Transcriptome profiling of the subventricular zone and dentate gyrus in an animal model of Parkinson's disease

Bao,Xin-Jie; Wang,Geng-Chao; Zuo,Fu-Xing; Li,Xue-Yuan; Wu,Jun; Chen,Guo; Dou,Wan‑Chen; Guo,Yi; Shen,Qin; Wang,Ren-Zhi

doi:10.3892/ijmm.2017.3052

Transcriptome profiling of the subventricular zone and dentate gyrus in an animal model of Parkinson's disease

Authors:
- Xin-Jie Bao
- Geng-Chao Wang
- Fu-Xing Zuo
- Xue-Yuan Li
- Jun Wu
- Guo Chen
- Wan‑Chen Dou
- Yi Guo
- Qin Shen
- Ren-Zhi Wang
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Affiliations: Department of Neurosurgery, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, P.R. China, State Key Laboratory of Medical Molecular Biology and Department of Biochemistry and Molecular Biology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100730, P.R. China, Department of Neurosurgery, National Cancer Center/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing 100021, P.R. China, Center for Stem Cell Biology and Regenerative Medicine, Center for Life Sciences, School of Medicine, Tsinghua University, Beijing 100084, P.R. China
Published online on: July 3, 2017 https://doi.org/10.3892/ijmm.2017.3052
Pages: 771-783
Copyright: © Bao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Adult neurogenesis in the subventricular zone (SVZ), as well as in the subgranular zone contributes to brain maintenance and regeneration. In the adult brain, dopamine (DA) can regulate the endogenous neural stem cells within these two regions, while a DA deficit may affect neurogenesis. Notably, the factors that regulate in vivo neurogenesis in these subregions have not yet been fully characterized, particularly following DA depletion. In thi study, we performed RNA sequencing to investigate transcriptomic changes in the SVZ and dentate gyrus (DG) of mice in response to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). This analysis identified differentially expressed genes which were involved in the regulation of transcription, immune response, extracellular region, cell junction and myelination. These genes partially displayed different temporal profiles of expression, some of which may participate in the metabolic switch related to neurogenesis. Additionally, the mitogen‑activated protein kinase (MAPK) signaling pathway was shown to be been positively regulated in the SVZ, while it was negatively affected in the DG following MPTP administration. Overall, our findings indicate that exposure to MPTP may exert different effects on transcriptome profiling between the SVZ and DG.

