Deep-brain stimulation associates with improved microvascular integrity in the subthalamic nucleus in Parkinson's disease

Neurobiology of Disease

Volumn 74, Issue 1, 2015, Pages 392-405

  Pienaar, Ilse S ^a   Lee, Cecilia Heyne ^b   Elson, Joanna L ^c,d   McGuinness, Louisa ^a   Gentleman, Stephen M ^a   Kalaria, Raj N ^c   Dexter, David T ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d NORTH WEST UNIVERSITY   (South Africa)

Author keywords

Deep brain stimulation; Growth factor; Parkinson's disease; Subthalamic nucleus; Tight junction proteins; Vasculature

Indexed keywords

ANGIOGENIC FACTOR; CELL ADHESION MOLECULE; CLAUDIN 5; GLUCOSE TRANSPORTER 1; IMMUNOGLOBULIN G; OCCLUDIN; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; VASCULOTROPIN; SLC2A1 PROTEIN, HUMAN; VASCULOTROPIN A; VEGFA PROTEIN, HUMAN;

ADULT; AGED; ANGIOGENESIS; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PARAMETERS; BRAIN DEPTH STIMULATION; CAPILLARY ENDOTHELIAL CELL; CELL DENSITY; CELL JUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MICROGLIA; MICROVASCULATURE; MICROVESSEL ENDOTHELIAL CELL DENSITY; MICROVESSEL ENDOTHELIAL CELL INNER DIAMETER; MICROVESSEL ENDOTHELIAL CELL LENGTH; MICROVESSEL ENDOTHELIAL CELL THICKNESS; MIDDLE AGED; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SUBTHALAMIC NUCLEUS; UPREGULATION; VASCULAR DISEASE; BLOOD; COMPARATIVE STUDY; ENDOTHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; ORGAN SIZE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TREATMENT OUTCOME; VASCULARIZATION; VERY ELDERLY;

AGED; AGED, 80 AND OVER; DEEP BRAIN STIMULATION; ENDOTHELIAL CELLS; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TRANSPORTER TYPE 1; HUMANS; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MICROVESSELS; ORGAN SIZE; PARKINSON DISEASE; SUBTHALAMIC NUCLEUS; TIGHT JUNCTION PROTEINS; TREATMENT OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84923623232     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.12.006     Document Type: Article

References (74)

1. Abbott N.J., Patabendige A.A., Dolman D.E., Yusof S.R., Begley D.J. Structure and function of the blood-brain barrier. Neurobiol. Dis. 2010, 37:13-25.
2. Asanuma K., Tang C., Ma Y., Dhawan V., Mattis P., Edwards C., et al. Network modulation in the treatment of Parkinson's disease. Brain 2006, 129:2667-2678.
3. Bailey T.L., Rivara C.B., Rocher A.B., Hof P.R. The nature and effects of cortical microvascular pathology in aging and Alzheimer's disease. Neurol. Res. 2004, 26:573-578.
4. Ballabh P., Braun A., Nedergaard M. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiol. Dis. 2004, 16:1-13.
5. Berding G., Odin P., Brooks D.J., Nikkhah G., Matthies C., Peschel T., et al. Resting regional cerebral glucose metabolism in advanced Parkinson's disease studied in the off and on conditions with [18F]FDG-PET. Mov. Disord. 2001, 16:1014-1022.
6. Bergman H., Wichmann T., DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990, 249:1436-1438.
7. Bergman H., Wichmann T., Karmon B., DeLong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
8. Black J.E., Isaacs K.R., Anderson B.J., Alcantara A.A., Greenough W.T. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:5568-5572.
9. Bohnen N.I., Minoshima S., Giordani B., Frey K.A., Kuhl D.E. Motor correlates of occipital glucose hypometabolism in Parkinson's disease without dementia. Neurology 1999, 52:541-546.
10. Bradbury M.W. The blood-brain barrier. Exp. Physiol. 1993, 78:453-472.
11. Burke M.J., Nelson L., Slade J.Y., Oakley A.E., Khundakar A.A., Kalaria R.N. Morphometry of the hippocampal microvasculature in post-stroke and age-related dementias. Neuropathol. Appl. Neurobiol. 2014, 40:284-295.
12. Cavaglia M., Dombrowski S.M., Drazba J., Vasanji A., Bokesch P.M., Janigro D. Regional variation in brain capillary and vascular response to ischemia. Brain Res. 2001, 910:81-93.
13. Ceballos-Baumann A.O., Boecker H., Bartenstein P., von Falkenhayn I., Riescher H., Conrad B., et al. A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Arch. Neurol. 1999, 56:997-1003.
14. Chen X., Lan X., Roche I., Liu R., Geiger J.D. Caffeine protects against MPTP-induced blood-brain barrier dysfunction in mouse striatum. J. Neurochem. 2008, 107:1147-1157.
15. Chen B., Friedman B., Cheng Q., Tsai P., Schim E., Kleinfeld D., et al. Severe blood-brain barrier disruption and surrounding tissue injury. Stroke 2009, 40:e666-e674.
16. Cresswell P., Ackerman A.L., Giodini A., Peaper D.R., Wearsch P.A. Mechanisms of MHC class I-restricted antigen processing and cross presentation. Immunol. Rev. 2005, 207:145-157.
17. Cristante E., McArthur S., Mauro C., Maggioli E., Romero I.A., Wylezinska-Arridge M., et al. Identification of an essential endogenous regulator of blood-brain barrier integrity, and its pathological and therapeutic implications. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:832-841.
18. Deiana E., Vestweber D. The role of VE-cadherin in vascular morphogenesis and permeability control. Prog. Mol. Biol. Transl. Sci. 2013, 116:119-144.
19. Ding Y.H., Li J., Zhou Y., Rafols J.A., Clark J. Cerebral angiogenesis and expression of angiogenic factors in aging rats after exercise. Current Neurovasc. Res. 2006, 3:15-23.
20. Eberling J.L., Richardson B.C., Reed B.R., Wolfe N., Jagust W. Cortical glucose metabolism in Parkinson's disease without dementia. Neurobiol. