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The beneficial effect of fiber supplementation in high- or low-fat diets on fetal development and antioxidant defense capacity in the rat

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Abstract

Background

There is mounting evidence that an imbalance in oxidant/antioxidant activities plays a pivotal role in fetal development.

Aim of the study

To determine the effects of maternal intake of fat and fiber on fetal intrauterine development and antioxidant defense systems of rats.

Methods

Virgin female Sprague–Dawley rats were randomly assigned to 4 groups according to diet: the low-fat, low-fiber group (LL); the low-fat, high-fiber group (LH); the high-fat, low-fiber group (HL); and the high-fat, high-fiber group (HH). The diets were fed 4 weeks prior to breeding through day 17.5 of pregnancy. Dietary intakes of fiber (wheat bran and oat) and fat were quantitatively varied, while intakes of energy and essential nutrients were kept constant among the diets.

Results

Rats fed a fiber-rich diet had significantly improved fetal numbers, as well as enhanced activity of superoxide dismutase (SOD) and capacity of scavenging free radicals (p < 0.05). Meanwhile, the placental malondialdehyde and protein carbonyl levels were affected by the diet fat and fiber levels (p < 0.05). Compared with the LL group, the mRNA abundance of hypoxia-inducible factor 1α (HIF-1α) and thioredoxin-2 (Trx2) in the maternal liver and glutathione peroxidase 1 (GPx1) in the placenta and fetus were significantly downregulated in the HL group (p < 0.05). Furthermore, rats fed a fiber-rich diet had significantly upregulated mRNA expressions of Cu,Zn-SOD, Mn-SOD, and HIF-1α in the maternal liver (p < 0.05); Cu,Zn-SOD and Mn-SOD in the placenta (p < 0.05); and Cu,Zn-SOD in the fetus (p < 0.05).

Conclusion

When energy intakes are equivalent, consumption of fiber in high- or low-fat diets benefits fetal development and growth, through improvements in maternal, placental, and fetal antioxidant defense capacities.

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References

  1. Luo ZC, Fraser WD, Julien P, Deal CL, Audibert F, Smith GN, Xiong X, Walker M (2006) Tracing the origins of “fetal origins” of adult diseases: programming by oxidative stress? Med Hypotheses 66:38–44

    Article  CAS  Google Scholar 

  2. Castagné V, Lefèvre K, Natero R, Clarke PG, Bedker DA (1999) An optimal redox status for the survival of axotomized ganglion cells in the developing retina. Neuroscience 93:313–320

    Article  Google Scholar 

  3. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212

    Article  CAS  Google Scholar 

  4. Salas-Vidal E, Lomelí H, Castro-Obregón S, Cuervo R, Escalante-Alcalde D, Covarrubias L (1998) Reactive oxygen species participate in the control of mouse embryonic cell death. Exp Cell Res 238:136–147

    Article  CAS  Google Scholar 

  5. Taylor PD, Poston L (2007) Developmental programming of obesity in mammals. Exp Physiol 92:287–298

    Article  CAS  Google Scholar 

  6. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, Yokoyama M, Honda M, Zen Y, Nakanuma Y, Miyamoto K, Kaneko S (2007) Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46:1392–1403

    Article  CAS  Google Scholar 

  7. Hempstock J, Jauniaux E, Greenwold N, Burton GJ (2003) The contribution of placental oxidative stress to early pregnancy failure. Hum Pathol 34:1265–1275

    Article  CAS  Google Scholar 

  8. White CL, Pistell PJ, Purpera MN, Gupta S, Fernandez-Kim SO, Hise TL, Keller JN, Ingram DK, Morrison CD, Bruce-Keller AJ (2009) Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Neurobiol Dis 35:3–13

    Article  CAS  Google Scholar 

  9. Barker DJ (1995) Fetal origins of coronary heart disease. Br Med J 311:171–174

    Article  CAS  Google Scholar 

  10. Jauniaux E, Greenwold N, Hempstock J, Burton GJ (2003) Comparison of ultrasonographic and Doppler mapping of the intervillous circulation in normal and abnormal early pregnancies. Fertil Steril 79:100–106

    Article  Google Scholar 

  11. Baker DJP, Gluckman PD, Godfrey KM, Harding J, Owens JA, Robinson JS (1993) Fetal nutrition and adult disease. Lancet 341:938–941

    Article  Google Scholar 

  12. Dégen L, Halas V, Tossenberger J, Szab CS, Babinszky L (2009) The impact of dietary fiber and fat levels on total tract digestibility of energy and nutrients in growing pigs and its consequence for diet formulation. Acta Agriculturae Scandinavica 59:150–160

