Diet-induced obesity in female mice leads to peroxidized lipid accumulations and impairment of hippocampal neurogenesis during the early life of their offspring

FASEB Journal

Volumn 23, Issue 6, 2009, Pages 1920-1934

  Tozuka, Yusuke ^a,b,c   Wada, Etsuko ^a,c   Wada, Keiji ^a,c  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b Japan Association for the Advancement of Medical Equipment   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Brain development; Hight fat diet; Lactation; Metabolic abnormalities; Neural progenitor cells; Oxidative stress

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DIVISION; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPUS; HYPERLIPIDEMIA; LACTATION; LIPID DIET; LIPID PEROXIDATION; LIPID STORAGE; MALE; MATING; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; OBESITY; POSTNATAL DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; PROGENY; PULSE RATE; STEM CELL; SUCKLING; ADULT; ANIMAL; BODY WEIGHT; C57BL MOUSE; CYTOLOGY; DIET; EATING; FAT INTAKE; GLUCOSE TOLERANCE TEST; HUMAN; METABOLISM; PHYSIOLOGY;

ANIMALIA; MUS;

ADULT; ANIMALS; BODY WEIGHT; DIET; DIETARY FATS; EATING; FEMALE; GLUCOSE TOLERANCE TEST; HIPPOCAMPUS; HUMANS; LIPID PEROXIDATION; MICE; MICE, INBRED C57BL; NEUROGENESIS; OBESITY; PREGNANCY; STEM CELLS; YOUNG ADULT;

EID: 67649306717     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-124784     Document Type: Article

References (77)

