Skip to main content
SpringerLink
Log in

Adult Endogenous Dopaminergic Neuroregeneration Against Parkinson’s Disease: Ideal Animal Models?

  • Review Article
  • Published:
Neurotoxicity Research Aims and scope Submit manuscript

Abstract

Parkinson’s disease (PD) is the second most common neurodegenerative disease. The etiology of PD remains an enigma with no available disease modifying treatment or cure. Pharmacological compensation is the only quality of life improving treatments available. Endogenous dopaminergic neuroregeneration has recently been considered a plausible therapeutic strategy for PD. However, researchers have to first decipher the complexity of adult endogenous neuroregeneration. This raises the need of animal models to understand the underlying molecular basis. Mammalian models with highly conserved genetic homology might aid researchers to identify specific molecular mechanisms. However, the scarcity of adult neuroregeneration potential in mammals obfuscates such investigations. Nowadays, non-mammalian models are gaining popularity due to their explicit ability to neuroregenerate naturally without the need of external enhancements, yet these non-mammals have a much diverse gene homology that critical molecular signals might not be conserved across species. The present review highlights the advantages and disadvantages of both mammalian and non-mammalian animal models that can be essentially used to study the potential of endogenous DpN regeneration against PD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agid Y, Blin J Nerve cell death in degenerative diseases of the central nervous system: clinical aspects. In: Ciba Found Symp, 1987. Wiley Online Library, pp 3-29

  • Alvarez-Buylla A, Kirn JR, Nottebohm F (1990) Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249:1444–1447

    CAS  PubMed  Google Scholar 

  • Anacker C, Denny CA, Hen R (2015) Regulation of hippocampal memory traces by neurogenesis. Neurogenesis 2:e1025180. https://doi.org/10.1080/23262133.2015.1025180

    Article  PubMed  PubMed Central  Google Scholar 

  • Andrew R, Watson D, Best S, Midgley J, Wenlong H et al (1993) The determination of hydroxydopamines and other trace amines in the urine of parkinsonian patients and normal controls. Neurochem Res 18:1175–1177

    CAS  PubMed  Google Scholar 

  • Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970

    CAS  PubMed  Google Scholar 

  • Assal F, Spahr L, Hadengue A, Rubbici-Brandt L, Burkhard PR (1998) Tolcapone and fulminant hepatitis. The Lancet 352:958. https://doi.org/10.1016/s0140-6736(05)61511-5

    Article  CAS  Google Scholar 

  • Baltazar T, Dinis-Oliveira RJ, Duarte JA, de Lourdes BM, Carvalho F (2013) Paraquat research: do recent advances in limiting its toxicity make its use safer? Br J Pharmacol 168:44–45

    CAS  PubMed  PubMed Central  Google Scholar 

  • Banati RB, Daniel SE, Blunt SB (1998) Glial pathology but absence of apoptotic nigral neurons in long-standing Parkinson’s disease. Mov Disord 13:221–227

    CAS  PubMed  Google Scholar 

  • Banks WA (2016) From blood-brain barrier to blood-brain interface: new opportunities for CNS drug delivery. Nat Rev Drug Discov. https://doi.org/10.1038/nrd.2015.21

    Article  PubMed  Google Scholar 

  • Barata-Antunes S, Teixeira FG, Mendes-Pinheiro B, Domingues AV, Vilaça-Faria H et al (2020) Impact of aging on the 6-OHDA-induced rat model of Parkinson’s disease. Int J Mol Sci 21:3459. https://doi.org/10.3390/ijms21103459

    Article  CAS  PubMed Central  Google Scholar 

  • Barbosa JS, Sanchez-Gonzalez R, Di Giaimo R, Baumgart EV, Theis FJ et al (2015) Live imaging of adult neural stem cell behavior in the intact and injured zebrafish brain. Science 348:789–793

    CAS  PubMed  Google Scholar 

  • Barreiro-Iglesias A, Mysiak KS, Scott AL, Reimer MM, Yang Y et al (2015) Serotonin promotes development and regeneration of spinal motor neurons in zebrafish. Cell Rep 13:924–932

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartzokis G, Cummings JL, Sultzer D, Henderson VW, Nuechterlein KH et al (2003) White matter structural integrity in healthy aging adults and patients with Alzheimer disease: a magnetic resonance imaging study. Arch Neurol 60:393–398. https://doi.org/10.1001/archneur.60.3.393

    Article  PubMed  Google Scholar 

  • Berg DA, Kirkham M, Beljajeva A, Knapp D, Habermann B et al (2010) Efficient regeneration by activation of neurogenesis in homeostatically quiescent regions of the adult vertebrate brain. Development 137:4127–4134

    CAS  PubMed  Google Scholar 

  • Berg DA, Kirkham M, Wang H, Frisén J, Simon A (2011) Dopamine controls neurogenesis in the adult salamander midbrain in homeostasis and during regeneration of dopamine neurons. Cell Stem Cell 8:426–433

    CAS  PubMed  Google Scholar 

  • Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV et al (2000) Chronic systemic pesticide exposure reproduces features of Parkinson’s disease. Nat Neurosci 3:1301–1306

    CAS  PubMed  Google Scholar 

  • Blanchet PJ, Calon F, Morissette M, Tahar AH, Bélanger N et al (2004) Relevance of the MPTP primate model in the study of dyskinesia priming mechanisms. Parkinsonism Relat D 10:297–304

    Google Scholar 

  • Blesa J, Przedborski S (2014) Parkinson’s disease: animal models and dopaminergic cell vulnerability. Front Neuroanat 8:155

    PubMed  PubMed Central  Google Scholar 

  • Bretaud S, Lee S, Guo S (2004) Sensitivity of zebrafish to environmental toxins implicated in Parkinson’s disease. Neurotoxicol Teratol 26:857–864

    CAS  PubMed  Google Scholar 

  • Büeler H (2009) Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson’s disease. Exp Neurol 218:235–246

    PubMed  Google Scholar 

  • Buhidma Y, Rukavina K, Chaudhuri KR, Duty S (2020) Potential of animal models for advancing the understanding and treatment of pain in Parkinson’s disease. NPJ Parkinsons Dis 6:1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Busby ER, Roch GJ, Sherwood NM (2010) Endocrinology of zebrafish: a small fish with a large gene pool. In: Fish Physiology, vol 29. Elsevier, pp 173-247

