Intermittent fasting increases the expressions of SODs and catalase in granule and polymorphic cells and enhances neuroblast dendrite complexity and maturation in the adult gerbil dentate gyrus

Ahn,Ji  Hyeon; Shin,Bich  Na; Song,Minah; Kim,Hyunjung; Park,Joon  Ha; Lee,Tae‑Kyeong; Park,Cheol  Woo; Park,Young  Eun; Lee,Jae‑Chul; Yong,Jun‑Hwan; Lee,Choong‑Hyun; Hwang,In  Koo; Won,Moo‑Ho; Lee,Yun Lyul

doi:10.3892/mmr.2019.9822

Intermittent fasting increases the expressions of SODs and catalase in granule and polymorphic cells and enhances neuroblast dendrite complexity and maturation in the adult gerbil dentate gyrus

Authors:
- Ji Hyeon Ahn
- Bich Na Shin
- Minah Song
- Hyunjung Kim
- Joon Ha Park
- Tae‑Kyeong Lee
- Cheol Woo Park
- Young Eun Park
- Jae‑Chul Lee
- Jun‑Hwan Yong
- Choong‑Hyun Lee
- In Koo Hwang
- Moo‑Ho Won
- Yun Lyul Lee
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Affiliations: Department of Biomedical Science and Research Institute for Bioscience and Biotechnology, Hallym University, Chuncheon, Gangwon 24252, Republic of Korea, Danchunok Company, Chuncheon, Gangwon 24210, Republic of Korea, Department of Neurobiology, School of Medicine, Kangwon National University, Chuncheon, Gangwon 24341, Republic of Korea, Department of Occupational Therapy, Dongnam Health University, Suwon, Gyeonggi 16238, Republic of Korea, Department of Pharmacy, College of Pharmacy, Dankook University, Cheonan, Chungcheongnam 31116, Republic of Korea, Department of Anatomy and Cell Biology, College of Veterinary Medicine, and Research Institute for Veterinary Science, Seoul National University, Seoul 08826, Republic of Korea, Department of Physiology, College of Medicine and Institute of Neurodegeneration and Neuroregeneration, Hallym University, Chuncheon, Gangwon 24252, Republic of Korea
Published online on: January 4, 2019 https://doi.org/10.3892/mmr.2019.9822
Pages: 1721-1727
Copyright: © Ahn et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Intermittent fasting (ImF) is known to reduce oxidative stress and affects adult neurogenesis in the hippocampal dentate gyrus. However, it is unknown how ImF affects endogenous antioxidants expressions, cell proliferation, and neuroblast differentiation and their dendrite remodeling over 3 months in the dentate gyrus of adult gerbils. The present study subjected 6‑month old male gerbils to a normal diet or alternate‑day ImF for 1, 2 and 3 months. Changes in body weight were not significantly different between gerbils fed a normal diet and on ImF. The present study also investigated the effects of ImF on antioxidant enzymes [superoxide dismutase (SOD)‑1, SOD2 and catalase] using immunohistochemistry, and endogenous cell proliferation, neuroblast differentiation and neuroblast dendrite complexity by using Ki67 (a cell proliferation marker) and doublecortin (neuroblast differentiation marker) immunohistochemistry in the dentate gyrus. SOD1, SOD2 and CAT immunoreactivities were shown in cells in the granule cell and polymorphic layers. SOD1, SOD2 and catalase immunoreactivity in the cells peaked at 2, 1 and 1 month, respectively, following ImF. Cell proliferation was ~250, 129 and 186% of the control, at 1, 2 and 3 months of ImF, respectively. Neuroblast differentiation was ~41, 32 and 12% of the control, at 1, 2 and 3 months of ImF, respectively, indicating that dendrites of neuroblasts were more arborized and developed at 3 months of ImF. Taken together, these results indicate that ImF for 3 months improves endogenous SOD1, SOD2 and catalase expressions and enhances cell proliferation, and neuroblast dendrites complexity and maturation in the adult gerbil dentate gyrus.

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1	Li L, Wang Z and Zuo Z: Chronic intermittent fasting improves cognitive functions and brain structures in mice. PLoS One. 8:e660692013. View Article : Google Scholar : PubMed/NCBI
2	Jeong JH, Yu KS, Bak DH, Lee JH, Lee NS, Jeong YG, Kim DK, Kim JJ and Han SY: Intermittent fasting is neuroprotective in focal cerebral ischemia by minimizing autophagic flux disturbance and inhibiting apoptosis. Exp Ther Med. 12:3021–3028. 2016. View Article : Google Scholar : PubMed/NCBI
3	Arumugam TV, Phillips TM, Cheng A, Morrell CH, Mattson MP and Wan R: Age and energy intake interact to modify cell stress pathways and stroke outcome. Ann Neurol. 67:41–52. 2010. View Article : Google Scholar : PubMed/NCBI
4	Mladenovic Djordjevic A, Perovic M, Tesic V, Tanic N, Rakic L, Ruzdijic S and Kanazir S: Long-term dietary restriction modulates the level of presynaptic proteins in the cortex and hippocampus of the aging rat. Neurochem Int. 56:250–255. 2010. View Article : Google Scholar : PubMed/NCBI
5	Ma L, Wang R, Dong W and Zhao Z: Caloric restriction can improve learning and memory in C57/BL mice probably via regulation of the AMPK signaling pathway. Exp Gerontol. 102:28–35. 2018. View Article : Google Scholar : PubMed/NCBI
6	Gage FH: Mammalian neural stem cells. Science. 287:1433–1438. 2000. View Article : Google Scholar : PubMed/NCBI
7	Lee J, Duan W and Mattson MP: Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem. 82:1367–1375. 2002. View Article : Google Scholar : PubMed/NCBI
8	Deng W, Aimone JB and Gage FH: New neurons and new memories: How does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci. 11:339–350. 2010. View Article : Google Scholar : PubMed/NCBI
9	Lee J, Duan W, Long JM, Ingram DK and Mattson MP: Dietary restriction increases the number of newly generated neural cells and induces BDNF expression, in the dentate gyrus of rats. J Mol Neurosci. 15:99–108. 2000. View Article : Google Scholar : PubMed/NCBI
10	Lee J, Seroogy KB and Mattson MP: Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J Neurochem. 80:539–547. 2002. View Article : Google Scholar : PubMed/NCBI
11	Zelko IN, Mariani TJ and Folz RJ: Superoxide dismutase multigene family: A comparison of the CuZn-SOD (SOD1), Mn-SOD (SOD2), and EC-SOD (SOD3) gene structures, evolution and expression. Free Radic Biol Med. 33:337–349. 2002. View Article : Google Scholar : PubMed/NCBI
12	Chelikani P, Fita I and Loewen PC: Diversity of structures and properties among catalases. Cell Mol Life Sci. 61:192–208. 2004. View Article : Google Scholar : PubMed/NCBI
13	Faiz M, Acarin L, Peluffo H, Villapol S, Castellano B and Gonzalez B: Antioxidant Cu/Zn SOD: Expression in postnatal brain progenitor cells. Neurosci Lett. 401:71–76. 2006. View Article : Google Scholar : PubMed/NCBI
14	Ostadsharif M, Ghaedi K, Hossein Nasr-Esfahani M, Mojbafan M, Tanhaie S, Karbalaie K and Baharvand H: The expression of peroxisomal protein transcripts increased by retinoic acid during neural differentiation. Differentiation. 81:127–132. 2011. View Article : Google Scholar : PubMed/NCBI
15	Tajes M, Gutierrez-Cuesta J, Folch J, Ortuño-Sahagun D, Verdaguer E, Jiménez A, Junyent F, Lau A, Camins A and Pallàs M: Neuroprotective role of intermittent fasting in senescence-accelerated mice P8 (SAMP8). Exp Gerontol. 45:702–710. 2010. View Article : Google Scholar : PubMed/NCBI
16	Ahn JH, Shin BN, Park JH, Kim IH, Cho JH, Chen B, Lee TK, Tae HJ, Lee JC, Cho JH, et al: Long-term observation of neuronal degeneration and microgliosis in the gerbil dentate gyrus after transient cerebral ischemia. J Neurol Sci. 363:21–26. 2016. View Article : Google Scholar : PubMed/NCBI
