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

Neurobiology of Disease

Volumn 94, Issue , 2016, Pages 95-105

  Padel, Thomas ^a   Özen, Ilknur ^a   Boix, Jordi ^a   Barbariga, Marco ^a   Gaceb, Abderahim ^a   Roth, Michaela ^a   Paul, Gesine ^a,b  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

6 Hydroxydopamine; Neurorestoration; Parkinson's disease; Pericyte; Platelet derived growth factor BB; Regulator of G protein signalling 5

Indexed keywords

MICROSOMAL AMINOPEPTIDASE; OXIDOPAMINE; PLATELET DERIVED GROWTH FACTOR BB; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; BECAPLERMIN; DOPAMINE; PLATELET DERIVED GROWTH FACTOR B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; DISEASE MODEL; DOPAMINERGIC SYSTEM; DORSAL STRIATUM; DORSOLATERAL STRIATUM; DRUG EFFECT; DRUG MECHANISM; DRUG RESPONSE; FOREBRAIN; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MALE; MOUSE; NEUROMODULATION; NEURORESTORATIVE EFFECT; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; OUTCOME ASSESSMENT; PARKINSON DISEASE; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT DURATION; VENTRAL STRIATUM; ANIMAL; CORPUS STRIATUM; DRUG EFFECTS; MEDIAL FOREBRAIN BUNDLE; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; DOPAMINE; MALE; MEDIAL FOREBRAIN BUNDLE; MICE, TRANSGENIC; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSON DISEASE; PERICYTES; PROTO-ONCOGENE PROTEINS C-SIS;

EID: 84976260728     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2016.06.002     Document Type: Article

References (47)

