485
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Identifying candidate genes associated with hippocampal dysfunction in a hemiparkinsonian rat model by transcriptomic profiling

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon show all
Pages 198-215 | Received 29 Jan 2024, Accepted 12 Mar 2024, Published online: 30 Apr 2024

References

  • Alieva AK, Filatova EV, Kolacheva AA, Rudenok MM, Slominsky PA, Ugrumov MV, Shadrina MI. 2017. Transcriptome profile changes in mice with MPTP-induced early stages of Parkinson's disease. Mol Neurobiol. 54(9):6775–6784. doi:10.1007/s12035-016-0190-y.
  • Amador A, Bostick CD, Olson H, Peters J, Camp CR, Krizay D, Chen W, Han W, Tang W, Kanber A, et al. 2020. Modelling and treating GRIN2A developmental and epileptic encephalopathy in mice. Brain. 143(7):2039–2057. doi:10.1093/brain/awaa147.
  • Ang MJ, Lee S, Kim JC, Kim SH, Moon C. 2021. Behavioral tasks evaluating schizophrenia-like symptoms in animal models: a recent update. Curr Neuropharmacol. 19(5):641–664. doi:10.2174/1570159X18666200814175114.
  • Avchalumov Y, Mandyam CD. 2021. Plasticity in the hippocampus, neurogenesis and drugs of abuse. Brain Sci. 11(3):404. doi:10.3390/brainsci11030404.
  • Bagetta V, Ghiglieri V, Sgobio C, Calabresi P, Picconi B. 2010. Synaptic dysfunction in Parkinson's disease. Biochem Soc Trans. 38(2):493–497. doi:10.1042/BST0380493.
  • Barrett T, Troup DB, Wilhite SE, Ledoux P, Rudnev D, Evangelista C, Kim IF, Soboleva A, Tomashevsky M, Marshall KA, et al. 2009. Ncbi GEO: archive for high-throughput functional genomic data. Nucleic Acids Res. 37(Database issue):D885–D890. doi:10.1093/nar/gkn764.
  • Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J R Stat Soc B. 57(1):289–300. doi:10.1111/j.2517-6161.1995.tb02031.x.
  • Berretta N, Berton F, Bianchi R, Capogna M, Francesconi W, Brunelli M. 1990. Effects of dopamine, D-1 and D-2 dopaminergic agonists on the excitability of hippocampal CA 1 pyramidal cells in Guinea pig. Exp Brain Res. 83:124–130. doi:10.1007/BF00232200.
  • Blasco-Serra A, Gonzalez-Soler EM, Cervera-Ferri A, Teruel-Marti V, Valverde-Navarro AA. 2017. A standardization of the novelty-suppressed feeding test protocol in rats. Neurosci Lett. 658:73–78. doi:10.1016/j.neulet.2017.08.019.
  • Calabresi P, Castrioto A, Di Filippo M, Picconi B. 2013. New experimental and clinical links between the hippocampus and the dopaminergic system in Parkinson's disease. Lancet Neurol. 12(8):811–821. doi:10.1016/S1474-4422(13)70118-2.
  • Chin CH, Chen SH, Wu HH, Ho CW, Ko MT, Lin CY. 2014. Cytohubba: identifying hub objects and sub-networks from complex interactome. BMC Syst Biol. 8:(Suppl 4):S11. doi:10.1186/1752-0509-8-4.
  • Costa C, Sgobio C, Siliquini S, Tozzi A, Tantucci M, Ghiglieri V, Di Filippo M, Pendolino V, de Iure A, Marti M, et al. 2012. Mechanisms underlying the impairment of hippocampal long-term potentiation and memory in experimental Parkinson's disease. Brain. 135(Pt 6):1884–1899. doi:10.1093/brain/aws101.
  • Ding J, Ding Y, Wu J, Deng J, Yu Q, Wang J. 2022. “Jing-Ning Granules” Can alleviate attention deficit hyperactivity disorder in rats by modulating dopaminergic D2/D1-like receptor-mediated signaling pathways. Evid-Based Compl Alt. 2022:9139841.
  • El Mahdy EM, Gamal M, Aboulhoda BE, Al Dreny BA, Shamaa A, Rashed L, Abdallah ANE, Shamseldeen AM. 2023. Amelioration of rotenone-induced Parkinson's disease; comparing therapeutic role of erythropoietin versus low-level laser activation of mesenchymal stem cells (an in-vivo and in-vitro study). Anim Cells Syst. 27(1):272–286. doi:10.1080/19768354.2023.2273467.
  • Feng C, Li X, Sha H, Luo X, Zou G, Liang H. 2022. Comparative transcriptome analysis provides novel insights into the molecular mechanism of the silver carp (Hypophthalmichthys molitrix) brain in response to hypoxia stress. Comp Biochem Phys D. 41:100951.
  • Ge SX, Jung D, Yao R. 2020. Shinygo: a graphical gene-set enrichment tool for animals and plants. Bioinformatics. 36(8):2628–2629. doi:10.1093/bioinformatics/btz931.
  • Ghiglieri V, Sgobio C, Costa C, Picconi B, Calabresi P. 2011. Striatum-hippocampus balance: from physiological behavior to interneuronal pathology. Prog Neurobiol. 94(2):102–114. doi:10.1016/j.pneurobio.2011.04.005.
  • Goncalves DF, Courtes AA, Hartmann DD, da Rosa PC, Oliveira DM, Soares FAA, Dalla Corte CL. 2019. 6-Hydroxydopamine induces different mitochondrial bioenergetics response in brain regions of rat. Neurotoxicology. 70:1–11. doi:10.1016/j.neuro.2018.10.005.
  • Grammatopoulos DK. 2017. Regulation of G-protein coupled receptor signalling underpinning neurobiology of mood disorders and depression. Mol Cell Endocrinol. 449:82–89. doi:10.1016/j.mce.2017.02.013.
  • Hain EG, Sparenberg M, Rasinska J, Klein C, Akyuz L, Steiner B. 2018. Indomethacin promotes survival of new neurons in the adult murine hippocampus accompanied by anti-inflammatory effects following MPTP-induced dopamine depletion. J Neuroinflammation. 15(1):162. doi:10.1186/s12974-018-1179-4.
  • Halliday GM, Leverenz JB, Schneider JS, Adler CH. 2014. The neurobiological basis of cognitive impairment in Parkinson's disease. Mov Disord. 29(5):634–650. doi:10.1002/mds.25857.
  • Hong S, Weerasinghe-Mudiyanselage PDE, Kang S, Moon C, Shin T. 2023. Retinal transcriptome profiling identifies novel candidate genes associated with visual impairment in a mouse model of multiple sclerosis. Anim Cells Syst (Seoul). 27(1):219–233. doi:10.1080/19768354.2023.2264354.
  • Howland JG, Wang YT. 2008. Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res. 169:145–158. doi:10.1016/S0079-6123(07)00008-8.
  • Huang GH, Cao XY, Li YY, Zhou CC, Li L, Wang K, Li H, Yu P, Jin Y, Gao L. 2019. Gene expression profile of the hippocampus of rats subjected to traumatic brain injury. J Cell Biochem. 120(9):15776–15789. doi:10.1002/jcb.28848.
  • Infante J, Prieto C, Sierra M, Sanchez-Juan P, Gonzalez-Aramburu I, Sanchez-Quintana C, Berciano J, Combarros O, Sainz J. 2015. Identification of candidate genes for Parkinson's disease through blood transcriptome analysis in LRRK2-G2019S carriers, idiopathic cases, and controls. Neurobiol Aging. 36(2):1105–1109. doi:10.1016/j.neurobiolaging.2014.10.039.
  • Kahl KG, Bens S, Ziegler K, Rudolf S, Kordon A, Dibbelt L, Schweiger U. 2009. Angiogenic factors in patients with current major depressive disorder comorbid with borderline personality disorder. Psychoneuroendocrinology. 34(3):353–357. doi:10.1016/j.psyneuen.2008.09.016.
  • Kalish BT, Cheadle L, Hrvatin S, Nagy MA, Rivera S, Crow M, Gillis J, Kirchner R, Greenberg ME. 2018. Single-cell transcriptomics of the developing lateral geniculate nucleus reveals insights into circuit assembly and refinement. Proc Natl Acad Sci USA. 115(5):E1051–E1060. doi:10.1073/pnas.1717871115.
  • Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, Li M, Sousa AM, Pletikos M, Meyer KA, Sedmak G, et al. 2011. Spatio-temporal transcriptome of the human brain. Nature. 478(7370):483–489. doi:10.1038/nature10523.
  • Kim B, Kim JS, Youn B, Moon C. 2023. Dopamine depletion alters neuroplasticity-related signaling in the rat hippocampus. Anim Cells Syst (Seoul). 27(1):436–446. doi:10.1080/19768354.2023.2294308.
  • Kim B, Weerasinghe-Mudiyanselage PDE, Ang MJ, Lee J, Kang S, Kim JC, Kim SH, Kim JS, Jung C, Shin T, et al. 2022. Changes in the neuronal architecture of the hippocampus in a 6-hydroxydopamine-lesioned Rat model of Parkinson disease. Int Neurourol J. 26(Suppl 2):S94–105. doi:10.5213/inj.2244252.126.
