Chuan FU, Xiating LI, Lichun SUN, Tianlun FAN

2912

Transcriptome sequencing reveals circRNA expression profile in Parkinson’s disease-like mice after aerobic exercis

Transcriptome sequencing reveals circRNA expression profile in Parkinson’s disease-like mice after aerobic exercis

Parkinson’s disease (PD) is a common complex neurodegenerative disease, and aerobic exercise (EX) has potential to improve motor dysfunction. This study aimed to explore whether EX acts on PD in mice mode. Mice were administered 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine (MPTP) and subjected to a 4-week physical exercise regimen (EX-PD group) and underwent RNA-Seq. Here, MPTP caused PD, which was characterized by neuron shrinkage and behavioral deficits, whereas EX improved PD by rescuing neuronal survival and motor function in mice. Moreover, circRNA expression profiles identified a total of 142 differentially expressed circRNAs (DEcircRNAs) between PD and EX-PD group. These DEcircRNAs were mainly involved in PD, dopaminergic synapses, and calcium signaling pathways. The expression of circZfp827 and circTshz2 were significantly elevated in PD group while reduced owing to EX intervention. In contrast, EX intervention significantly restored decline in circHivep2 expression due to PD. The circRNA-miRNAmRNA network suggested that circZfp827, circHivep2, and circTshz2 were involved in ceRNA mechanism of EX to improve PD, and their target genes were significantly decreased after interference. The directly binding regulation relationship of circTshz2-mmu-miR326-3p-Th was verified by double luciferase reporter assay. Our research revealed that EX improved motor behavioral deficits and pathological features of PD mice, and circRNA-based signatures are potential candidates for further assessment as PD biomarkers for improvement by EX.
PDF