  • Caldwell LJ, Davies NO, Cavone L, Mysiak KS, Semenova SA et al (2019) Regeneration of dopaminergic neurons in adult zebrafish depends on immune system activation and differs for distinct populations. J Neurosci 39:4694–4713

    PubMed  PubMed Central  Google Scholar 

  • Caneda-Ferrón B, De Girolamo LA, Costa T, Beck KE, Layfield R et al (2008) Assessment of the direct and indirect effects of MPP+ and dopamine on the human proteasome: implications for Parkinson’s disease aetiology. J Neurochem 105:225–238

    PubMed  Google Scholar 

  • Cannon JR, Geghman KD, Tapias V, Sew T, Dail MK et al (2013) Expression of human E46K-mutated α-synuclein in BAC-transgenic rats replicates early-stage Parkinson’s disease features and enhances vulnerability to mitochondrial impairment. Exp Neurol 240:44–56

    CAS  PubMed  Google Scholar 

  • Cave JW, Baker H (2009) Dopamine systems in the forebrain. Development and Engineering of Dopamine Neurons. Springer , New York, NY, pp 15–35

    Google Scholar 

  • Cenci MA, Ohlin KE, Rylander D (2009) Plastic effects of L-DOPA treatment in the basal ganglia and their relevance to the development of dyskinesia. Parkinsonism Relat D 15:S59–S63

    Google Scholar 

  • Chaudhuri KR, Healy DG, Schapira AH (2006) Non-motor symptoms of Parkinson’s disease: diagnosis and management. Lancet Neurol 5:235–245

    PubMed  Google Scholar 

  • Chen M, Reed RR, Lane AP (2017) Acute inflammation regulates neuroregeneration through the NF-κB pathway in olfactory epithelium. PNAS 114:8089–8094

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Y-C, Priyadarshini M, Panula P (2009) Complementary developmental expression of the two tyrosine hydroxylase transcripts in zebrafish. Histochem Cell Biol 132:375–381

    CAS  PubMed  Google Scholar 

  • Chernoff EA, Stocum DL, Nye HL, Cameron JA (2003) Urodele spinal cord regeneration and related processes. Dev Dyn 226:295–307

    PubMed  Google Scholar 

  • Choi SJ, Panhelainen A, Schmitz Y, Larsen KE, Kanter E et al (2015) Changes in neuronal dopamine homeostasis following 1-methyl-4-phenylpyridinium (MPP+) exposure. J Biol Chem 290:6799–6809

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choi W-S, Palmiter RD, Xia Z (2011) Loss of mitochondrial complex I activity potentiates dopamine neuron death induced by microtubule dysfunction in a Parkinson’s disease model. J Cell Biol 192:873–882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S et al (2009) Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7:e1000112. https://doi.org/10.1371/journal.pbio.1000112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costa ROd, Gadelha-Filho CVJ, Costa AEMd, Feitosa ML, Araújo DPd et al (2017) The treadmill exercise protects against dopaminergic neuron loss and brain oxidative stress in parkinsonian rats. Oxid Med Cell Longev. https://doi.org/10.1155/2017/2138169

    Article  PubMed  PubMed Central  Google Scholar 

  • Costello S, Cockburn M, Bronstein J, Zhang X, Ritz B (2009) Parkinson’s disease and residential exposure to maneb and paraquat from agricultural applications in the central valley of California. Am J Epidemiol 169:919–926

    PubMed  PubMed Central  Google Scholar 

  • Crane AM, Bhattacharya SK (2013) The use of bromodeoxyuridine incorporation assays to assess corneal stem cell proliferation. In: Corneal Regenerative Medicine. Springer, pp 65-70

  • Curtis MA, Penney EB, Pearson AG, van Roon-Mom WM, Butterworth NJ et al (2003) Increased cell proliferation and neurogenesis in the adult human Huntington’s disease brain. PNAS 100:9023–9027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Da Fonseca TL, Correia A, Hasselaar W, Van Der Linde HC, Willemsen R et al (2013) The zebrafish homologue of Parkinson’s disease ATP13A2 is essential for embryonic survival. Brain Res Bull 90:118–126

    Google Scholar 

  • Dass B, Iravani MM, Jackson M, Engber T, Galdes A et al (2002) Behavioural and immunohistochemical changes following supranigral administration of sonic hedgehog in 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-treated common marmosets. Neuroscience 114:99–109

    CAS  PubMed  Google Scholar 

  • Dawson TM, Golde TE, Lagier-Tourenne C (2018) Animal models of neurodegenerative diseases. Nat Neurosci 21:1370–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson TM, Ko HS, Dawson VL (2010) Genetic animal models of Parkinson’s disease. Neuron 66:646–661

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Hemptinne C, Swann NC, Ostrem JL, Ryapolova-Webb ES, San Luciano M et al (2015) Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson’s disease. Nat Neurosci 18:779–786

    PubMed  PubMed Central  Google Scholar 

  • de Oliveira-Carlos V, Ganz J, Hans S, Kaslin J, Brand M (2013) Notch receptor expression in neurogenic regions of the adult zebrafish brain. PLoS ONE 8:e73384. https://doi.org/10.1371/journal.pone.0073384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Y, Guo Q, Shan M, Wu Y, Huang S et al (2016) Spatial and temporal distribution of dopaminergic neurons during development in zebrafish. Front Neuroanat 10:115. https://doi.org/10.3389/fnana.2016.00115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Y, Zhang X, Tao Q, Chen S, Le W (2013) Adeno-associated virus type 2 vector-mediated glial cell line-derived neurotrophic factor gene transfer induces neuroprotection and neuroregeneration in a ubiquitin-proteasome system impairment animal model of Parkinson’s disease. Neurodegener Dis 11:113–128

    CAS  PubMed  Google Scholar 

  • Ehringer H, Hornykiewicz O (1960) Verteilung von Noradrenalin und Dopamin (3-Hydroxytyramin) im Gehirn des Menschen und ihr Verhalten bei Erkrankungen des extrapyramidalen Systems. Klin Wochenschr 38:1236–1239