1. Kopelman, P. G. (2006) Obesity as a medical problem. Nature 404, 635-643
2. Mokdad, A. H., Ford, E. S., Bowman, B. A., Dietz, W. H., Vinicor, F., Bales, V. S., and Marks, J. S. (2003) Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001 JAMA 289, 76-79 (Pubitemid 36026281)
3. Ogden, C. L., Carroll, M. D., Curtin, L. R., McDowell, M. A., Tabak, C. J., and Flegal, K. M. (2006) Prevalence of overweight and obesity in the United States, 1999-2004. JAMA 295, 1549-1555
4. Naeye, R. L. (1990) Maternal body weight and pregnancy outcome. Am. J. Clin. Nutr. 52, 273-279 (Pubitemid 20227824)
5. Srinivasan, M., Katewa, S. D., Palaniyappan, A., Pandya, J. D., and Patel, M. S. (2006) Maternal high-fat diet consumption results in fetal malprogramming predisposing to the onset of metabolic syndrome-like phenotype in adulthood. Am. J. Physiol. Endocrinol. Metab. 291, 792-799 (Pubitemid 44484922)
6. Samuelsson, A. M., Matthews, P. A., Argenton, M., Christie, M. R., McConnell, J. M., Jansen, E. H. J., Piersma, A. H., Ozanne, S. E., Twinn, D. F., Remacle, C., Rowlerson, A., Poston, L., and Taylor, P. D. (2008) Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: A novel murine model of developmental programming. Hypertension 51, 383-392 (Pubitemid 351159954)
7. Shankar, K., Harrell, A., Liu, X., Gilchrist, J. M., Ronis, M. J., and Badger, T. M. (2008) Maternal obesity at conception programs obesity in the offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, 528-538 (Pubitemid 351213759)
8. Chang, G. Q., Gaysinskaya, V., Karatayev, O., and Leibowitz, S. F. (2008) Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J. Neurosci. 28, 12107-12119
9. Férézou-Viala, J., Roy, A. F., Sérougne, C., Gripois, D., Parquet, M., Bailleux, V., Gertler, A., Delplanque, B., Djiane, J., Riottot, M., and Tauis, M. (2007) Long-term consequences of maternal high-fat feeding on hypothalamic leptin sensitivity and diet-induced obesity in the offspring. Am. J. Physiol. Regul. Comp. Physiol. 293, 1056-1062 (Pubitemid 47358924)
10. Muhlhausler, B. S., Adam, C. L., Findlay, P. A., Duffield, J. A., and McMillen, I. C. (2006) Increased maternal nutrition alters development of the appetite-regulating network in the brain. FASEB J. 20, 556-565
11. Wu, A., Ying, Z., and Gomez-Pinilla, F. (2004) The interplay between oxidative stress and brain-derived neurotrophic factor modulates the outcome of a saturated fat diet on synaptic plasticity and cognition. Eur. J. Neurosci. 19, 1699-1707 (Pubitemid 38482558)
12. Stranahan, A. M., Norman, E. D., Lee, K., Cutler, R. G., Telljohann, R. S., Egan, J. M., and Mattson, M. P. (2008) Diet-induced insulin resistance impairs hippocampal synaptic plasticity and cognition in middle-aged rats. Hippocampus 18, 1085-1088
13. Nicholas, K. R., and Hartmann, P. E. (1991) Milk secretion in the rat: progressive changes in milk composition during lactation and weaning and the effect of diet. Comp. Biochem. Physiol. A 98, 535-542
14. Del Prado, M., Delgado, G., and Villalpando, S. (1997) Maternal lipid intake during pregnancy and lactation alters milk composition and production and litter growth in rats. J. Nutr. 127, 458-462 (Pubitemid 27120000)
15. Trottier, G., Koski, K. G., Brun, T., Toufexis, D. J., Richard, D., and Walker, C. D. (1998) Increased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: a possible role for leptin. Endocrinology 139, 3704-3711 (Pubitemid 28512248)
16. Jones, H. N., Woollett, L. A., Barbour, N., Prasad, P. D., Powell, T. L., and Jansson, T. (2008) 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
17. Liu, D., Diorio, J., Day, J. C., Francis, D. D., and Meaney, M. J. (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799-806 (Pubitemid 30485705)
18. Lee, H. H., Kim, H., Lee, J. W., Kim, Y. S., Yang, H. Y., Chang, H. K., Lee, T. H., Shin, M. C., Lee, M. H., Shin, M. S., Park, S., Baek, S., and Kim, C. J. (2006) Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain Dev. 28, 147-154 (Pubitemid 43326233)
19. Yang, J., Han, H., Cao, J., Li, L., and Xu, L. (2006) Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16, 431-436 (Pubitemid 44712066)