___

  • Beach TG, Carew J, Serrano G, Adler CH, Shill HA et al. (2014). Phosphorylated alpha-synuclein-immunoreactive retinal neuronal elements in Parkinson’s disease subjects. Neuroscience Letters 571: 34-38. doi: 10.1016/j.neulet.2014.04.027
  • Bidonde J, Busch AJ, Schachter CL, Overend TJ, Kim SY et al. (2017). Aerobic exercise training for adults with fibromyalgia. The Cochrane Database of Systematic Reviews 6: CD012700. doi: 10.1002/14651858.CD012700
  • Botta-Orfila T, Morato X, Compta Y, Lozano JJ, Falgas N et al. (2014). Identification of blood serum micro-RNAs associated with idiopathic and LRRK2 Parkinson’s disease. Journal of Neuroscience Research 92: 1071-1077. doi: 10.1002/jnr.23377
  • Cai S-y, Liu Z-h, Peng G-l, Tian R-h, Li P (2017a). The Effects of Exercise Therapy on Motor Behaviors of Preterm Infant Rats Induced by Intrauterine Inflammation. Neuropsychiatry (London) 7: 667-674.
  • Cai Y, Sun Z, Jia H, Luo H, Ye X et al. (2017b). Rpph1 Upregulates CDC42 Expression and Promotes Hippocampal Neuron Dendritic Spine Formation by Competing with miR-330-5p. Frontiers in Molecular Neuroscience 10: 27. doi: 10.3389/ fnmol.2017.00027
  • Cali T, Ottolini D, Brini M (2014). Calcium signaling in Parkinson’s disease. Cell and Tissue Research 357: 439-454. doi: 10.1007/ s00441-014-1866-0
  • Cohen JE, Lee PR, Fields RD (2014). Systematic identification of 3’-UTR regulatory elements in activity-dependent mRNA stability in hippocampal neurons. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 369. doi: 10.1098/rstb.2013.0509
  • D’Ambra E, Capauto D, Morlando M (2019). Exploring the Regulatory Role of Circular RNAs in Neurodegenerative Disorders. International Journal of Molecular Sciences 20. doi: 10.3390/ijms20215477
  • Desai BS, Monahan AJ, Carvey PM, Hendey B (2007). Blood-brain barrier pathology in Alzheimer’s and Parkinson’s disease: implications for drug therapy. Cell Transplantation 16: 285- 299. doi: 10.3727/000000007783464731
  • Eschbach J, Danzer KM (2014). alpha-Synuclein in Parkinson’s disease: pathogenic function and translation into animal models. Neuro-Degenerative Diseases 14: 1-17. doi: 10.1159/000354615
  • Farag ES, Vinters HV, Bronstein J (2009). Pathologic findings in retinal pigment epithelial cell implantation for Parkinson disease. Neurology 73: 1095-1102. doi: 10.1212/ WNL.0b013e3181bbff1c
  • Feng Z, Zhang L, Wang S, Hong Q (2020). Circular RNA circDLGAP4 exerts neuroprotective effects via modulating miR-134-5p/ CREB pathway in Parkinson’s disease. Biochemical and Biophysical Research Communications 522: 388-394. doi: 10.1016/j.bbrc.2019.11.102
  • Fisher BE, Li Q, Nacca A, Salem GJ, Song J et al. (2013). Treadmill exercise elevates striatal dopamine D2 receptor binding potential in patients with early Parkinson’s disease. Neuroreport 24: 509-514. doi: 10.1097/WNR.0b013e328361dc13
  • Gao H, Han Z, Huang S, Bai R, Ge X et al. (2017). Intermittent hypoxia caused cognitive dysfunction relate to miRNAs dysregulation in hippocampus. Behavioural Brain Research 335: 80-87. doi: 10.1016/j.bbr.2017.06.025
  • Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ et al. (2011). American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Medicine and Science in Sports and Exercise 43: 1334-1359. doi: 10.1249/MSS.0b013e318213fefb
  • Gokool A, Anwar F, Voineagu I (2020). The Landscape of Circular RNA Expression in the Human Brain. Biological Psychiatry 87: 294-304. doi: 10.1016/j.biopsych.2019.07.029
  • Gomes-Osman J, Cabral DF, Hinchman C, Jannati A, Morris TP et al. (2017). The effects of exercise on cognitive function and brain plasticity - a feasibility trial. Restorative Neurology and Neuroscience 35: 547-556. doi: 10.3233/RNN-170758
  • Guo M, Qiu J, Shen F, Wang S, Yu J et al. (2020a). Comprehensive analysis of circular RNA profiles in skeletal muscles of aging mice and after aerobic exercise intervention. Aging 12: 5071- 5090. doi: 10.18632/aging.102932
  • Guo M, Qiu J, Shen F, Wang S, Yu J et al. (2020b). Comprehensive analysis of circular RNA profiles in skeletal muscles of aging mice and after aerobic exercise intervention. Aging 12: 5071- 5090. doi: 10.18632/aging.102932
  • Haavik J, Almas B, Flatmark T (1997). Generation of reactive oxygen species by tyrosine hydroxylase: a possible contribution to the degeneration of dopaminergic neurons? Journal of Neurochemistry 68: 328-332. doi: 10.1046/j.1471- 4159.1997.68010328.x
  • Hanan M, Simchovitz A, Yayon N, Vaknine S, Kadener S (2020). A Parkinson’s disease Circ RNA s Resource reveals a link between circ SLC 8A1 and oxidative stress. EMBO Molecular Medicine 12.
  • Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B et al. (2013). Natural RNA circles function as efficient microRNA sponges. Nature 495: 384-388. doi: 10.1038/nature11993
  • Hubert T, Grimal S, Carroll P, Fichard-Carroll A (2009). Collagens in the developing and diseased nervous system. Cellular and Molecular Life Sciences : CMLS. 66: 1223-1238. doi: 10.1007/ s00018-008-8561-9
  • Klaperski S, von Dawans B, Heinrichs M, Fuchs R (2014). Effects of a 12-week endurance training program on the physiological response to psychosocial stress in men: a randomized controlled trial. Journal of Behavioral Medicine 37: 1118-1133. doi: 10.1007/s10865-014-9562-9
  • Koo JH, Jang YC, Hwang DJ, Um HS, Lee NH et al. (2017). Treadmill exercise produces neuroprotective effects in a murine model of Parkinson’s disease by regulating the TLR2/MyD88/NFkappaB signaling pathway. Neuroscience 356: 102-113. doi: 10.1016/j.neuroscience.2017.05.016
  • Li D, Wang Y, Jin X, Hu D, Xia C et al. (2020). NK cell-derived exosomes carry miR-207 and alleviate depression-like symptoms in mice. Journal of Neuroinflammation. 17: 126. doi: 10.1186/s12974-020-01787-4
  • Liu W, Li L, Liu S, Wang Z, Kuang H et al. (2019). MicroRNA Expression Profiling Screen miR-3557/324-Targeted CaMK/ mTOR in the Rat Striatum of Parkinson’s Disease in Regular Aerobic Exercise. BioMed Research International 2019: 7654798. doi: 10.1155/2019/7654798
  • Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408. doi: 10.1006/ meth.2001.1262
  • Marques O, Outeiro TF (2012). Alpha-synuclein: from secretion to dysfunction and death. Cell Death & Disease 3: e350. doi: 10.1038/cddis.2012.94
  • Maurus I, Hasan A, Roh A, Takahashi S, Rauchmann B et al. (2019). Neurobiological effects of aerobic exercise, with a focus on patients with schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 269: 499-515. doi: 10.1007/s00406- 019-01025-w
  • Meder D, Herz DM, Rowe JB, Lehericy S, Siebner HR (2019). The role of dopamine in the brain - lessons learned from Parkinson’s disease. NeuroImage 190: 79-93. doi: 10.1016/j. neuroimage.2018.11.021
  • Meredith GE, Rademacher DJ (2011). MPTP mouse models of Parkinson’s disease: an update. Journal of Parkinson’s Disease 1: 19-33. doi: 10.3233/JPD-2011-11023
  • Mo WL, Jiang JT, Zhang L, Lu QC, Li J et al. (2020). Circular RNA hsa_circ_0000467 Promotes the Development of Gastric Cancer by Competitively Binding to MicroRNA miR-326- 3p. BioMed Research International 2020: 4030826. doi: 10.1155/2020/4030826
  • Moylan S, Eyre HA, Maes M, Baune BT, Jacka FN et al. (2013). Exercising the worry away: how inflammation, oxidative and nitrogen stress mediates the beneficial effect of physical activity on anxiety disorder symptoms and behaviours. Neuroscience and Biobehavioral Reviews 37: 573-584. doi: 10.1016/j. neubiorev.2013.02.003
  • Patel A, Toia GV, Colletta K, Bradaric BD, Carvey PM et al. (2011). An angiogenic inhibitor, cyclic RGDfV, attenuates MPTPinduced dopamine neuron toxicity. Experimental Neurology 231: 160-170. doi: 10.1016/j.expneurol.2011.06.004
  • Piwecka M, Glazar P, Hernandez-Miranda LR, Memczak S, Wolf SA et al. (2017). Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357. doi: 10.1126/science.aam8526
  • Real CC, Garcia PC, Britto LRG (2017). Treadmill Exercise Prevents Increase of Neuroinflammation Markers Involved in the Dopaminergic Damage of the 6-OHDA Parkinson’s Disease Model. Journal of Molecular Neuroscience : MN. 63: 36-49. doi: 10.1007/s12031-017-0955-4
  • Ridgel AL, Peacock CA, Fickes EJ, Kim CH (2012). Active-assisted cycling improves tremor and bradykinesia in Parkinson’s disease. Archives of Physical Medicine and Rehabilitation. 93: 2049-2054. doi: 10.1016/j.apmr.2012.05.015
  • Sang Q, Liu X, Wang L, Qi L, Sun W et al. (2018). CircSNCA downregulation by pramipexole treatment mediates cell apoptosis and autophagy in Parkinson’s disease by targeting miR-7. Aging 10: 1281-1293. doi: 10.18632/aging.101466
  • Segura-Aguilar J, Paris I, Munoz P, Ferrari E, Zecca L et al. (2014). Protective and toxic roles of dopamine in Parkinson’s disease. Journal of Neurochemistry 129: 898-915. doi: 10.1111/ jnc.12686
  • Si Z, Hu K, Wang C, Jia L, Zhang X et al. (2016). The effects of neuromuscular facilitation techniques on osteoporosis of hemiplegia limbs and serum leptin level in patients or rats with cerebral infarction. Brain Injury 30: 474-479. doi: 10.3109/02699052.2016.1140809
  • Tysnes OB, Storstein A (2017). Epidemiology of Parkinson’s disease. Journal of Neural Transmission. 124: 901-905. doi: 10.1007/ s00702-017-1686-y
  • Veys L, Vandenabeele M, Ortuno-Lizaran I, Baekelandt V, Cuenca N et al. (2019). Retinal alpha-synuclein deposits in Parkinson’s disease patients and animal models. Acta Neuropathologica. 137: 379-395. doi: 10.1007/s00401-018-01956-z
  • Wang J, Zhang Q, Li S, Chen Z, Tan J et al. (2020). Low molecular weight fucoidan alleviates diabetic nephropathy by binding fibronectin and inhibiting ECM-receptor interaction in human renal mesangial cells. International Journal of Biological Macromolecules 150: 304-314. doi: 10.1016/j. ijbiomac.2020.02.087
  • Wang Z, Xu P, Chen B, Zhang Z, Zhang C et al. (2018). Identifying circRNA-associated-ceRNA networks in the hippocampus of Abeta1-42-induced Alzheimer’s disease-like rats using microarray analysis. Aging 10: 775-788. doi: 10.18632/ aging.101427
  • Wu PL, Lee M, Huang TT (2017). Effectiveness of physical activity on patients with depression and Parkinson’s disease: A systematic review. PLoS One 12: e0181515. doi: 10.1371/ journal.pone.0181515
  • Zaichick SV, McGrath KM, Caraveo G (2017). The role of Ca(2+) signaling in Parkinson’s disease. Disease Models & Mechanisms 10: 519-535. doi: 10.1242/dmm.028738
  • Zhai K, Liu B, Gao L (2020). Long-Noncoding RNA TUG1 Promotes Parkinson’s Disease via Modulating MiR-152-3p/PTEN Pathway. Human Gene Therapy doi: 10.1089/hum.2020.106
  • Zhai S, Shen W, Graves SM, Surmeier DJ (2019). Dopaminergic modulation of striatal function and Parkinson’s disease. Journal of Neural Transmission 126: 411-422. doi: 10.1007/ s00702-019-01997-y
  • Zhang P, Ha M, Li L, Huang X, Liu C (2020). MicroRNA-3064-5p sponged by MALAT1 suppresses angiogenesis in human hepatocellular carcinoma by targeting the FOXA1/CD24/Src pathway. Federation of American Societies for Experimental Biology 34: 66-81. doi: 10.1096/fj.201901834R
  • Zhao J, Chen C, Bell RL, Qing H, Lin Z (2019). Identification of HIVEP2 as a dopaminergic transcription factor related to substance use disorders in rats and humans. Translational Psychiatry 9: 247. doi: 10.1038/s41398-019-0573-8
  • Zill P, Buttner A, Eisenmenger W, Muller J, Moller HJ et al. (2009). Predominant expression of tryptophan hydroxylase 1 mRNA in the pituitary: a postmortem study in human brain. Neuroscience 159: 1274-1282. doi: 10.1016/j.neuroscience.2009.01.006
  • Zoladz JA, Majerczak J, Zeligowska E, Mencel J, Jaskolski A et al. (2014). Moderate-intensity interval training increases serum brain-derived neurotrophic factor level and decreases inflammation in Parkinson’s disease patients. Journal of Physiology and Pharmacology : Journal of the Polish Physiological Society 65: 441-448.
Turkish Journal of Biology-Cover
  • ISSN: 1300-0152
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Arşiv
Sayıdaki Diğer Makaleler

