of consuming fructose- and glucose-sweetened beverages with meals in obese Men and women: influence of insulin resistance on plasma triglyceride responses. J Clin Endocrinol Metab. 2009;94(5):1562–69. doi: 10.1210/jc.2008-2192
   PubMed Web of Science ®Google Scholar
• Lowette K, Roosen L, Tack J, Vanden Berghe P. Effects of high-fructose diets on central appetite signaling and cognitive function. Front Nutr. 2015;2:5. doi: 10.3389/fnut.2015.00005
   PubMedGoogle Scholar
• Gaillard D, Laugerette F, Darcel N, El-Yassimi A, Passilly-Degrace P, Hichami A, et al. The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 2008;22(5):1458–68. doi: 10.1096/fj.07-8415com
   PubMed Web of Science ®Google Scholar
• Korićanac G, Tepavčević S, Romić S, Živković M, Stojiljković M, Milosavljević T, et al. Estradiol enhances effects of fructose rich diet on cardiac fatty acid transporter CD36 and triglycerides accumulation. Eur J Pharmacol. 2012;694(1–3):127–34. doi: 10.1016/j.ejphar.2012.08.007
   PubMed Web of Science ®Google Scholar
• Laugerette F, Passilly-Degrace P, Patris B, Niot I, Febbraio M, Montmayeur J-P, et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest. 2005;115(11):3177–84. PubMed PMID: PMC1265871. doi: 10.1172/JCI25299
   PubMed Web of Science ®Google Scholar