1. Armulik, A., et al. Endothelial/pericyte interactions. Circ. Res. 97 (2005), 512–523.
2. Armulik, A., et al. Pericytes regulate the blood-brain barrier. Nature 468 (2010), 557–561.
3. Barcia, C., et al. Increased plasma levels of TNF-alpha but not of IL1-beta in MPTP-treated monkeys one year after the MPTP administration. Parkinsonism Relat. Disord. 11 (2005), 435–439.
4. Berger, M., et al. Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood 105 (2005), 1094–1101.
5. Blume, S.R., et al. Stepping test in mice: a reliable approach in determining forelimb akinesia in MPTP-induced Parkinsonism. Exp. Neurol. 219 (2009), 208–211.
6. Boix, J., et al. A partial lesion model of Parkinson's disease in mice–characterization of a 6-OHDA-induced medial forebrain bundle lesion. Behav. Brain Res. 284 (2015), 196–206.
7. Bowenkamp, K.E., et al. 6-Hydroxydopamine induces the loss of the dopaminergic phenotype in substantia nigra neurons of the rat. A possible mechanism for restoration of the nigrostriatal circuit mediated by glial cell line-derived neurotrophic factor. Exp. Brain Res. 111 (1996), 1–7.
8. Carvey, P.M., et al. 6-Hydroxydopamine-induced alterations in blood-brain barrier permeability. Eur. J. Neurosci. 22 (2005), 1158–1168.
9. Chakroborty, D., et al. Dopamine stabilizes tumor blood vessels by up-regulating angiopoietin 1 expression in pericytes and Kruppel-like factor-2 expression in tumor endothelial cells. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 20730–20735.
10. Chen, X., et al. Caffeine protects against MPTP-induced blood-brain barrier dysfunction in mouse striatum. J. Neurochem. 107 (2008), 1147–1157.
11. Cho, H., et al. Pericyte-specific expression of Rgs5: implications for PDGF and EDG receptor signaling during vascular maturation. FASEB J. 17 (2003), 440–442.
12. Clapp, C., et al. Peptide hormone regulation of angiogenesis. Physiol. Rev. 89 (2009), 1177–1215.
13. de Rijk, M.C., et al. Prevalence of parkinsonism and Parkinson's disease in Europe: the EUROPARKINSON Collaborative Study. European Community Concerted Action on the Epidemiology of Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 62 (1997), 10–15.
14. Desai Bradaric, B., et al. Evidence for angiogenesis in Parkinson's disease, incidental Lewy body disease, and progressive supranuclear palsy. J. Neural Transm. 119 (2012), 59–71.
15. Di Matteo, P., et al. Enhanced expression of CD13 in vessels of inflammatory and neoplastic tissues. J. Histochem. Cytochem. 59 (2011), 47–59.
16. Dore-Duffy, P., Pericytes: pluripotent cells of the blood brain barrier. Curr. Pharm. Des. 14 (2008), 1581–1593.
17. Dore-Duffy, P., Cleary, K., Morphology and properties of pericytes. Methods Mol. Biol. 686 (2011), 49–68.
18. Farkas, E., et al. Pathological features of cerebral cortical capillaries are doubled in Alzheimer's disease and Parkinson's disease. Acta Neuropathol. 100 (2000), 395–402.
19. Faucheux, B.A., et al. Blood vessels change in the mesencephalon of patients with Parkinson's disease. Lancet 353 (1999), 981–982.
20. Fearnley, J.M., Lees, A.J., Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114:Pt 5 (1991), 2283–2301.
21. Frielingsdorf, H., et al. No evidence for new dopaminergic neurons in the adult mammalian substantia nigra. Proc. Natl. Acad. Sci. U. S. A. 101 (2004), 10177–10182.
22. Grealish, S., et al. Characterisation of behavioural and neurodegenerative changes induced by intranigral 6-hydroxydopamine lesions in a mouse model of Parkinson's disease. Eur. J. Neurosci. 31 (2010), 2266–2278.
23. Gunaje, J.J., et al. PDGF-dependent regulation of regulator of G protein signaling-5 expression and vascular smooth muscle cell functionality. Am. J. Phys. Cell Physiol. 301 (2011), C478–C489.
24. Huschak, G., et al. Changes in monocytic expression of aminopeptidase N/CD13 after major trauma. Clin. Exp. Immunol. 134 (2003), 491–496.
25. Janelidze, S., et al. Increased CSF biomarkers of angiogenesis in Parkinson disease. Neurology 85 (2015), 1834–1842.
26. Kordower, J.H., et al. Disease duration and the integrity of the nigrostriatal system in Parkinson's disease. Brain 136 (2013), 2419–2431.
27. Kortekaas, R., et al. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann. Neurol. 57 (2005), 176–179.
28. Kovac, A., et al. Brain microvascular pericytes are immunoactive in culture: cytokine, chemokine, nitric oxide, and LRP-1 expression in response to lipopolysaccharide. J. Neuroinflammation, 8, 2011, 139.
29. Nikkhah, G., et al. Platelet-derived growth factor promotes survival of rat and human mesencephalic dopaminergic neurons in culture. Exp. Brain Res. 92 (1993), 516–523.
30. Nisancioglu, M.H., et al. Generation and characterization of rgs5 mutant mice. Mol. Cell. Biol. 28 (2008), 2324–2331.
31. Ozen, I., et al. Perivascular mesenchymal stem cells in the adult human brain: a future target for neuroregeneration?. Clin. Transl. Med., 1, 2012, 30.
32. Ozen, I., et al. Brain pericytes acquire a microglial phenotype after stroke. Acta Neuropathol. 128 (2014), 381–396.
33. Ozerdem, U., et al. NG2 proteoglycan is expressed exclusively by mural cells during vascular morphogenesis. Dev. Dyn. 222 (2001), 218–227.
34. Paul, G., et al. The adult human brain harbors multipotent perivascular mesenchymal stem cells. PLoS One, 7, 2012, e35577.
35. Paul, G., et al. Safety and Efficacy of Recombinant Human Platelet derived Growth Factor BB (rhPDGF-BB) in Parkinson's Disease. 2013.
36. Paul, G., et al. Safety and tolerability of intracerebroventricular PDGF-BB in Parkinson's disease patients. J. Clin. Invest. 125 (2015), 1339–1346.
37. Pietz, K., et al. Protective effect of platelet-derived growth factor against 6-hydroxydopamine-induced lesion of rat dopaminergic neurons in culture. Neurosci. Lett. 204 (1996), 101–104.
38. Sagare, A.P., et al. Pericyte loss influences Alzheimer-like neurodegeneration in mice. Nat. Commun., 4, 2013, 2932.
39. Schallert, T., et al. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39 (2000), 777–787.
40. Shimizu, F., et al. Pericyte-derived glial cell line-derived neurotrophic factor increase the expression of claudin-5 in the blood-brain barrier and the blood-nerve barrier. Neurochem. Res. 37 (2012), 401–409.
41. Ungerstedt, U., Arbuthnott, G.W., Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res. 24 (1970), 485–493.
42. Wada, K., et al. Expression levels of vascular endothelial growth factor and its receptors in Parkinson's disease. Neuroreport 17 (2006), 705–709.
43. West, M.J., Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 22 (1999), 51–61.
44. Winkler, E.A., et al. Pericyte-specific expression of PDGF beta receptor in mouse models with normal and deficient PDGF beta receptor signaling. Mol. Neurodegener., 5, 2010, 32.
45. Yang, P., et al. String Vessel Formation is Increased in the Brain of Parkinson Disease. J. Parkinsons Dis. 5 (2015), 821–836.
46. Yasuda, T., et al. Correlation between levels of pigment epithelium-derived factor and vascular endothelial growth factor in the striatum of patients with Parkinson's disease. Exp. Neurol. 206 (2007), 308–317.
47. Zachrisson, O., et al. Restorative effects of platelet derived growth factor-BB in rodent models of Parkinson's disease. J. Parkinsons Dis. 1 (2011), 49–63.