Progress in Research on Brain Development and Function of Mice During Weaning

Page: [705 - 712] Pages: 8

  • * (Excluding Mailing and Handling)

Abstract

Lactation is a critical phase for brain function development. New dietary experiences of mouse caused by weaning can regulate brain development and function, increase their response to food and environment, and eventually give rise to corresponding behavioral changes. Changes in weaning time induce the alteration of brain tissues morphology and molecular characteristics, glial cell activity and behaviors in the offspring. In addition, it is also sensitive to the intervention of environment and drugs during this period. That is to say, the study focused on brain development and function based on mouse weaning is critical to demonstrate the underlying pathogenesis of neuropsychiatric diseases and find new drug targets. This article mainly focuses on the developmental differentiation of the brain during lactation, especially during weaning in mice.

Keywords: Wean, brain development, behavioral changes, neuron, glial cell, lactation.

Graphical Abstract

[1]
Song, P.; Zhang, R.; Wang, X.; He, P.; Tan, L.; Ma, X. Dietary grape-seed procyanidins decreased postweaning diarrhea by modulating intestinal permeability and suppressing oxidative stress in rats. J. Agric. Food Chem., 2011, 59(11), 6227-6232.
[2]
Gracia-Rubio, I.; Moscoso-Castro, M.; Pozo, O.J.; Marcos, J.; Nadal, R.; Valverde, O. Maternal separation induces neuroinflammation and long-lasting emotional alterations in mice. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2016, 65, 104-117.
[3]
Nakamura, K.; Kikusui, T.; Takeuchi, Y.; Mori, Y. The influence of early weaning on aggressive behavior in mice. J. Vet. Med. Sci., 2003, 65(12), 1347-1349.
[4]
Curley, J.P.; Jordan, E.R.; Swaney, W.T.; Izraelit, A.; Kammel, S.; Champagne, F.A. The meaning of weaning: Influence of the weaning period on behavioral development in mice. Dev. Neurosci., 2009, 31(4), 318-331.
[5]
Gottlieb, A.; Keydar, I.; Epstein, H.T. Rodent brain growth stages: An analytical review. Biol. Neonate, 1977, 32(3-4), 166-176.
[6]
Murakami, T.; Ohtsuka, A.; Taguchi, T.; Piao, D.X. Perineuronal sulfated proteoglycans and dark neurons in the brain and spinal cord: A histochemical and electron microscopic study of newborn and adult mice. Arch. Histol. Cytol., 1995, 58(5), 557-565.
[7]
Kikusui, T.; Kiyokawa, Y.; Mori, Y. Deprivation of mother-pup interaction by early weaning alters myelin formation in male, but not female, ICR mice. Brain Res., 2007, 1133(1), 115-122.
[8]
Duque, A.; Coman, D.; Carlyle, B.C.; Bordner, K.A.; George, E.D.; Papademetris, X.; Hyder, F.; Simen, A.A. Neuroanatomical changes in a mouse model of early life neglect. Brain Struct. Funct., 2012, 217(2), 459-472.
[9]
Kikusui, T.; Ichikawa, S.; Mori, Y. Maternal deprivation by early weaning increases corticosterone and decreases hippocampal BDNF and neurogenesis in mice. Psychoneuroendocrinology, 2009, 34(5), 762-772.
[10]
Han, M.; Wang, C.; Liu, P.; Li, D.; Li, Y.; Ma, X. Dietary fiber gap and host gut microbiota. Protein Pept. Lett., 2017, 24(5), 388-396.
[11]
Demotes-Mainard, J.; Henry, C.; Jeantet, Y.; Arsaut, J.; Arnauld, E. Postnatal ontogeny of dopamine D3 receptors in the mouse brain: Autoradiographic evidence for a transient cortical expression. Brain Res. Dev. Brain Res., 1996, 94(2), 166-174.
[12]
Nakamura, K.; Kikusui, T.; Takeuchi, Y.; Mori, Y. Changes in social instigation- and food restriction-induced aggressive behaviors and hippocampal 5HT1B mRNA receptor expression in male mice from early weaning. Behav. Brain Res., 2008, 187(2), 442-448.