    Article  Google Scholar 

  13. Deuchi K, Kanauchi O, Imasato Y, Kobayashi E (1994) Decreasing effect of chitosan on the apparent fat digestibility by rats fed on a high-fat diet. Biosci Biotech Biochem 58:1613–1616

    Article  CAS  Google Scholar 

  14. Ichikawa H, Shineha R, Satomi S, Sakata T (2002) Gastric or rectal instillation of short-chain fatty acids stimulates epithelial cell proliferation of small and large intestine in rats. Dig Dis Sci 47:1141–1146

    Article  CAS  Google Scholar 

  15. Galisteo M, Duarte J, Zarzuelo A (2008) Effects of dietary fibers on disturbances clustered in the metabolic syndrome. J Nutr Biochem 19:71–84

    Article  CAS  Google Scholar 

  16. Lecumberri E, Goya L, Mateos R, Alía M, Ramos S, Izquierdo-Pulido M, Bravo L (2007) A diet rich in dietary fiber from cocoa improves lipid profile and reduces malondialdehyde in hypercholesterolemic rats. Nutrition 3:332–341

    Article  Google Scholar 

  17. Malville-Shipan K, Fleming SE (1992) Wheat bran and corn oil do not influence proliferation in the colon of healthy rats when energy intakes are equivalent. J Nutr 122:37–45

    CAS  Google Scholar 

  18. Mertens DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. J AOAC Int 85:1217–1240

    CAS  Google Scholar 

  19. Bertuzzi MA, Armada M, Gottifredi JC (2007) Physiochemical characterization of starch based films. J Food Eng 82:17–25

    Article  CAS  Google Scholar 

  20. Hatfield RD (1991) Alfalfa-stempectins: enzymic degradation and structural characterization of a buffer-soluble fraction. Carbohydr Res 212:177–186

    Article  CAS  Google Scholar 

  21. Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34:497–500

    CAS  Google Scholar 

  22. Spitz DR, Oberley LW (1989) An assay for superoxide dismutase activity in mammalian tissue homogenates. Anal Biochem 179:8–18

    Article  CAS  Google Scholar 

  23. Elizabeth K, Rao MNA (1990) Oxygen radical scavenging activity of curcumin. Int J Pharmaceut 58:237–240

    Article  Google Scholar 

  24. Fontana M, Mosca L, Rosei MA (2001) Interaction of enkephalines with oxyradicals. Biochem Pharmacol 61:1253–1257

    Article  CAS  Google Scholar 

  25. Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  26. Jones HN, Woollett LA, Barbour N, Prasad PD, Powell TL, Jansson T (2009) High-fat diet before and during pregnancy causes marked up-regulation of placental nutrient transport and fetal overgrowth in C57/BL6 mice. FASEB J 23:271–278

    Article  CAS  Google Scholar 

  27. Khan IY, Dekou V, Douglas G, Jensen R, Hanson MA, Poston L, Taylor PD (2005) A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol 288:127–133

    Article  Google Scholar 

  28. Oakes ND, Cooney GJ, Camilleri S, Chisholm DJ, Kraegen EW (1997) Mechanisms of liver and muscle insulin resistance induced by chronic high-fat feeding. Diabetes 46:1768–1774

    Article  CAS  Google Scholar 

  29. Han DH, Hansen PA, Host HH, Holloszy JO (1997) Insulin resistance of muscle glucose transport in rats fed a high-fat diet: a reevaluation. Diabetes 46:1761–1767

    Article  CAS  Google Scholar 

  30. Nasr-Esfahani MH, Aitken JR, Johnson MH (1990) Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed invitro or invivo. Development 109:501–507

    CAS  Google Scholar 

  31. Milagro FI, Campión J, Martínez JA (2006) Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity 14:1118–1123

    Article  CAS  Google Scholar 

  32. Ramos S, Moulay L, Granado-Serrano AB, Vilanova O, Muguerza B, Goya L, Bravo L (2008) Hypolipidemic effect in cholesterol-fed rats of a soluble fiber-rich product obtained from cocoa husks. J Agric Food Chem 56:6985–6993

    Article  CAS  Google Scholar 

  33. Granado-Serrano AB, Martín MA, Bravo L, Goya L, Ramos S (2009) A diet rich in cocoa attenuates N-nitrosodiethylamine-induced liver injury in rats. Food Chem Toxicol 47:2499–2506

    Article  CAS  Google Scholar 

  34. Bruce KD, Cagampang FR, Argenton M, Zhang J, Ethirajan PL, Burdge GC, Bateman AC, Clough GF, Poston L, Hanson MA, McConnell JM, Byrne CD (2009) Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50:1796–1808