    CAS  PubMed  Google Scholar 

  • Ekstrand MI, Galter D (2009) The MitoPark mouse–an animal model of Parkinson’s disease with impaired respiratory chain function in dopamine neurons. Parkinsonism Relat D 15:S185–S188

    Google Scholar 

  • Elsworth J, Taylor J, Sladek J, Collier T, Redmond D et al (2000) Striatal dopaminergic correlates of stable parkinsonism and degree of recovery in old-world primates one year after MPTP treatment. Neuroscience 95:399–408

    Google Scholar 

  • Faivre F, Joshi A, Bezard E, Barrot M (2019) The hidden side of Parkinson’s disease: studying pain, anxiety and depression in animal models. Neurosci Biobehav Rev 96:335–352

    PubMed  Google Scholar 

  • Felten DL, Sladek JR Jr (1983) Monoamine distribution in primate brain V. Monoaminergic nuclei: anatomy, pathways and local organization. Brain Res Bull 10:171–284

    CAS  PubMed  Google Scholar 

  • Ferrari E, Capucciati A, Prada I, Zucca FA, D’Arrigo G et al (2017) Synthesis, structure characterization, and evaluation in microglia cultures of neuromelanin analogues suitable for modeling Parkinson’s disease. ACS Chem Neurosci 8:501–512

    CAS  PubMed  Google Scholar 

  • Fleming SM, Zhu C, Fernagut P-O, Mehta A, DiCarlo CD et al (2004) Behavioral and immunohistochemical effects of chronic intravenous and subcutaneous infusions of varying doses of rotenone. Exp Neurol 187:418–429

    CAS  PubMed  Google Scholar 

  • French V, Bryant PJ, Bryant SV (1976) Pattern regulation in epimorphic fields. Science 193:969–981

    CAS  PubMed  Google Scholar 

  • Freundlieb N, François C, Tandé D, Oertel WH, Hirsch EC et al (2006) Dopaminergic substantia nigra neurons project topographically organized to the subventricular zone and stimulate precursor cell proliferation in aged primates. J Neurosci 26:2321–2325

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galant S, Furlan G, Coolen M, Dirian L, Foucher I et al (2016) Embryonic origin and lineage hierarchies of the neural progenitor subtypes building the zebrafish adult midbrain. Dev Biol 420:120–135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Garbayo E, Ansorena E, Lana H, del Mar C-A, Marcilla I et al (2016) Brain delivery of microencapsulated GDNF induces functional and structural recovery in parkinsonian monkeys. Biomaterials 110:11–23

    CAS  PubMed  Google Scholar 

  • Gash DM, Zhang Z, Ai Y, Grondin R, Coffey R et al (2005) Trophic factor distribution predicts functional recovery in parkinsonian monkeys. Ann Neurol 58:224–233

    CAS  PubMed  Google Scholar 

  • Godwin JW, Pinto AR, Rosenthal NA (2013) Macrophages are required for adult salamander limb regeneration. PNAS 110:9415–9420

    CAS  PubMed  PubMed Central  Google Scholar 

  • Götz M, Barde Y-A (2005) Radial glial cells: defined and major intermediates between embryonic stem cells and CNS neurons. Neuron 46:369–372

    PubMed  Google Scholar 

  • Grant HC, Lantos P, Parkinson C (1980) Cerebral damage in paraquat poisoning. Histopathology 4:185–195

    CAS  PubMed  Google Scholar 

  • Grimmig B, Daly L, Subbarayan M, Hudson C, Williamson R et al (2018) Astaxanthin is neuroprotective in an aged mouse model of Parkinson’s disease. Oncotarget 9:10388. https://doi.org/10.18632/oncotarget.23737

    Article  PubMed  Google Scholar 

  • Grondin R, Zhang Z, Yi A, Cass WA, Maswood N et al (2002) Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 125:2191–2201

    PubMed  Google Scholar 

  • Hafkemeijer A, Altmann-Schneider I, de Craen AJ, Slagboom PE, van der Grond J et al (2014) Associations between age and gray matter volume in anatomical brain networks in middle-aged to older adults. Aging Cell 13:1068–1074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haines DE Neuroanatomy: an atlas of structures, sections, and systems vol 153. vol 2004. Lippincott Williams & Wilkins,

  • Hameed LS, Berg DA, Belnoue L, Jensen LD, Cao Y et al (2015) Environmental changes in oxygen tension reveal ROS-dependent neurogenesis and regeneration in the adult newt brain. Elife 4:34. https://doi.org/10.7554/eLife.08422

    Article  Google Scholar 

  • Hirsch L, Jette N, Frolkis A, Steeves T, Pringsheim T (2016) The incidence of Parkinson’s disease: a systematic review and meta-analysis. Neuroepidemiology 46:292–300

    PubMed  Google Scholar 

  • Hosamani R, Krishna G, Muralidhara, (2016) Standardized Bacopa monnieri extract ameliorates acute paraquat-induced oxidative stress, and neurotoxicity in prepubertal mice brain. Nutr Neurosci 19:434–446

    PubMed  Google Scholar 

  • Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hruscha A, Krawitz P, Rechenberg A, Heinrich V, Hecht J et al (2013) Efficient CRISPR/Cas9 genome editing with low off-target effects in zebrafish. Development 140:4982–4987

    CAS  PubMed  Google Scholar 

  • Huang H, Chen L (2015) Neurorestorative process, law, and mechanisms. Journal of Neurorestoratology 3:23–30. https://doi.org/10.2147/JN.S74139

    Article  Google Scholar 

  • Imokawa Y, Simon A, Brockes JP (2004) A critical role for thrombin in vertebrate lens regeneration. Philosophical Transactions of the Royal Society of London B: Biological Sciences 359:765–776

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson-Lewis V, Przedborski S (2007) Protocol for the MPTP mouse model of Parkinson’s disease. Nat Protoc 2:141–151

    CAS  PubMed  Google Scholar 

  • Joers V, Tansey MG, Mulas G, Carta AR (2017) Microglial phenotypes in Parkinson’s disease and animal models of the disease. Prog Neurobiol 155:57–75