[13]
Pellerin, L.; Pellegri, G.; Martin, J.L.; Magistretti, P.J. Expression of monocarboxylate transporter mRNAs in mouse brain: Support for a distinct role of lactate as an energy substrate for the neonatal vs. adult brain. Proc. Natl. Acad. Sci. USA, 1998, 95(7), 3990-3995.
[14]
Bayer, S.A. Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J. Comp. Neurol., 1980, 190(1), 115-134.
[15]
Hodge, R.D.; Kowalczyk, T.D.; Wolf, S.A.; Encinas, J.M.; Rippey, C.; Enikolopov, G.; Kempermann, G.; Hevner, R.F. Intermediate progenitors in adult hippocampal neurogenesis: Tbr2 expression and coordinate regulation of neuronal output. J. Neurosci., 2008, 28(14), 3707-3717.
[16]
Tanaka, T.; Abe, H.; Kimura, M.; Onda, N.; Mizukami, S.; Yoshida, T.; Shibutani, M. Developmental exposure to T-2 toxin reversibly affects postnatal hippocampal neurogenesis and reduces neural stem cells and progenitor cells in mice. Arch. Toxicol., 2016, 90(8), 2009-2024.
[17]
Clarke, G.; Grenham, S.; Scully, P.; Fitzgerald, P.; Moloney, R.D.; Shanahan, F.; Dinan, T.G.; Cryan, J.F. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. Mol. Psychiatry, 2013, 18(6), 666-673.
[18]
Neufeld, K.M.; Kang, N.; Bienenstock, J.; Foster, J.A. Reduced anxiety-like behavior and central neurochemical change in germ-free mice., Neurogastroenterol. Motil.,. 2011, 23(3), 255-264, e119..
[19]
Nishie, H.; Miyata, R.; Fujikawa, R.; Kinoshita, K.; Muroi, Y.; Ishii, T. Post-weaning mice fed exclusively milk have deficits in induction of long-term depression in the CA1 hippocampal region and spatial learning and memory. Neurosci. Res., 2012, 73(4), 292-301.
[20]
Cheng, Y.; Gidday, J.M.; Yan, Q.; Shah, A.R.; Holtzman, D.M. Marked age-dependent neuroprotection by brain-derived neurotrophic factor against neonatal hypoxic-ischemic brain injury. Ann. Neurol., 1997, 41(4), 521-529.
[21]
Levine, E.S.; Dreyfus, C.F.; Black, I.B.; Plummer, M.R. Differential effects of NGF and BDNF on voltage-gated calcium currents in embryonic basal forebrain neurons. J. Neurosci., 1995, 15(4), 3084-3091.
[22]
Mogi, K.; Ishida, Y.; Nagasawa, M.; Kikusui, T. Early weaning impairs fear extinction and decreases brain-derived neurotrophic factor expression in the prefrontal cortex of adult male C57BL/6 mice. Dev. Psychobiol., 2016, 58(8), 1034-1042.
[23]
Gorski, J.A.; Zeiler, S.R.; Tamowski, S.; Jones, K.R. Brain-derived neurotrophic factor is required for the maintenance of cortical dendrites. J. Neurosci., 2003, 23(17), 6856-6865.
[24]
Maeda, N.; Kawakami, S.; Ohmoto, M.; le Coutre, J.; Vinyes-Pares, G.; Arigoni, F.; Okada, S.; Abe, K.; Aizawa, H.; Misaka, T. Differential expression analysis throughout the weaning period in the mouse cerebral cortex. Biochem. Biophys. Res. Commun., 2013, 431(3), 437-443.
[25]
De Pietri, T.D.; Pulvers, J.N.; Haffner, C.; Murchison, E.P.; Hannon, G.J.; Huttner, W.B. miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development, 2008, 135(23), 3911-3921.
[26]
Murofushi, W.; Mori, K.; Murata, K.; Yamaguchi, M. Functional development of olfactory tubercle domains during weaning period in mice. Sci. Rep., 2018, 8(1), 13204.
[27]
Motoike, T.; Skach, A.G.; Godwin, J.K.; Sinton, C.M.; Yamazaki, M.; Abe, M.; Natsume, R.; Sakimura, K.; Yanagisawa, M. Transient expression of neuropeptide W in postnatal mouse hypothalamus--a putative regulator of energy homeostasis. Neuroscience, 2015, 301, 323-337.