  • Ko KR, Lee J, Lee D, Nho B, Kim S. 2018. Hepatocyte growth factor (HGF) promotes peripheral nerve regeneration by activating repair Schwann cells. Sci Rep. 8(1):8316. doi:10.1038/s41598-018-26704-x.
  • Kondo J, Kitamura Y, Inden M, Taniguchi T. 2004. Hemiparkinsonian rat models: different sensitivity of dopaminergic neurotoxins. Int Congr Ser. 1260:281–285. doi:10.1016/S0531-5131(03)01573-5.
  • Kutlu MG, Gould TJ. 2016. Effects of drugs of abuse on hippocampal plasticity and hippocampus-dependent learning and memory: contributions to development and maintenance of addiction. Learn Mem. 23(10):515–533. doi:10.1101/lm.042192.116.
  • Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods. 9(4):357–359. doi:10.1038/nmeth.1923.
  • Lauss M, Kriegner A, Vierlinger K, Noehammer C. 2007. Characterization of the drugged human genome. Pharmacogenomics. 8(8):1063–1073. doi:10.2217/14622416.8.8.1063.
  • Lee J, Weerasinghe-Mudiyanselage PDE, Kim B, Kang S, Kim JS, Moon C. 2023. Impact of diesel particulate matter on the olfactory bulb of mice: insights from behavioral, histological, and molecular assessments. Mol Cell Toxicol. In press. doi:10.1007/s13273-023-00414-6.
  • Lisman JE, Grace AA. 2005. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron. 46(5):703–713. doi:10.1016/j.neuron.2005.05.002.
  • Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12):550. doi:10.1186/s13059-014-0550-8.
  • Luders KA, Patzig J, Simons M, Nave KA, Werner HB. 2017. Genetic dissection of oligodendroglial and neuronal Plp1 function in a novel mouse model of spastic paraplegia type 2. Glia. 65(11):1762–1776. doi:10.1002/glia.23193.
  • Lyu Y, Huang Y, Shi G, Lei X, Li K, Zhou R, Bai L, Qin C. 2021. Transcriptome profiling of five brain regions in a 6-hydroxydopamine rat model of Parkinson's disease. CNS Neurosci Ther. 27(11):1289–1299. doi:10.1111/cns.13702.
  • Mascolo A, Sessa M, Scavone C, De Angelis A, Vitale C, Berrino L, Rossi F, Rosano G, Capuano A. 2017. New and old roles of the peripheral and brain renin-angiotensin-aldosterone system (RAAS): focus on cardiovascular and neurological diseases. Int J Cardiol. 227:734–742. doi:10.1016/j.ijcard.2016.10.069.
  • Moni MA, Rana HK, Islam MB, Ahmed MB, Xu H, Hasan MAM, Lei Y, Quinn JMW. 2019. A computational approach to identify blood cell-expressed Parkinson's disease biomarkers that are coordinately expressed in brain tissue. Comput Biol Med. 113:103385. doi:10.1016/j.compbiomed.2019.103385.
  • Mu Y, Gage FH. 2011. Adult hippocampal neurogenesis and its role in Alzheimer's disease. Mol Neurodegener. 6(1):85. doi:10.1186/1750-1326-6-85.
  • Olivares D, Deshpande VK, Shi Y, Lahiri DK, Greig NH, Rogers JT, Huang X. 2012. N-methyl D-aspartate (NMDA) receptor antagonists and memantine treatment for Alzheimer's disease, vascular dementia and Parkinson's disease. Curr Alzheimer Res. 9(6):746–758. doi:10.2174/156720512801322564.
  • Parker KL, Lamichhane D, Caetano MS, Narayanan NS. 2013. Executive dysfunction in Parkinson's disease and timing deficits. Front Integr Neurosci. 7:75. doi:10.3389/fnint.2013.00075.
  • R Core Team. 2013. R: a language and environment for statistical computing.
  • Regensburger M, Prots I, Winner B. 2014. Adult hippocampal neurogenesis in Parkinson's disease: impact on neuronal survival and plasticity. Neural Plast. 2014:454696. doi:10.1155/2014/454696.
  • Russo AJ. 2010. Decreased serum hepatocyte growth factor (HGF) in individuals with depression correlates with severity of disease. Biomark Insights. 5:63–67. doi:10.4137/BMI.S5183.
  • Schaefers AT, Teuchert-Noodt G. 2016. Developmental neuroplasticity and the origin of neurodegenerative diseases. World J Biol Psychiatry. 17(8):587–599.
  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 1971. Cytoscape: a software environment for integrated models. Genome Res. 13(22):426.
  • Sodhi RK, Bansal Y, Singh R, Saroj P, Bhandari R, Kumar B, Kuhad A. 2021. IDO-1 inhibition protects against neuroinflammation, oxidative stress and mitochondrial dysfunction in 6-OHDA induced murine model of Parkinson's disease. Neurotoxicology. 84:184–197. doi:10.1016/j.neuro.2021.03.009.
  • Speranza L, di Porzio U, Viggiano D, de Donato A, Volpicelli F. 2021. Dopamine: the neuromodulator of long-term synaptic plasticity, reward and movement control. Cells. 10(4):735. doi:10.3390/cells10040735.
  • Szklarczyk D, Gable AL, Nastou KC, Lyon D, Kirsch R, Pyysalo S, Doncheva NT, Legeay M, Fang T, Bork P, et al. 2021. The STRING database in 2021: customizable protein–protein networks, and functional characterization of user-uploaded gene/measurement sets. Nucleic Acids Res. 49(D1):D605–D612. doi:10.1093/nar/gkaa1074.
  • Tomita H, Ziegler ME, Kim HB, Evans SJ, Choudary PV, Li JZ, Meng F, Dai M, Myers RM, Neal CR, et al. 2013. G protein-linked signaling pathways in bipolar and major depressive disorders. Front Genet. 4:297. doi:10.3389/fgene.2013.00297.
  • Trabucchi M, Albizzati MG, Frattola L, Scarlato G. 1979. Hemiparkinsonism. A human model for studying dopaminergic supersensitivity. Arch Neurol. 36(4):246–248. doi:10.1001/archneur.1979.00500400100020.
  • Trujillo-Paredes N, Valencia C, Guerrero-Flores G, Arzate DM, Baizabal JM, Guerra-Crespo M, Fuentes-Hernandez A, Zea-Armenta I, Covarrubias L. 2016. Regulation of differentiation flux by Notch signalling influences the number of dopaminergic neurons in the adult brain. Biol Open. 5(3):336–347. doi:10.1242/bio.013383.
  • Villar-Conde S, Astillero-Lopez V, Gonzalez-Rodriguez M, Villanueva-Anguita P, Saiz-Sanchez D, Martinez-Marcos A, Flores-Cuadrado A, Ubeda-Banon I. 2021. The human hippocampus in Parkinson's disease: an integrative stereological and proteomic study. J Parkinsons Dis. 11(3):1345–1365. doi:10.3233/JPD-202465.
  • Wada M, Ang MJ, Weerasinghe-Mudiyanselage PDE, Kim SH, Kim JC, Shin T, Moon C. 2021. Behavioral characterization in MPTP/p mouse model of Parkinson's disease. J Integr Neurosci. 20(2):307–320. doi:10.31083/j.jin2002030.
  • Wang N, Zhang L, Yang H, Luo X, Fan G. 2019. Do multiple system atrophy and Parkinson’s disease show distinct patterns of volumetric alterations across hippocampal subfields? An exploratory study. Eur Radiol. 29:4948–4956. doi:10.1007/s00330-019-06043-9.
  • Weerasinghe-Mudiyanselage PDE, Kang S, Kim JS, Kim SH, Wang H, Shin T, Moon C. 2024. Changes in structural plasticity of hippocampal neurons in an animal model for multiple sclerosis. Zool Res. 45(2):398–414. doi:10.24272/j.issn.2095-8137.2023.309.
  • Weerasinghe-Mudiyanselage PDE, Kang S, Kim JS, Moon C. 2023. Therapeutic approaches to non-motor symptoms of Parkinson's disease: a current update on preclinical evidence. Curr Neuropharmacol. 21(3):560–577. doi:10.2174/1570159X20666221005090126.
  • Yao DB, Li MY, Shen DD, Ding F, Lu SB, Zhao Q, Gu XS. 2012. Gene expression profiling of the rat sciatic nerve in early Wallerian degeneration after injury. Neural Regen Res. 7(17):1285–1292.
  • Zhang D, Yang S, Toledo EM, Gyllborg D, Salto C, Carlos Villaescusa J, Arenas E. 2017. Niche-derived laminin-511 promotes midbrain dopaminergic neuron survival and differentiation through YAP. Sci Signal. 10(493):eaal4165. doi:10.1126/scisignal.aal4165.
  • Zhang H, Li J, Ren J, Sun S, Ma S, Zhang W, Yu Y, Cai Y, Yan K, Li W, et al. 2021. Single-nucleus transcriptomic landscape of primate hippocampal aging. Protein Cell. 12(9):695–716. doi:10.1007/s13238-021-00852-9.
  • Zhu G, Chen Y, Huang Y, Li Q, Behnisch T. 2011. MPTP-meditated hippocampal dopamine deprivation modulates synaptic transmission and activity-dependent synaptic plasticity. Toxicol Appl Pharmacol. 254(3):332–341. doi:10.1016/j.taap.2011.05.007.