    Article  CAS  Google Scholar 

  35. Theys N, Bouckenooghe T, Ahn MT, Remacle C, Reusens B (2009) Maternal low-protein diet alters pancreatic islet mitochondrial function in a sex-specific manner in the adult rat. Am J Physiol Regul Integr Comp Physiol 297:1516–1525

    Article  Google Scholar 

  36. Wang J, Sun BG, Cao YP, Song HL, Tian Y (2008) Inhibitory effect of wheat bran feruloyl oligosaccharides on oxidative DNA damage in human lymphocytes. Food Chem 109:129–136

    Article  CAS  Google Scholar 

  37. Abrahamse SL, Pool-Zobel BL, Rechkemmer G (1999) Potential of short chain fatty acids to modulate the induction of DNA damage and changes in the intracellular calcium concentration by oxidative stress in isolated rat distal colon cells. Carcinogenesis 20:629–634

    Article  CAS  Google Scholar 

  38. Ufer C, Wang CC, Borchert A, Heydeck D, Kuhn H (2010) Redox control in mammalian embryo development. Antioxid Redox Signal. [Epub ahead of print]

  39. Wang X, Falcone T, Attaran M, Goldberg JM, Agarwal A, Sharma RK (2002) Vitamin C and vitamin E supplementation reduce oxidative stress–induced embryo toxicity and improve the blastocyst development rate. Fertil Steril 78:1272–1277

    Article  Google Scholar 

  40. Arikan S, Konukoglu D, Arikan C, Akcay T, Davas I (2001) Lipid peroxidation and antioxidant status in maternal and cord blood. Gynecol Obstet Invest 51:145–149

    Article  CAS  Google Scholar 

  41. Liguori A, D’Armiento FP, Palagiano A, Balestrieri ML, Williams-Ignarro S, de Nigris F, Lerman LO, D’Amora M, Rienzo M, Fiorito C, Ignarro LJ, Palinski W, Napoli C (2007) Effect of gestational hypercholesterolaemia on omental vasoreactivity, placental enzyme activity and transplacental passage of normal and oxidised fatty acids. BJOG 114:1547–1556

    Article  CAS  Google Scholar 

  42. Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572:25–30

    CAS  Google Scholar 

  43. Burton GJ, Hempstock J, Jauniaux E (2003) Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 6:84–96

    Article  Google Scholar 

  44. Watson AL, Skepper JN, Jauniaux E, Burton GJ (1998) Susceptibility of human placental syncytiotrophoblast mitochondria to oxygen-mediated damage in relation to gestational age. J Clin Endocrinol Metab 83:1697–1705

    Article  CAS  Google Scholar 

  45. Martyn CN, Barker DJP, Osmond C (1996) Mothers pelvic size, fetal growth and death from stroke in men. Lancet 348:1264–1268

    Article  CAS  Google Scholar 

  46. Huang LE, Arany Z, Livingston DM, Bunn HF (1996) Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 271:32253–32259

    Article  CAS  Google Scholar 

  47. Kozak KR, Abbott B, Hankinson O (1997) ARNT-deficient mice and placental differentiation. Dev Biol 191:297–305

    Article  CAS  Google Scholar 

  48. Bonello S, Zähringer C, BelAiba RS, Djordjevic T, Hess J, Michiels C, Kietzmann T, Görlach A (2007) Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 27:755–761

    Article  CAS  Google Scholar 

  49. Tajima M, Kurashima Y, Sugiyama K, Ogura T, Sakagami H (2009) The redox state of glutathione regulates the hypoxic induction of HIF-1. Eur J Pharmacol 606:45–49

    Article  CAS  Google Scholar 

  50. Isoe T, Makino Y, Mizumoto K, Sakagami H, Fujita Y, Honjo J, Takiyama Y, Itoh H, Haneda M (2010) High glucose activates HIF-1-mediated signal transduction in glomerular mesangial cells through a carbohydrate response element binding protein. Kidney Int 78:48–59

    Article  CAS  Google Scholar 

  51. Reynolds LP, Borowicz PP, Vonnahme KA, Johnson ML, Grazul-Bilska AT, Wallace JM, Caton JS, Redmer DA (2005) Animal models of placental angiogenesis. Placenta 26:689–708

    Article  CAS  Google Scholar 

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Acknowledgments

The present research was supported by the Educational Commission of Sichuan Province of China (09ZB056) and the National Natural Science Foundation of China (31072044). All authors read and approved the final manuscript.

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Correspondence to De Wu.

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Lin, Y., Han, Xf., Fang, Zf. et al. The beneficial effect of fiber supplementation in high- or low-fat diets on fetal development and antioxidant defense capacity in the rat. Eur J Nutr 51, 19–27 (2012). https://doi.org/10.1007/s00394-011-0185-4

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  • DOI: https://doi.org/10.1007/s00394-011-0185-4

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