[28]
Bordner, K.A.; George, E.D.; Carlyle, B.C.; Duque, A.; Kitchen, R.R.; Lam, T.T.; Colangelo, C.M.; Stone, K.L.; Abbott, T.B.; Mane, S.M.; Nairn, A.C.; Simen, A.A. Functional genomic and proteomic analysis reveals disruption of myelin-related genes and translation in a mouse model of early life neglect. Front. Psychiatry, 2011, 2, 18.
[29]
Ono, M.; Kikusui, T.; Sasaki, N.; Ichikawa, M.; Mori, Y.; Murakami-Murofushi, K. Early weaning induces anxiety and precocious myelination in the anterior part of the basolateral amygdala of male Balb/c mice. Neuroscience, 2008, 156(4), 1103-1110.
[30]
Kodama, Y.; Kikusui, T.; Takeuchi, Y.; Mori, Y. Effects of early weaning on anxiety and prefrontal cortical and hippocampal myelination in male and female Wistar rats. Dev. Psychobiol., 2008, 50(4), 332-342.
[31]
Fujikura, K.; Setsu, T.; Tanigaki, K.; Abe, T.; Kiyonari, H.; Terashima, T.; Sakisaka, T. Kif14 mutation causes severe brain malformation and hypomyelination. PLoS One, 2013, 8(1)e53490
[32]
Haque, Z.U.; Mozaffar, Z. Importance of dietary cholesterol for the maturation of mouse brain myelin. Biosci. Biotechnol. Biochem., 1992, 56(8), 1351-1354.
[33]
Ma, N.; Guo, P.; Zhang, J.; He, T.; Kim, S.W.; Zhang, G.; Ma, X. Nutrients mediate intestinal bacteria-mucosal immune crosstalk. Front. Immunol., 2018, 9, 5.
[34]
Du, K.; Wang, C.; Liu, P.; Li, Y.; Ma, X. Effects of dietary mycotoxins on gut microbiome. Protein Pept. Lett., 2017, 24(5), 397-405.
[35]
Hoban, A.E.; Stilling, R.M.; Ryan, F.J.; Shanahan, F.; Dinan, T.G.; Claesson, M.J.; Clarke, G.; Cryan, J.F. Regulation of prefrontal cortex myelination by the microbiota. Transl. Psychiatry, 2016, 6e774
[36]
Kabouridis, P.S.; Lasrado, R.; McCallum, S.; Chng, S.H.; Snippert, H.J.; Clevers, H.; Pettersson, S.; Pachnis, V. Microbiota controls the homeostasis of glial cells in the gut lamina propria. Neuron, 2015, 85(2), 289-295.
[37]
Yamashita, T.; Wu, Y.P.; Sandhoff, R.; Werth, N.; Mizukami, H.; Ellis, J.M.; Dupree, J.L.; Geyer, R.; Sandhoff, K.; Proia, R.L. Interruption of ganglioside synthesis produces central nervous system degeneration and altered axon-glial interactions. Proc. Natl. Acad. Sci. USA, 2005, 102(8), 2725-2730.
[38]
Partadiredja, G.; Simpson, R.; Bedi, K.S. The effects of pre-weaning undernutrition on the expression levels of free radical deactivating enzymes in the mouse brain. Nutr. Neurosci., 2005, 8(3), 183-193.
[39]
Dutra-Tavares, A.C.; Silva, J.O.; Nunes-Freitas, A.L.; Guimaraes, V.; Araujo, U.C.; Conceicao, E. Moura, E.G.; Lisboa, P.C.; Filgueiras, C.C.; Manhaes, A.C.; Abreu-Villaca, Y.; Ribeiro-Carvalho, A. Maternal undernutrition during lactation alters nicotine reward and DOPAC/dopamine ratio in cerebral cortex in adolescent mice, but does not affect nicotine-induced nAChRs upregulation. Int. J. Dev. Neurosci., 2018, 65, 45-53.