20. Gould, E., and Gross, C. G. (2002) Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619-623 (Pubitemid 34141740)
21. Ming, G. L., and Song, H. (2005) Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223-250 (Pubitemid 41098905)
22. Fukuda, S., Kato, F., Tozuka, Y., Yamaguchi, M., Miyamoto, Y., and Hisatsune, T. (2003) Two distinct subpopulations of nestin-positive cells in adult mouse dentate gyrus. J. Neurosci. 23, 9357-9366 (Pubitemid 37323035)
23. Tozuka, Y., Fukuda, S., Namba, T., Seki, T., and Hisatsune, T. (2005) GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47, 803-815 (Pubitemid 41266948)
24. Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T., and Gould, E. (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410, 372-376 (Pubitemid 32246054)
25. Saxe, M. D., Battaglia, F., Wang, J. W., Malleret, G., David, D. J., Monckton, J. E., Garcia, A. D., Sofroniew, M. V., Kandel, E. R., Santarelli, L., Hen, R., and Drew, M. R. (2006) Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc. Natl. Acad. Sci. U. S. A. 103, 17501-17506 (Pubitemid 44788998)
26. Glenn, M. J., Gibson, E. M., Kirby, E. D., Mellott, T. J., Blusztajn, J. K., and Williams, C. L. (2007) Prenatal choline availability modulates hippocampal neurogenesis and neurogenic responses to enriching experiences in adult female rats. Eur. J. Neurosci. 25, 2473-2482
27. Zhang, C. L., Zou, Y., He, W., Gage, F. H., and Evans, R. M. (2008) A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007 (Pubitemid 351301727)
28. Wong-Goodrich, S. J., Glenn, M. J., Mellott, T. J., Blusztajn, J. K., Meck, W. H., and Williams, C. L. (2008) Spatial memory and hippocampal plasticity are differentially sensitive to the availability of choline in adulthood as a function of choline supply in utero. Brain Res. 1237, 153-166
29. Dupret, D., Revest, J. M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., Abrous, D. N., and Piazza, P. V. (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3, 1-14 (Pubitemid 351984392)
30. Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S., and Kageyama, R. (2008) Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain. Nat. Neurosci. 11, 1153-1161
31. Farioli-Vecchioli, S., Saraulli, D., Costanzi, M., Pacioni, S., Cinà, I., Aceti, M., Micheli, L., Bacci, A., Cestari, V., and Tirone, F. (2008) The timing of differentiation of adult hippocampal neurons is crucial for spatial memory. PLoS Biol. 6, 2188-2204
32. Craciunescu, C. N., Albright, C. D., Mar, M. H., Song, J., and Zeisel, S. H. (2003) Choline availability during embryonic development alters progenitor cell mitosis in developing mouse hippocampus. J. Nutr. 133, 3614-3618 (Pubitemid 37409496)
33. Wong-Goodrich, S. J., Mellott, T. J., Glenn, M. J., Blusztajn, J. K., and Williams, C. L. (2008) Prenatal choline supplementation attenuates neuropathological response to status epilepticus in the adult rat hippocampus. Neurobiol. Dis. 30, 255-269
34. Mirescu, C., Peters, J. D., and Gould, E. (2004) Early life experience alters response of adult neurogenesis to stress. Nat. Neurosci. 7, 841-846 (Pubitemid 38989507)
35. Bick-Sander, A., Steiner, B., Wolf, S. A., Babu, H., and Kempermann, G. (2006) Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. Proc. Natl. Acad. Sci. U. S. A. 103, 3852-3857 (Pubitemid 43376644)
36. Lindqvist, A., Mohapel, P., Bouter, B., Frielingsdorf, H., Pizzo, D., Brundin, P., and Erlanson-Albertsson, C. (2006) High-fat diet impairs hippocampal neurogenesis in male rats. Eur. J. Neurol. 13, 1385-1388 (Pubitemid 44736653)
37. Stranahan, A. M., Arumugam, T. V., Cutler, R. G., Lee, K., Egan, J. M., and Mattson, M. P. (2008) Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat. Neurosci. 11, 309-317 (Pubitemid 351311802)
38. Zhang, W. J., Tan, Y. F., Yue, J. T., Vranic, M., and Wojtowicz, J. M. (2008) Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats. Acta Neurol. Scand. 117, 205-210 (Pubitemid 351190151)