    CAS  PubMed  Google Scholar 

  • Kah O, Chambolle P, Thibault J, Geffard M (1984) Existence of dopaminergic neurons in the preoptic region of the goldfish. Neurosci Lett 48:293–298

    CAS  PubMed  Google Scholar 

  • Kalueff AV, Stewart AM, Gerlai R (2014) Zebrafish as an emerging model for studying complex brain disorders. Trends Pharmacol Sci 35:63–75

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaslin J, Kroehne V, Benato F, Argenton F, Brand M (2013) Development and specification of cerebellar stem and progenitor cells in zebrafish: from embryo to adult. Neural Dev 8:9. https://doi.org/10.1186/1749-8104-8-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaslin J, Panula P (2001) Comparative anatomy of the histaminergic and other aminergic systems in zebrafish (Danio rerio). Journal of Comparative Neurology 440:342–377

    CAS  PubMed  Google Scholar 

  • Kastner A, Hirsch E, Lejeune O, Javoy-Agid F, Rascol O et al (1992) Is the vulnerability of neurons in the substantia nigra of patients with Parkinson’s disease related to their neuromelanin content? J Neurochem 59:1080–1089

    CAS  PubMed  Google Scholar 

  • Kells AP, Eberling J, Su X, Pivirotto P, Bringas J et al (2010) Regeneration of the MPTP-lesioned dopaminergic system after convection-enhanced delivery of AAV2-GDNF. J Neurosci 30:9567–9577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kirkham M, Berg DA, Simon A (2011) Microglia activation during neuroregeneration in the adult vertebrate brain. Neurosci Lett 497:11–16

    CAS  PubMed  Google Scholar 

  • Kirkham M, Joven A (2015) Studying newt brain regeneration following subtype specific neuronal ablation. Salamanders in Regeneration Research: Methods and Protocols 1290:91–99

    Google Scholar 

  • Kishimoto N, Shimizu K, Sawamoto K (2012) Neuronal regeneration in a zebrafish model of adult brain injury. Dis Model Mech 5:200–209

    CAS  PubMed  Google Scholar 

  • Kizil C, Kaslin J, Kroehne V, Brand M (2012) Adult neurogenesis and brain regeneration in zebrafish. Dev Neurobiol 72:429–461

    PubMed  Google Scholar 

  • Konieczny J, Czarnecka A, Lenda T, Kamińska K, Antkiewicz-Michaluk L (2017) The significance of rotational behavior and sensitivity of striatal dopamine receptors in hemiparkinsonian rats: a comparative study of lactacystin and 6-OHDA. Neuroscience 340:308–318

    CAS  PubMed  Google Scholar 

  • Kriks S, Shim J-W, Piao J, Ganat YM, Wakeman DR et al (2011) Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson’s disease. Nature 480:547–551

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar A, Leinisch F, Kadiiska MB, Corbett J, Mason RP (2016) Formation and implications of alpha-synuclein radical in maneb-and paraquat-induced models of Parkinson’s disease. Mol Neurobiol 53:2983–2994

    CAS  PubMed  Google Scholar 

  • Kyritsis N, Kizil C, Zocher S, Kroehne V, Kaslin J et al (2012) Acute inflammation initiates the regenerative response in the adult zebrafish brain. Science 338:1353–1356

    CAS  PubMed  Google Scholar 

  • LaMonica BE, Lui JH, Hansen DV, Kriegstein AR (2013) Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat Commun 4:1665. https://doi.org/10.1038/ncomms2647

    Article  CAS  PubMed  Google Scholar 

  • Langston J, Forno L, Tetrud J, Reeves A, Kaplan J et al (1999) Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine exposure. Ann Neurol 46:598–605

    CAS  PubMed  Google Scholar 

  • Langston JW, Ballard P, Tetrud JW, Irwin I (1983) Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219:979–980

    CAS  PubMed  Google Scholar 

  • Lazarini F, Gabellec M-M, Moigneu C, De Chaumont F, Olivo-Marin J-C et al (2014) Adult neurogenesis restores dopaminergic neuronal loss in the olfactory bulb. J Neurosci 34:14430–14442

    PubMed  PubMed Central  Google Scholar 

  • LeClair EE, Topczewski J (2010) Development and regeneration of the zebrafish maxillary barbel: a novel study system for vertebrate tissue growth and repair. PLoS ONE 5:e8737. https://doi.org/10.1371/journal.pone.0008737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee DA, Yoo S, Pak T, Salvatierra J, Velarde E et al (2014) Dietary and sex-specific factors regulate hypothalamic neurogenesis in young adult mice. Front Neurosci 8:157. https://doi.org/10.3389/fnins.2014.00157

    Article  PubMed  PubMed Central  Google Scholar 

  • Li C, Jackson RM (2002) Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol 282:C227–C241

    CAS  PubMed  Google Scholar 

  • Liao C-H, Chen S-Y, Kuo J-S, Pang C-Y (2013) Reduction of motor disorder in 6-OHDA-induced severe parkinsonism rats by post treatment with granulocyte-colony stimulating factor. Chin J Physiol 56:147–154

    CAS  PubMed  Google Scholar 

  • Lim KL, Ng CH (2009) Genetic models of Parkinson disease. Biochim Biophys Acta-Molecular Basis of Disease 1792:604–615

    CAS  Google Scholar 

  • Lindsey BW, Darabie A, Tropepe V (2012) The cellular composition of neurogenic periventricular zones in the adult zebrafish forebrain. Journal of Comparative Neurology 520:2275–2316

    PubMed  Google Scholar 

  • Lindsey BW, Hall ZJ, Heuzé A, Joly J-S, Tropepe V et al (2018) The role of neuro-epithelial-like and radial-glial stem and progenitor cells in development, plasticity, and repair. Prog Neurobiol 170:99–114

    CAS  PubMed  Google Scholar 

  • Lu X-H, Fleming SM, Meurers B, Ackerson LC, Mortazavi F et al (2009) Bacterial artificial chromosome transgenic mice expressing a truncated mutant Parkin exhibit age-dependent hypokinetic motor deficits, dopaminergic neuron degeneration, and accumulation of proteinase K-resistant α-synuclein. J Neurosci 29:1962–1976

    PubMed  PubMed Central  Google Scholar 

  • Luthman J, Fredriksson A, Sundström E, Jonsson G, Archer T (1989) Selective lesion of central dopamine or noradrenaline neuron systems in the neonatal rat: motor behavior and monoamine alterations at adult stage. Behav Brain Res 33:267–277

    CAS  PubMed  Google Scholar 

  • Maheras AL, Dix B, Carmo OM, Young AE, Gill VN et al. (2018) Genetic pathways of neuroregeneration in a novel mild traumatic brain injury model in adult zebrafish. eNeuro 5:ENEURO. 0208–0217.2017 doi:https://doi.org/10.1523/ENEURO.0208-17.2017.