17	Yan BC, Park JH, Chen BH, Cho JH, Kim IH, Ahn JH, Lee JC, Hwang IK, Cho JH, Lee YL, et al: Long-term administration of scopolamine interferes with nerve cell proliferation, differentiation and migration in adult mouse hippocampal dentate gyrus, but it does not induce cell death. Neural Regen Res. 9:1731–1739. 2014. View Article : Google Scholar : PubMed/NCBI
18	Carpenter JW: Exotic animal formulary (ED 4). J Exotic Pet Med. 22:308–309. 2013.
19	Chen BH, Ahn JH, Park JH, Song M, Kim H, Lee TK, Lee JC, Kim YM, Hwang IK, Kim DW, et al: Rufinamide, an antiepileptic drug, improves cognition and increases neurogenesis in the aged gerbil hippocampal dentate gyrus via increasing expressions of IGF-1, IGF-1R and p-CREB. Chem Biol Interact. 286:71–77. 2018. View Article : Google Scholar : PubMed/NCBI
20	Lee TK, Park JH, Ahn JH, Shin MC, Cho JH, Bae EJ, Kim YM, Won MH and Lee CH: Pretreated duloxetine protects hippocampal CA1 pyramidal neurons from ischemia-reperfusion injury through decreases of glial activation and oxidative stress. J Neurol Sci. 370:229–236. 2016. View Article : Google Scholar : PubMed/NCBI
21	Chen BH, Yan BC, Park JH, Ahn JH, Lee DH, Kim IH, Cho JH, Lee JC, Kim SK, Lee B, et al: Aripiprazole, an atypical antipsychotic drug, improves maturation and complexity of neuroblast dendrites in the mouse dentate gyrus via increasing superoxide dismutases. Neurochem Res. 38:1980–1988. 2013. View Article : Google Scholar : PubMed/NCBI
22	Anson RM, Guo Z, de Cabo R, Iyun T, Rios M, Hagepanos A, Ingram DK, Lane MA and Mattson MP: Intermittent fasting dissociates beneficial effects of dietary restriction on glucose metabolism and neuronal resistance to injury from calorie intake. Proc Natl Acad Sci USA. 100:6216–6220. 2003. View Article : Google Scholar : PubMed/NCBI
23	Vasconcelos AR, Kinoshita PF, Yshii LM, Marques Orellana AM, Böhmer AE, de Sá Lima L, Alves R, Andreotti DZ, Marcourakis T, Scavone C and Kawamoto EM: Effects of intermittent fasting on age-related changes on Na,K-ATPase activity and oxidative status induced by lipopolysaccharide in rat hippocampus. Neurobiol Aging. 36:1914–1923. 2015. View Article : Google Scholar : PubMed/NCBI
24	Walsh ME, Shi Y and Van Remmen H: The effects of dietary restriction on oxidative stress in rodents. Free Radic Biol Med. 66:88–99. 2014. View Article : Google Scholar : PubMed/NCBI
25	Brandhorst S, Choi IY, Wei M, Cheng CW, Sedrakyan S, Navarrete G, Dubeau L, Yap LP, Park R, Vinciguerra M, et al: A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 22:86–99. 2015. View Article : Google Scholar : PubMed/NCBI
26	Fishman K, Baure J, Zou Y, Huang TT, Andres-Mach M, Rola R, Suarez T, Acharya M, Limoli CL, Lamborn KR and Fike JR: Radiation-induced reductions in neurogenesis are ameliorated in mice deficient in CuZnSOD or MnSOD. Free Radic Biol Med. 47:1459–1467. 2009. View Article : Google Scholar : PubMed/NCBI
27	Liao AC, Craver BM, Tseng BP, Tran KK, Parihar VK, Acharya MM and Limoli CL: Mitochondrial-targeted human catalase affords neuroprotection from proton irradiation. Radiat Res. 180:1–6. 2013. View Article : Google Scholar : PubMed/NCBI
28	Parihar VK, Allen BD, Tran KK, Chmielewski NN, Craver BM, Martirosian V, Morganti JM, Rosi S, Vlkolinsky R, Acharya MM, et al: Targeted overexpression of mitochondrial catalase prevents radiation-induced cognitive dysfunction. Antioxid Redox Signal. 22:78–91. 2015. View Article : Google Scholar : PubMed/NCBI
29	Chmielewski NN, Caressi C, Giedzinski E, Parihar VK and Limoli CL: Contrasting the effects of proton irradiation on dendritic complexity of subiculum neurons in wild type and MCAT mice. Environ Mol Mutagen. 57:364–371. 2016. View Article : Google Scholar : PubMed/NCBI
30	Dias GP, Cavegn N, Nix A, do Nascimento Bevilaqua MC, Stangl D, Zainuddin MS, Nardi AE, Gardino PF and Thuret S: The role of dietary polyphenols on adult hippocampal neurogenesis: Molecular mechanisms and behavioural effects on depression and anxiety. Oxid Med Cell Longev 2012. 5419712012.