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1	Ming GL and Song H: Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 70:687–702. 2011. View Article : Google Scholar : PubMed/NCBI
2	Höglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I and Hirsch EC: Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci. 7:726–735. 2004. View Article : Google Scholar : PubMed/NCBI
3	Ohtani N, Goto T, Waeber C and Bhide PG: Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci. 23:2840–2850. 2003.PubMed/NCBI
4	van den Berge SA, van Strien ME, Korecka JA, Dijkstra AA, Sluijs JA, Kooijman L, Eggers R, De Filippis L, Vescovi AL, Verhaagen J, et al: The proliferative capacity of the subventricular zone is maintained in the parkinsonian brain. Brain. 134:3249–3263. 2011. View Article : Google Scholar : PubMed/NCBI
5	Marxreiter F, Regensburger M and Winkler J: Adult neurogenesis in Parkinson's disease. Cell Mol Life Sci. 70:459–473. 2013. View Article : Google Scholar
6	Aponso PM, Faull RL and Connor B: Increased progenitor cell proliferation and astrogenesis in the partial progressive 6-hydroxydopamine model of Parkinson's disease. Neuroscience. 151:1142–1153. 2008. View Article : Google Scholar : PubMed/NCBI
7	Winner B, Geyer M, Couillard-Despres S, Aigner R, Bogdahn U, Aigner L, Kuhn G and Winkler J: Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp Neurol. 197:113–121. 2006. View Article : Google Scholar
8	Horgusluoglu E, Nudelman K, Nho K and Saykin AJ: Adult neurogenesis and neurodegenerative diseases: a systems biology perspective. Am J Med Genet B Neuropsychiatr Genet. 174:93–112. 2017. View Article : Google Scholar
9	Faigle R and Song H: Signaling mechanisms regulating adult neural stem cells and neurogenesis. Biochim Biophys Acta. 1830:2435–2448. 2013. View Article : Google Scholar :
10	Llorens-Bobadilla E, Zhao S, Baser A, Saiz-Castro G, Zwadlo K and Martin-Villalba A: Single-cell transcriptomics reveals a population of dormant neural stem cells that become activated upon brain injury. Cell Stem Cell. 17:329–340. 2015. View Article : Google Scholar : PubMed/NCBI
11	Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, Haladyniak U, Agbemenyah HY, Zovoilis A, Salinas-Riester G, et al: A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J. 30:4071–4083. 2011. View Article : Google Scholar : PubMed/NCBI
12	Zhou R, Diehl D, Hoeflich A, Lahm H and Wolf E: IGF-binding protein-4: biochemical characteristics and functional consequences. J Endocrinol. 178:177–193. 2003. View Article : Google Scholar : PubMed/NCBI
13	Shin J, Berg DA, Zhu Y, Shin JY, Song J, Bonaguidi MA, Enikolopov G, Nauen DW, Christian KM, Ming GL, et al: Single-cell RNA-seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell. 17:360–372. 2015. View Article : Google Scholar : PubMed/NCBI
14	Zuo FX, Bao XJ, Sun XC, Wu J, Bai QR, Chen G, Li XY, Zhou QY, Yang YF, Shen Q, et al: Transplantation of human neural stem cells in a parkinsonian model exerts neuroprotection via regulation of the host microenvironment. Int J Mol Sci. 16:26473–26492. 2015. View Article : Google Scholar : PubMed/NCBI
15	Jackson-Lewis V and Przedborski S: Protocol for the MPTP mouse model of Parkinson's disease. Nat Protoc. 2:141–151. 2007. View Article : Google Scholar : PubMed/NCBI
16	Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ and Lee VM: Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron. 34:521–533. 2002. View Article : Google Scholar : PubMed/NCBI
17	Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL and Pachter L: Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 7:562–578. 2012. View Article : Google Scholar : PubMed/NCBI
18	Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, et al: WEGO: a web tool for plotting GO annotations. Nucleic Acids Res. 34(Web server): W293–W297. 2006. View Article : Google Scholar : PubMed/NCBI
19	Kolobova E, Tuganova A, Boulatnikov I and Popov KM: Regulation of pyruvate dehydrogenase activity through phosphorylation at multiple sites. Biochem J. 358:69–77. 2001. View Article : Google Scholar : PubMed/NCBI
20	Lee DW, Rajagopalan S, Siddiq A, Gwiazda R, Yang L, Beal MF, Ratan RR and Andersen JK: Inhibition of prolyl hydroxylase protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity: model for the potential involvement of the hypoxia-inducible factor pathway in Parkinson disease. J Biol Chem. 284:29065–29076. 2009. View Article : Google Scholar : PubMed/NCBI
21	Daniele S, Lecca D, Trincavelli ML, Ciampi O, Abbracchio MP and Martini C: Regulation of PC12 cell survival and differentiation by the new P2Y-like receptor GPR17. Cell Signal. 22:697–706. 2010. View Article : Google Scholar : PubMed/NCBI
22	Charbonnier-Beaupel F, Malerbi M, Alcacer C, Tahiri K, Carpentier W, Wang C, During M, Xu D, Worley PF, Girault JA, et al: Gene expression analyses identify Narp contribution in the development of L-DOPA-induced dyskinesia. J Neurosci. 35:96–111. 2015. View Article : Google Scholar : PubMed/NCBI