[40]
Sadagurski, M.; Landeryou, T.; Cady, G.; Bartke, A.; Bernal-Mizrachi, E.; Miller, R.A. Transient early food restriction leads to hypothalamic changes in the long-lived crowded litter female mice. Physiol. Rep., 2015, 3(4)e12379
[41]
Langie, S.A.; Achterfeldt, S.; Gorniak, J.P.; Halley-Hogg, K.J.; Oxley, D.; van Schooten, F.J.; Godschalk, R.W.; McKay, J.A.; Mathers, J.C. Maternal folate depletion and high-fat feeding from weaning affects DNA methylation and DNA repair in brain of adult offspring. FASEB J., 2013, 27(8), 3323-3334.
[42]
Li, N.; Qiao, M.; Zhao, Q.; Zhang, P.; Song, L.; Li, L.; Cui, C. Effects of maternal lead exposure on RGMa and RGMb expression in the hippocampus and cerebral cortex of mouse pups. Brain Res. Bull., 2016, 127, 38-46.
[43]
Li, N.; Li, X.; Li, L.; Zhang, P.; Qiao, M.; Zhao, Q.; Song, L.; Yu, Z. Original Research: The expression of MMP2 and MMP9 in the hippocampus and cerebral cortex of newborn mice under maternal lead exposure. Exp. Biol. Med., (Maywood), 2016, 241(16), 1811-1818.
[44]
Li, N.; Zhang, P.; Qiao, M.; Shao, J.; Li, H.; Xie, W. The effects of early life lead exposure on the expression of P2X7 receptor and synaptophysin in the hippocampus of mouse pups. J. Trace Elem. Med. Biol., 2015, 30, 124-128.
[45]
Sanchez-Martin, F.J.; Lindquist, D.M.; Landero-Figueroa, J.; Zhang, X.; Chen, J.; Cecil, K.M.; Medvedovic, M.; Puga, A. Sex- and tissue-specific methylome changes in brains of mice perinatally exposed to lead. Neurotoxicology, 2015, 46, 92-100.
[46]
Horii-Hayashi, N.; Sasagawa, T.; Matsunaga, W.; Matsusue, Y.; Azuma, C.; Nishi, M. Developmental changes in desensitisation of c-Fos expression induced by repeated maternal separation in pre-weaned mice. J. Neuroendocrinol., 2013, 25(2), 158-167.
[47]
Heiderstadt, K.M.; Vandenbergh, D.J.; Gyekis, J.P.; Blizard, D.A. Communal nesting increases pup growth but has limited effects on adult behavior and neurophysiology in inbred mice. J. Am. Assoc. Lab. Anim. Sci., 2014, 53(2), 152-160.
[48]
Branchi, I.; D’Andrea, I.; Cirulli, F.; Lipp, H.P.; Alleva, E. Shaping brain development: mouse communal nesting blunts adult neuroendocrine and behavioral response to social stress and modifies chronic antidepressant treatment outcome. Psychoneuroendocrinology, 2010, 35(5), 743-751.
[49]
Branchi, I.; D’Andrea, I.; Fiore, M.; Di Fausto, V.; Aloe, L.; Alleva, E. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol. Psychiatry, 2006, 60(7), 690-696.
[50]
Oddi, D.; Subashi, E.; Middei, S.; Bellocchio, L.; Lemaire-Mayo, V.; Guzman, M.; Crusio, W.E.; D’Amato, F.R.; Pietropaolo, S. Early social enrichment rescues adult behavioral and brain abnormalities in a mouse model of fragile X syndrome. Neuropsychopharmacology, 2015, 40(5), 1113-1122.
[51]
Takai, Y.; Kawai, M.; Ogo, T.; Ichinose, T.; Furuya, S.; Takaki, N.; Tone, Y.; Udo, H.; Furuse, M.; Yasuo, S. Early-life Photoperiod influences depression-like behavior, prepulse inhibition of the acoustic startle response, and hippocampal astrogenesis in mice. Neuroscience, 2018, 374, 133-143.
[52]
Benner, S.; Endo, T.; Endo, N.; Kakeyama, M.; Tohyama, C. Early deprivation induces competitive subordinance in C57BL/6 male mice. Physiol. Behav., 2014, 137, 42-52.