  • Matsui H (2017) Dopamine system, cerebellum, and nucleus ruber in fish and mammals. Dev Growth Differ 59:219–227

    CAS  PubMed  Google Scholar 

  • Mattam U, Jagota A (2015) Daily rhythms of serotonin metabolism and the expression of clock genes in suprachiasmatic nucleus of rotenone-induced Parkinson’s disease male Wistar rat model and effect of melatonin administration. Biogerontology 16:109–123

    CAS  PubMed  Google Scholar 

  • McGeer PL, Itagaki S, Boyes BE, McGeer E (1988) Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson’s and Alzheimer’s disease brains. Neurology 38:1285–1285

    CAS  PubMed  Google Scholar 

  • Merkle FT, Mirzadeh Z, Alvarez-Buylla A (2007) Mosaic organization of neural stem cells in the adult brain. Science 317:381–384

    CAS  PubMed  Google Scholar 

  • Mochizuki H (2011) Adult neurogenesis in Parkinson’s disease. Neurogenesis in the Adult Brain II. Springer, Tokyo, pp 23–36

    Google Scholar 

  • Moreira CG, Barbiero JK, Ariza D, Dombrowski PA, Sabioni P et al (2012) Behavioral, neurochemical and histological alterations promoted by bilateral intranigral rotenone administration: a new approach for an old neurotoxin. Neurotox Res 21:291–301

    CAS  PubMed  Google Scholar 

  • Morest DK (1970) A study of neurogenesis in the forebrain of opossum pouch young. Zeitschrift für Anatomie und Entwicklungsgeschichte 130:265–305

    CAS  PubMed  Google Scholar 

  • Morin N, Grégoire L, Gomez-Mancilla B, Gasparini F, Di Paolo T (2010) Effect of the metabotropic glutamate receptor type 5 antagonists MPEP and MTEP in parkinsonian monkeys. Neuropharmacology 58:981–986

    CAS  PubMed  Google Scholar 

  • Muñoz-Manchado AB, Villadiego J, Romo-Madero S, Suárez-Luna N, Bermejo-Navas A et al (2016) Chronic and progressive Parkinson’s disease MPTP model in adult and aged mice. J Neurochem 136:373–387

    PubMed  Google Scholar 

  • Nandhagopal R, McKeown MJ, Stoessl AJ (2008) Invited article: functional imaging in Parkinson disease. Neurology 70:1478–1488

    CAS  PubMed  Google Scholar 

  • Naughton C, O’Toole D, Kirik D, Dowd E (2017) Interaction between subclinical doses of the Parkinson’s disease associated gene, α-synuclein, and the pesticide, rotenone, precipitates motor dysfunction and nigrostriatal neurodegeneration in rats. Behav Brain Res 316:160–168

    CAS  PubMed  Google Scholar 

  • Nonnekes J, Timmer MH, Vries NM, Rascol O, Helmich RC et al (2016) Unmasking levodopa resistance in Parkinson’s disease. Mov Disord 31:1602–1609

    CAS  PubMed  Google Scholar 

  • Noristani H, Meadows R, Olabarria M, Verkhratsky A, Rodríguez J (2011) Increased hippocampal CA1 density of serotonergic terminals in a triple transgenic mouse model of Alzheimer’s disease: an ultrastructural study. Cell Death Dis 2:e210. https://doi.org/10.1038/cddis.2011.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nunes MC, Roy NS, Keyoung HM, Goodman RR, McKhann G et al (2003) Identification and isolation of multipotential neural progenitor cells from the subcortical white matter of the adult human brain. Nat Med 9:439–447

    CAS  PubMed  Google Scholar 

  • Nunes ME, Müller TE, Braga MM, Fontana BD, Quadros VA et al (2016) Chronic treatment with paraquat induces brain injury, changes in antioxidant defenses system, and modulates behavioral functions in zebrafish. Mol Neurobiol 54:3925–3934

    PubMed  Google Scholar 

  • Nyholm D, Askmark H, Gomes-Trolin C, Knutson T, Lennernäs H et al (2003) Optimizing levodopa pharmacokinetics: intestinal infusion versus oral sustained-release tablets. Clin Neuropharmacol 26:156–163

    CAS  PubMed  Google Scholar 

  • O’Sullivan SS, Williams DR, Gallagher DA, Massey LA, Silveira-Moriyama L et al (2008) Nonmotor symptoms as presenting complaints in Parkinson’s disease: a clinicopathological study. Mov Disord 23:101–106

    PubMed  Google Scholar 

  • Okun MS (2012) Deep-brain stimulation for Parkinson’s disease. N Engl J Med 367:1529–1538

    CAS  PubMed  Google Scholar 

  • Olanow CW (2000) Tolcapone and hepatotoxic effects. Arch Neurol 57:263–267

    CAS  PubMed  Google Scholar 

  • Padel T, Özen I, Boix J, Barbariga M, Gaceb A et al (2016) Platelet-derived growth factor-BB has neurorestorative effects and modulates the pericyte response in a partial 6-hydroxydopamine lesion mouse model of Parkinson’s disease. Neurobiol Dis 94:95–105

    CAS  PubMed  Google Scholar 

  • Palfi S, Leventhal L, Chu Y, Ma SY, Emborg M et al (2002) Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration. J Neurosci 22:4942–4954

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paredes-Rodriguez E, Vegas-Suarez S, Morera-Herreras T, De Deurwaerdere P, Miguelez C (2020) The noradrenergic system in Parkinson’s disease. Front Pharmacol. https://doi.org/10.3389/fphar.2020.00435