Design and in vitro, in vivo evaluation of antioxidant bioadhesive gels for burn treatment

Çetin PEKÇETİN, Evren ALGIN YAPAR, Göksel GÖKÇE, Alper BAĞRIYANIK, Sinem Yaprak KARAVANA, Gülşen AYBAR TURAL, Evren Homan GÖKÇE

siRNA-mediated stathmin1 silencing inhibits proliferation of prostate carcinoma cell line

Ebru ETEM ÖNALAN, Selcen GÖKTÜRK, Gökhan ARTAŞ, Asude AKSOY, Mustafa KOÇ, Ahmet TEKTEMUR, Asuman VAROĞLU

p110α activity at the M-to-G1 transition is critical for cellular proliferation and reentry into the cell cycle

Onur ÇİZMECİOĞLU

Transcriptome sequencing reveals circRNA expression profile in Parkinson’s disease-like mice after aerobic exercis

Chuan FU, Xiating LI, Lichun SUN, Tianlun FAN

Point-of-care diagnosis of cervical cancer: potential protein biomarkers in cervicovaginal fluid

Özgüç TAKMAZ, Mete GÜNGÖR, Ahmet Tarık BAYKAL, Büşra KÖSE

Cytoplasmically localized tRNA-derived fragments inhibit translation in Drosophila S2 cells

Bünyamin AKGÜL, Syed Muhammad HAMID