[53]
Zhang, L.F.; Shi, L.; Liu, H.; Meng, F.T.; Liu, Y.J.; Wu, H.M.; Du, X.; Zhou, J.N. Increased hippocampal tau phosphorylation and axonal mitochondrial transport in a mouse model of chronic stress. Int. J. Neuropsychopharmacol., 2012, 15(3), 337-348.
[54]
D’Amato, F.R.; Zanettini, C.; Sgobio, C.; Sarli, C.; Carone, V.; Moles, A.; Ammassari-Teule, M. Intensification of maternal care by double-mothering boosts cognitive function and hippocampal morphology in the adult offspring. Hippocampus, 2011, 21(3), 298-308.
[55]
Simonetti, T.; Lee, H.; Bourke, M.; Leamey, C.A.; Sawatari, A. Enrichment from birth accelerates the functional and cellular development of a motor control area in the mouse. PLoS One, 2009, 4(8)e6780
[56]
Branchi, I.; D’Andrea, I.; Sietzema, J.; Fiore, M.; Di Fausto, V.; Aloe, L.; Alleva, E. Early social enrichment augments adult hippocampal BDNF levels and survival of BrdU-positive cells while increasing anxiety- and “depression”-like behavior. J. Neurosci. Res., 2006, 83(6), 965-973.
[57]
Fan, C.; Fu, H.; Dong, H.; Lu, Y.; Lu, Y.; Qi, K. Maternal n-3 polyunsaturated fatty acid deprivation during pregnancy and lactation affects neurogenesis and apoptosis in adult offspring: Associated with DNA methylation of brain-derived neurotrophic factor transcripts. Nutr. Res., 2016, 36(9), 1013-1021.
[58]
Woronowicz, A.; Cawley, N.X.; Peng, L.Y. Carbamazepine prevents hippocampal neurodegeneration in mice lacking the neuroprotective protein, carboxypetidase E. Clin. Pharmacol. Biopharm., 2012(Suppl. 1), 2.
[59]
Bouayed, J.; Desor, F.; Rammal, H.; Kiemer, A.K.; Tybl, E.; Schroeder, H.; Rychen, G.; Soulimani, R. Effects of lactational exposure to benzo[alpha]pyrene (B[alpha]P) on postnatal neurodevelopment, neuronal receptor gene expression and behaviour in mice. Toxicology, 2009, 259(3), 97-106.
[60]
Tozuka, Y.; Kumon, M.; Wada, E.; Onodera, M.; Mochizuki, H.; Wada, K. Maternal obesity impairs hippocampal BDNF production and spatial learning performance in young mouse offspring. Neurochem. Int., 2010, 57(3), 235-247.
[61]
Li, N.; Liu, F.; Song, L.; Zhang, P.; Qiao, M.; Zhao, Q.; Li, W. The effects of early life Pb exposure on the expression of IL1-beta, TNF-alpha and Abeta in cerebral cortex of mouse pups. J. Trace Elem. Med. Biol., 2014, 28(1), 100-104.
[62]
Li, N.; Yu, Z.L.; Wang, L.; Zheng, Y.T.; Jia, J.X.; Wang, Q.; Zhu, M.J.; Liu, X.H.; Xia, X.; Li, W.J. Early-life lead exposure affects the activity of TNF-alpha and expression of SNARE complex in hippocampus of mouse pups. Biol. Trace Elem. Res., 2009, 132(1-3), 227-238.
[63]
Wang, L.; Shiraki, A.; Itahashi, M.; Akane, H.; Abe, H.; Mitsumori, K.; Shibutani, M. Aberration in epigenetic gene regulation in hippocampal neurogenesis by developmental exposure to manganese chloride in mice. Toxicol. Sci., 2013, 136(1), 154-165.
[64]
Wang, L.; Ohishi, T.; Shiraki, A.; Morita, R.; Akane, H.; Ikarashi, Y.; Mitsumori, K.; Shibutani, M. Developmental exposure to manganese chloride induces sustained aberration of neurogenesis in the hippocampal dentate gyrus of mice. Toxicol. Sci., 2012, 127(2), 508-521.
[65]
Jaya, P.R.; Hariprasad, R.G.; Bhuvaneswari, D.C.; Rajarami, R.G. Zinc and calcium reduce lead induced perturbations in the aminergic system of developing brain. Biometals, 2005, 18(6), 615-626.