    Article  PubMed  PubMed Central  Google Scholar 

  • Parent A, Levesque M, Parent M (2001) A re-evaluation of the current model of the basal ganglia. Parkinsonism Relat D 7:193–198

    CAS  Google Scholar 

  • Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802–813

    PubMed  Google Scholar 

  • Parish CL, Beljajeva A, Arenas E, Simon A (2007) Midbrain dopaminergic neurogenesis and behavioural recovery in a salamander lesion-induced regeneration model. Development 134:2881–2887

    CAS  PubMed  Google Scholar 

  • Parker MO, Brock AJ, Walton RT, Brennan CH (2014) The role of zebrafish (Danio rerio) in dissecting the genetics and neural circuits of executive function. Frontiers in Neural Circuits 7:63. https://doi.org/10.3389/fncir.2013.00063

    Article  Google Scholar 

  • Patton EE, Zon LI (2001) The art and design of genetic screens: zebrafish. Nat Rev Genet 2:956–966

    CAS  PubMed  Google Scholar 

  • Perese D, Ulman J, Viola J, Ewing S, Bankiewicz K (1989) A 6-hydroxydopamine-induced selective parkinsonian rat model. Brain Res 494:285–293

    CAS  PubMed  Google Scholar 

  • Petkó M, Orosz V (1996) Distribution of somatostatin-immunoreactive structures in the central nervous system of the frog, Rana esculenta. J Hirnforsch 37:109–120

    PubMed  Google Scholar 

  • Petzinger GM, Fisher B, Hogg E, Abernathy A, Arevalo P et al (2006) Behavioral motor recovery in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine-lesioned squirrel monkey (Saimiri sciureus): Changes in striatal dopamine and expression of tyrosine hydroxylase and dopamine transporter proteins. J Neurosci Res 83:332–347

    CAS  PubMed  Google Scholar 

  • Politis M, Wu K, Loane C, Quinn NP, Brooks DJ et al (2010) Serotonergic neurons mediate dyskinesia side effects in Parkinson’s patients with neutral transplants. Sci Transl Med 2:38ra46-38ra46

    PubMed  Google Scholar 

  • Pont-Sunyer C, Hotter A, Gaig C, Seppi K, Compta Y et al (2015) The onset of nonmotor symptoms in Parkinson’s disease (the ONSET PD study). Mov Disord 30:229–237

    PubMed  Google Scholar 

  • Potashkin J, Blume S, Runkle N (2010) Limitations of animal models of Parkinson’s disease. Parkinson’s Dis. https://doi.org/10.4061/2011/658083

    Article  Google Scholar 

  • Przedborski S, Jackson-Lewis V, Naini AB, Jakowec M, Petzinger G et al (2001) The parkinsonian toxin 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP): a technical review of its utility and safety. J Neurochem 76:1265–1274

    CAS  PubMed  Google Scholar 

  • Przedborski S, Vila M (2003) The 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model. Ann N Y Acad Sci 991:189–198

    CAS  PubMed  Google Scholar 

  • Przedbroski S, Leviver M, Jiang H, Ferreira M, Jackson-Lewis V et al (1995) Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by instrastriatal injection of 6-hydroxydopamine. Neuroscience 67:631–647

    Google Scholar 

  • Ramachandran R, Zhao X-F, Goldman D (2011) Ascl1a/Dkk/β-catenin signaling pathway is necessary and glycogen synthase kinase-3β inhibition is sufficient for zebrafish retina regeneration. PNAS 108:15858–15863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Razgado-Hernandez LF, Espadas-Alvarez AJ, Reyna-Velazquez P, Sierra-Sanchez A, Anaya-Martinez V et al (2015) The transfection of BDNF to dopamine neurons potentiates the effect of dopamine D3 receptor agonist recovering the striatal innervation, dendritic spines and motor behavior in an aged rat model of Parkinson’s disease. PLoS ONE 10:e0117391. https://doi.org/10.1371/journal.pone.0117391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riederer P (1976) Time course of nigrostriatal degeneration in Parkinson’s disease. J Neural Transm 38:277–301

    CAS  PubMed  Google Scholar 

  • Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316–330

    CAS  PubMed  Google Scholar 

  • Rojo AI, Cavada C, de Sagarra MR, Cuadrado A (2007) Chronic inhalation of rotenone or paraquat does not induce Parkinson’s disease symptoms in mice or rats. Exp Neurol 208:120–126

    CAS  PubMed  Google Scholar 

  • Roth BL, Zanettini R, Antonini A, Gatto G, Gentile R et al (2007) Valvular heart disease and the use of dopamine agonists for Parkinson’s disease. N Engl J Med. https://doi.org/10.1056/NEJMoa054830

    Article  PubMed  Google Scholar 

  • Rothenaigner I, Krecsmarik M, Hayes JA, Bahn B, Lepier A et al (2011) Clonal analysis by distinct viral vectors identifies bona fide neural stem cells in the adult zebrafish telencephalon and characterizes their division properties and fate. Development 138:1459–1469

    CAS  PubMed  Google Scholar 

  • Sachs C, Jonsson G (1975) Mechanisms of action of 6-hydroxydopamine. Biochem Pharmacol 24:1–8

    CAS  PubMed  Google Scholar 

  • S Salari S, Bagheri M (2019) In vivo, in vitro and pharmacologic models of Parkinson's disease. Physiol Res 68

  • Sánchez-Camacho C, Marín O, Smeets WJ, Ten Donkelaar HJ, González A (2001) Descending supraspinal pathways in amphibians. II. Distribution and origin of the catecholaminergic innervation of the spinal cord. Journal of Comparative Neurology 434:209–232

    PubMed  Google Scholar 

  • Santiago RM, Barbieiro J, Lima MM, Dombrowski PA, Andreatini R et al (2010) Depressive-like behaviors alterations induced by intranigral MPTP, 6-OHDA, LPS and rotenone models of Parkinson’s disease are predominantly associated with serotonin and dopamine. Prog Neuropsychopharmacol Biol Psychiatry 34:1104–1114

    CAS  PubMed  Google Scholar 

  • Sarath Babu N, Murthy CLN, Kakara S, Sharma R, Swamy B et al (2016) 1-Methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine induced Parkinson’s disease in zebrafish. Proteomics 16:1407–1420