39. Oike, Y., Akao, M., Yasunaga, K., Yamauchi, T., Morisada, T., Ito, Y., Urano, T., Kimura, Y., Kubota, Y., Maekawa, H., Miyamoto, T., Miyata, K., Matsumoto, S., Sakai, J., Nakagata, N., Takeya, M., Koseki, H., Ogawa, Y., Kadowaki, T., and Suda, T. (2005) Angiopoietin-related growth factor antagonizes obesity and insulin resistance. Nat. Med. 11, 400-408 (Pubitemid 40562330)
40. Chapman, R. H., and Stern, J. M. (1979) Failure of severe maternal stress or ACTH during pregnancy to affect emotionality of male rat offspring: implications of litter effects for prenatal studies. Dev. Psychobiol. 12, 255-267
41. Vallée, M., MacCari, S., Dellu, F., Simon, H., Le Moal, M., and Mayo, W. (1999) Long-term effects of prenatal stress and postnatal handling on age-related glucocorticoid secretion and cognitive performance: a longitudinal study in the rat. Eur. J. Neurosci. 11, 2906-2916 (Pubitemid 29364207)
42. Ohki-Hamazaki, H., Watase, K., Yamamoto, K., Ogura, H., Yamano, M., Yamada, K., Maeno, H., Imaki, J., Kikuyama, S., Wada, E., and Wada, K. (1997) Mice lacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390, 165-169 (Pubitemid 27507984)
43. Tanaka, Y., Tozuka, Y., Takata, T., Shimazu, N., Matsumura, N., Ohta, A., and Hisatsune, T. (2008) Excitatory GABAergic activation of cortical dividing glial cells. [E-pub ahead of print] Cereb. Cortex doi: 10.1093/cercor/bhn238
44. Nixon, K., and Crews, F. T. (2004) Temporally specific burst in cell proliferation increases hippocampal neurogenesis in protracted abstinence from alcohol. J. Neurosci. 24, 9714-9722 (Pubitemid 39441527)
45. Suh, H., Consiglio, A., Ray, J., Sawai, T., D'Amour, K. A., and Gage, F. H. (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1, 515-528 (Pubitemid 350056408)
46. Kabuta, T., Suzuki, Y., and Wada, K. (2006) Degradation of amyotrophic lateral sclerosis-linked mutant Cu,Zn-superoxide dismutase proteins by macroautophagy and the proteasome. J. Biol. Chem. 281, 30524-30533 (Pubitemid 44582109)
47. Nishimoto, M., Furuta, A., Aoki, S., Kudo, Y., Miyakawa, H., and Wada, K. (2007) PACAP/PAC1 autocrine system promotes proliferation and astrogenesis in neural progenitor cells. Glia 55, 317-327 (Pubitemid 46225964)
48. Yamato, M., Shiba, T., Yoshida, M., Ide, T., Seri, N., Kudou, W., Kinugawa, S., and Tsutsui, H. (2007) Fatty acids increase the circulating levels of oxidative stress factors in mice with diet-induced obesity via redox changes of albumin. FEBS. J. 274, 3855-3863 (Pubitemid 47087670)
49. Yamaguchi, Y., Yoshikawa, N., Kagota, S., Nakamura, K., Haginaka, J., and Kunitomo, M. (2006) Elevated circulating levels of markers of oxidative-nitrative stress and inflammation in a genetic rat model of metabolic syndrome. Nitric Oxide 15, 380-386
50. Maekawa, M., Takashima, N., Arai, Y., Nomura, T., Inokuchi, K., Yuasa, S., and Osumi, N. (2005) Pax6 is required for production and maintenance of progenitor cells in postnatal hippocampal neurogenesis. Genes Cells 10, 1001-1014 (Pubitemid 41404009)
51. Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997) More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495 (Pubitemid 27164074)
52. Cerf, M. E., Williams, K., Nkomo, X. I., Muller, C. J., Du-Toit, D. F., Louw, J., and Wolfe-Coote, S. A. (2005) Islet cell response in the neonatal rat after exposure to a high-fat diet during pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, 1122-1128 (Pubitemid 40593694)
53. Yogman, M. W., and Zeisel, S. H. (1985) Nutrients, neurotransmitters and infant behavior. Am. J. Clin. Nutr. 42, 352-360
54. Jones, H. N., Powell, T. L., and Jansson, T. (2007) Regulation of placental nutrient transport - a review. Placenta 28, 763-774
55. Innis, S. M. (2005) Essential fatty acid transfer and fetal development. Placenta 26, 70-75
56. Cetin, I., and Koletzko, B. (2008) Long-chain omega-3 fatty acid supply in pregnancy and lactation. Curr. Opin. Clin. Nutr. Metab. Care 11, 297-302
57. Da Costa, T. H., and Williamson, D. H. (1993) Effects of exogenous insulin or vanadate on disposal of dietary triacylglycerols between mammary gland and adipose tissue in the lactating rat: insulin resistance in white adipose tissue. Biochem. J. 290, 557-561