23	Södersten E, Feyder M, Lerdrup M, Gomes AL, Kryh H, Spigolon G, Caboche J, Fisone G and Hansen K: Dopamine signaling leads to loss of Polycomb repression and aberrant gene activation in experimental parkinsonism. PLoS Genet. 10:e10045742014. View Article : Google Scholar : PubMed/NCBI
24	Safe S, Jin UH, Morpurgo B, Abudayyeh A, Singh M and Tjalkens RB: Nuclear receptor 4A (NR4A) family - orphans no more. J Steroid Biochem Mol Biol. 157:48–60. 2016. View Article : Google Scholar
25	Björklund A and Dunnett SB: Dopamine neuron systems in the brain: an update. Trends Neurosci. 30:194–202. 2007. View Article : Google Scholar : PubMed/NCBI
26	Baker SA, Baker KA and Hagg T: Dopaminergic nigrostriatal projections regulate neural precursor proliferation in the adult mouse subventricular zone. Eur J Neurosci. 20:575–579. 2004. View Article : Google Scholar : PubMed/NCBI
27	Eells JB, Wilcots J, Sisk S and Guo-Ross SX: NR4A gene expression is dynamically regulated in the ventral tegmental area dopamine neurons and is related to expression of dopamine neurotransmission genes. J Mol Neurosci. 46:545–553. 2012. View Article : Google Scholar :
28	Velazquez FN, Prucca CG, Etienne O, D'Astolfo DS, Silvestre DC, Boussin FD and Caputto BL: Brain development is impaired in c-fos −/− mice. Oncotarget. 6:16883–16901. 2015. View Article : Google Scholar : PubMed/NCBI
29	Xiao G, Sun T, Songming C and Cao Y: NR4A1 enhances neural survival following oxygen and glucose deprivation: an in vitro study. J Neurol Sci. 330:78–84. 2013. View Article : Google Scholar : PubMed/NCBI
30	Tomioka T, Maruoka H, Kawa H, Yamazoe R, Fujiki D, Shimoke K and Ikeuchi T: The histone deacetylase inhibitor trichostatin A induces neurite outgrowth in PC12 cells via the epigenetically regulated expression of the nur77 gene. Neurosci Res. 88:39–48. 2014. View Article : Google Scholar : PubMed/NCBI
31	Yang SH, Sharrocks AD and Whitmarsh AJ: Transcriptional regulation by the MAP kinase signaling cascades. Gene. 320:3–21. 2003. View Article : Google Scholar : PubMed/NCBI
32	Guo Z, Zhang L, Wu Z, Chen Y, Wang F and Chen G: In vivo direct reprogramming of reactive glial cells into functional neurons after brain injury and in an Alzheimer's disease model. Cell Stem Cell. 14:188–202. 2014. View Article : Google Scholar
33	Sconce MD, Churchill MJ, Greene RE and Meshul CK: Intervention with exercise restores motor deficits but not nigrostriatal loss in a progressive MPTP mouse model of Parkinson's disease. Neuroscience. 299:156–174. 2015. View Article : Google Scholar : PubMed/NCBI
34	Sánchez-Mendoza E, Burguete MC, Castelló-Ruiz M, González MP, Roncero C, Salom JB, Arce C, Cañadas S, Torregrosa G, Alborch E, et al: Transient focal cerebral ischemia significantly alters not only EAATs but also VGLUTs expression in rats: relevance of changes in reactive astroglia. J Neurochem. 113:1343–1355. 2010.PubMed/NCBI
35	Etxeberria A, Mangin JM, Aguirre A and Gallo V: Adult-born SVZ progenitors receive transient synapses during remyelination in corpus callosum. Nat Neurosci. 13:287–289. 2010. View Article : Google Scholar : PubMed/NCBI
36	Aguirre A, Dupree JL, Mangin JM and Gallo V: A functional role for EGFR signaling in myelination and remyelination. Nat Neurosci. 10:990–1002. 2007. View Article : Google Scholar : PubMed/NCBI
37	Whitehouse A, Doherty K, Yeh HH, Robinson AC, Rollinson S, Pickering-Brown S, Snowden J, Thompson JC, Davidson YS and Mann DM: Histone deacetylases (HDACs) in frontotemporal lobar degeneration. Neuropathol Appl Neurobiol. 41:245–257. 2015. View Article : Google Scholar
38	Vithayathil J, Pucilowska J, Goodnough LH, Atit RP and Landreth GE: Dentate gyrus development requires ERK activity to maintain progenitor population and MAPK pathway feedback regulation. J Neurosci. 35:6836–6848. 2015. View Article : Google Scholar : PubMed/NCBI
39	Jiang P, Zhu T, Xia Z, Gao F, Gu W, Chen X, Yuan T and Yu H: Inhibition of MAPK/ERK signaling blocks hippocampal neurogenesis and impairs cognitive performance in prenatally infected neonatal rats. Eur Arch Psychiatry Clin Neurosci. 265:497–509. 2015. View Article : Google Scholar : PubMed/NCBI
40	Banzhaf-Strathmann J, Benito E, May S, Arzberger T, Tahirovic S, Kretzschmar H, Fischer A and Edbauer D: MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease. EMBO J. 33:1667–1680. 2014. View Article : Google Scholar : PubMed/NCBI
41	Majava M, Hoornaert KP, Bartholdi D, Bouma MC, Bouman K, Carrera M, Devriendt K, Hurst J, Kitsos G, Niedrist D, et al: A report on 10 new patients with heterozygous mutations in the COL11A1 gene and a review of genotype-phenotype correlations in type XI collagenopathies. Am J Med Genet A. 143A:258–264. 2007. View Article : Google Scholar : PubMed/NCBI
42	Buraschi S, Neill T, Goyal A, Poluzzi C, Smythies J, Owens RT, Schaefer L, Torres A and Iozzo RV: Decorin causes autophagy in endothelial cells via Peg3. Proc Natl Acad Sci USA. 110:E2582–E2591. 2013. View Article : Google Scholar : PubMed/NCBI