    CAS  PubMed  Google Scholar 

  • Schlachetzki JC, Winkler J (2015) The innate immune system in Parkinson’s disease: a novel target promoting endogenous neuroregeneration. Neural Regen Res 10:704–706

    PubMed  PubMed Central  Google Scholar 

  • Schmidt N, Ferger B (2001) Neurochemical findings in the MPTP model of Parkinson’s disease. J Neural Transm 108:1263–1282

    CAS  PubMed  Google Scholar 

  • Schmidt R, Strahle U, Scholpp S (2013) Neurogenesis in zebrafish-from embryo to adult. Neural Dev 8:8104–8108

    Google Scholar 

  • Schmitz Y, Castagna C, Mrejeru A, Lizardi-Ortiz JE, Klein Z et al (2013) Glycine transporter-1 inhibition promotes striatal axon sprouting via NMDA receptors in dopamine neurons. J Neurosci 33:16778–16789

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schober A (2004) Classic toxin-induced animal models of Parkinson’s disease: 6-OHDA and MPTP. Cell Tissue Res 318:215–224

    PubMed  Google Scholar 

  • Senoh S, Creveling CR, Udenfriend S, Witkop B (1959) Chemical, enzymatic and metabolic studies on the mechanism of oxidation of dopamine1. J Am Chem Soc 81:6236–6240

    CAS  Google Scholar 

  • Senoh S, Witkop B (1959) Non-enzymatic conversions of dopamine to norepinephrine and trihydroxyphenethylamines1. J Am Chem Soc 81:6222–6231

    CAS  Google Scholar 

  • Shimizu K, Ohtaki K, Matsubara K, Aoyama K, Uezono T et al (2001) Carrier-mediated processes in blood–brain barrier penetration and neural uptake of paraquat. Brain Res 906:135–142

    CAS  PubMed  Google Scholar 

  • Sidorova YA, Volcho KP, Salakhutdinov NF (2019) Neuroregeneration in Parkinson’s disease: from proteins to small molecules. Curr Neuropharmacol 17:268–287

    CAS  PubMed  PubMed Central  Google Scholar 

  • Simon A, Berg D, Kirkham M Not lost in translation: Sensing the loss and filling the gap during regeneration. In: Seminars in Cell & Developmental Biology, 2009. vol 6. Elsevier, pp 691-696

  • Somayajulu-Niţu M, Sandhu JK, Cohen J, Sikorska M, Sridhar T et al (2009) Paraquat induces oxidative stress, neuronal loss in substantia nigra region and Parkinsonism in adult rats: neuroprotection and amelioration of symptoms by water-soluble formulation of coenzyme Q 10. BMC Neurosci 10:88. https://doi.org/10.1186/1471-2202-10-88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sotoyama H, Iwakura Y, Oda K, Sasaoka T, Takei N et al (2017) Striatal hypodopamine phenotypes found in transgenic mice that overexpress glial cell line-derived neurotrophic factor. Neurosci Lett 654:99–106

    CAS  PubMed  Google Scholar 

  • Stamatovic SM, Martinez-Revollar G, Hu A, Choi J, Keep RF et al (2019) Decline in Sirtuin-1 expression and activity plays a critical role in blood-brain barrier permeability in aging. Neurobiol Dis 126:105–116

    CAS  PubMed  Google Scholar 

  • Steinbeck JA, Choi SJ, Mrejeru A, Ganat Y, Deisseroth K et al (2015) Optogenetics enables functional analysis of human embryonic stem cell-derived grafts in a Parkinson’s disease model. Nat Biotechnol 33:204–209

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strand NS, Hoi KK, Phan TM, Ray CA, Berndt JD et al (2016) Wnt/β-catenin signaling promotes regeneration after adult zebrafish spinal cord injury. Biochem Biophys Res Commun 477:952–956

    CAS  PubMed  Google Scholar 

  • Tabar V, Studer L (2014) Pluripotent stem cells in regenerative medicine: challenges and recent progress. Nat Rev Genet 15:82–92

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tandé D, Höglinger G, Debeir T, Freundlieb N, Hirsch EC et al (2006) New striatal dopamine neurons in MPTP-treated macaques result from a phenotypic shift and not neurogenesis. Brain 129:1194–1200

    PubMed  Google Scholar 

  • Tay TL, Ronneberger O, Ryu S, Nitschke R, Driever W (2011) Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat Commun 2:171. https://doi.org/10.1038/ncomms1171

    Article  CAS  PubMed  Google Scholar 

  • Than-Trong E, Bally-Cuif L (2015) Radial glia and neural progenitors in the adult zebrafish central nervous system. Glia 63:1406–1428

    PubMed  Google Scholar 

  • Thiruchelvam M, Powers J, Cory-Slechta D, Richfield E (2004) Risk factors for dopaminergic neuron loss in human α-synuclein transgenic mice. Eur J Neurosci 19:845–854

    CAS  PubMed  Google Scholar 

  • Tillet Y (1994) Catecholaminergic neuronal systems in the diencephalon of mammals, vol 207. Cambridge University Press, Cambridge

    Google Scholar 

  • Tintner R, Manian P, Gauthier P, Jankovic J (2005) Pleuropulmonary fibrosis after long-term treatment with the dopamine agonist pergolide for Parkinson disease. Arch Neurol 62:1290–1295

    PubMed  Google Scholar 

  • Tranzer J, Thoenen H (1968) An electron microscopic study of selective, acute degeneration of sympathetic nerve terminals after administration of 6-hydroxydopamine. Experientia 24:155–156

    CAS  PubMed  Google Scholar 

  • Trist BG, Hare DJ, Double KL (2019) Oxidative stress in the aging substantia nigra and the etiology of Parkinson’s disease. Aging Cell 18:e13031. https://doi.org/10.1111/acel.13031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Kampen JM, Eckman CB (2006) Dopamine D3 receptor agonist delivery to a model of Parkinson’s disease restores the nigrostriatal pathway and improves locomotor behavior. J Neurosci 26:7272–7280