58. Woollett, L. A. (2005) Maternal cholesterol in fetal development: transport of cholesterol from the maternal to the fetal circulation. Am. J. Clin. Nutr. 82, 1155-1161 (Pubitemid 43779712)
59. Sarafidis, P. A., and Bakris, G. L. (2007) Non-esterified fatty acids and blood pressure elevation: a mechanism for hypertension in subjects with obesity/insulin resistance? J. Hum. Hypertens. 21, 12-19
60. Tripathy, D., Mohanty, P., Dhindsa, S., Syed, T., Ghanim, H., Aljada, A., and Dandona, P. (2003) Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 52, 2882-2887 (Pubitemid 37466856)
61. Madsen, T. M., Kristjansen, P. E., Bolwig, T. G., and Wörtwein, G. (2003) Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119, 635-642
62. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S. R., Morhardt, D. R., and Fike, J. R. (2004) Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol. 188, 316-330 (Pubitemid 38891593)
63. Limoli, C. L., Giedzinski, E., Rola, R., Otsuka, S., Palmer, T. D., and Fike, J. R. (2004) Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat. Res. 161, 17-27 (Pubitemid 38018720)
64. Giedzinski, E., Rola, R., Fike, J. R., and Limoli, C. L. (2005) Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons. Radiat. Res. 164, 540-544 (Pubitemid 41368933)
65. Herrera, D. G., Yague, A. G., Johnsen-Soriano, S., Bosch-Morell, F., Collado-Morente, L., Muriach, M., Romero, F. J., and Garcia- Verdugo, J. M. (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc. Natl. Acad. Sci. U. S. A. 100, 7919-7924
66. Sun, A. Y., and Sun, G. Y. (2001) Ethanol and oxidative mechanisms in the brain. J. Biomed. Sci. 8, 37-43
67. Sava, V., Velasquez, A., Song, S., and Sanchez-Ramos, J. (2007) Adult hippocampal neural stem/progenitor cells in vitro are vulnerable to the mycotoxin ochratoxin-A. Toxicol. Sci. 98, 187-197 (Pubitemid 47073831)
68. Manganas, L. N., Zhang, X., Li, Y., Hazel, R. D., Smith, S. D., Wagshul, M. E., Henn, F., Benveniste, H., Djuric, P. M., Enikolopov, G., and Maletic-Savatic, M. (2007) Magnetic resonance spectroscopy identifies neural progenitor cells in the live human brain. Science 318, 980-985 (Pubitemid 350098995)
69. Cameron, H. A., and Gould, E. (1994) Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209
70. Casolini, P., Domenici, M. R., Cinque, C., Alemà, G.S., Chiodi, V., Galluzzo, M., Musumeci, M., Mairesse, J., Zuena, A. R., Matteucci, P., Marano, G., Maccari, S., Nicoletti, F., and Catalani, A. (2007) Maternal exposure to low levels of corticosterone during lactation protects the adult offspring against ischemic brain damage. J. Neurosci. 27, 7041-7046 (Pubitemid 47015896)
71. Chan, O., Chan, S., Inouye, K., Vranic, M., and Matthews, S. G. (2001) Molecular regulation of the hypothalamo-pituitary-adrenal axis in streptozotocin-induced diabetes: effects of insulin treatment. Endocrinology 142, 4872-4879 (Pubitemid 33022363)
72. Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001) Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. J. Neurophysiol. 85, 2423-2431 (Pubitemid 32525520)
73. Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004) Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature 429, 184-187 (Pubitemid 38656194)
74. Bergami, M., Rimondini, R., Santi, S., Blum, R., Götz, M., and Canossa, M. (2008) Deletion of TrkB in adult progenitors alters newborn neuron integration into hippocampal circuits and increases anxiety-like behavior. Proc. Natl. Acad. Sci. U. S. A. 105, 15570-15575
75. Andersen, R. E. (2000) The spread of the childhood obesity epidemic. CMAJ 163, 1461-1462
76. Mohn, A., Catino, M., Capanna, R., Giannini, C., Marcovecchio, M., and Chiarelli, F. (2005) Increased oxidative stress in prepubertal severely obese children: effect of a dietary restriction-weight loss program. J. Clin. Endocrinol. Metab. 90, 2653-2658 (Pubitemid 40686305)
77. Cserjési, R., Molnár, D., Luminet, O., and Lénárd, L. (2007) Is there any relationship between obesity and mental flexibility in children?. Appetite 49, 675-678