    PubMed  PubMed Central  Google Scholar 

  • Vecchia DD, Schamne MG, Ferro MM, Santos AFCd, Latyki CL et al (2015) Effects of Hypericum perforatum on turning behavior in an animal model of Parkinson’s disease. Braz J Pharm Sci 51:111–115

    CAS  Google Scholar 

  • Vijayanathan Y, Lim FT, Lim SM, Long CM, Tan MP et al (2017) 6-OHDA-lesioned adult zebrafish as a useful Parkinson’s disease model for dopaminergic neuroregeneration. Neurotox Res 32:496–508

    CAS  PubMed  Google Scholar 

  • Vila M, Vukosavic S, Jackson-Lewis V, Neystat M, Jakowec M et al (2000) α-Synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J Neurochem 74:721–729

    CAS  PubMed  Google Scholar 

  • Wan J, Goldman D (2016) Retina regeneration in zebrafish. Curr Opin Genet Dev 40:41–47

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Liu W, Yang J, Wang F, Sima Y et al (2017) Parkinson’s disease-like motor and non-motor symptoms in rotenone-treated zebrafish. NeuroToxicology 58:103–109

    CAS  PubMed  Google Scholar 

  • Ward RJ, Zucca FA, Duyn JH, Crichton RR, Zecca L (2014) The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol 13:1045–1060

    CAS  PubMed  PubMed Central  Google Scholar 

  • Worlitzer MM, Viel T, Jacobs AH, Schwamborn JC (2013) The majority of newly generated cells in the adult mouse substantia nigra express low levels of doublecortin, but their proliferation is unaffected by 6-OHDA-induced nigral lesion or minocycline-mediated inhibition of neuroinflammation. Eur J Neurosci 38:2684–2692

    PubMed  Google Scholar 

  • Xi Y, Noble S, Ekker M (2011) Modeling neurodegeneration in zebrafish. Curr Neurol Neurosci Rep 11:274–282

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu K, Di Luca D, Orrú M, Xu Y, Chen J-F et al (2016) Neuroprotection by caffeine in the MPTP model of Parkinson’s disease and its dependence on adenosine A2A receptors. Neuroscience 322:129–137

    CAS  PubMed  Google Scholar 

  • Yamamoto K, Vernier P (2011) The evolution of dopamine systems in chordates. Front Neuroanat 5:21. https://doi.org/10.3389/fnana.2011.00021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanettini R, Antonini A, Gatto G, Gentile R, Tesei S et al (2007) Valvular heart disease and the use of dopamine agonists for Parkinson’s disease. N Engl J Med 356:39–46

    CAS  PubMed  Google Scholar 

  • Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337–341

    PubMed  Google Scholar 

  • Zecca L, Wilms H, Geick S, Claasen J-H, Brandenburg L-O et al (2008) Human neuromelanin induces neuroinflammation and neurodegeneration in the rat substantia nigra: implications for Parkinson’s disease. Acta Neuropathol 116:47–55

    CAS  PubMed  Google Scholar 

  • Zhang W, Phillips K, Wielgus AR, Liu J, Albertini A et al (2011) Neuromelanin activates microglia and induces degeneration of dopaminergic neurons: implications for progression of Parkinson’s disease. Neurotox Res 19:63–72

    PubMed  Google Scholar 

  • Zhao Y-Z, Jin R-R, Yang W, Xiang Q, Yu W-Z et al (2016) Using gelatin nanoparticle mediated intranasal delivery of neuropeptide substance P to enhance neuro-recovery in hemiparkinsonian rats. PLoS ONE 11:e0148848. https://doi.org/10.1371/journal.pone.0148848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu C, Vourc’h P, Fernagut PO, Fleming SM, Lacan S et al (2004) Variable effects of chronic subcutaneous administration of rotenone on striatal histology. Journal of Comparative Neurology 478:418–426

    CAS  PubMed  Google Scholar 

  • Zucca FA, Segura-Aguilar J, Ferrari E, Muñoz P, Paris I et al (2017) Interactions of iron, dopamine and neuromelanin pathways in brain aging and Parkinson’s disease. Prog Neurobiol 155:96–119

    CAS  PubMed  Google Scholar 

  • Zucca FA, Vanna R, Cupaioli FA, Bellei C, De Palma A et al (2018) Neuromelanin organelles are specialized autolysosomes that accumulate undegraded proteins and lipids in aging human brain and are likely involved in Parkinson’s disease. NPJ Parkinsons Dis 4:1–23

    CAS  Google Scholar 

Download references

Funding

This work was supported by the Ministry of Higher Education Malaysia [600-RMI/FRGS 5/3 (0078/2016)].

Author information

Authors and Affiliations

  1. Collaborative Drug Discovery Research (CDDR) Group and Brain Degeneration and Therapeutics Group, Faculty of Pharmacy, Universiti Teknologi MARA (UiTM) Cawangan Selangor, Kampus Puncak Alam, 42300, Bandar Puncak Alam, Selangor Darul Ehsan, Malaysia

    Yuganthini Vijayanathan, Siong Meng Lim, Fei Ting Lim, Abu Bakar Abdul Majeed & Kalavathy Ramasamy

  2. Department of Medicine, Faculty of Medicine, Universiti Malaya, 50603, Kuala Lumpur, Malaysia

    Yuganthini Vijayanathan & Maw Pin Tan

Authors
  1. Yuganthini Vijayanathan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Siong Meng Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maw Pin Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fei Ting Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abu Bakar Abdul Majeed
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kalavathy Ramasamy
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YV: investigation, visualization, writing-original draft, writing-review and editing; KR: conceptualization, funding acquisition, project administration, supervision, writing-review and editing; SML: conceptualization, supervision, writing-review and editing; FTL: conceptualization, writing-review and editing; ABAM: writing-review and editing; MPT: supervision, writing-review and editing.

Corresponding author

Correspondence to Kalavathy Ramasamy.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vijayanathan, Y., Lim, S.M., Tan, M.P. et al. Adult Endogenous Dopaminergic Neuroregeneration Against Parkinson’s Disease: Ideal Animal Models?. Neurotox Res 39, 504–532 (2021). https://doi.org/10.1007/s12640-020-00298-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12640-020-00298-7

Keywords

Search

Navigation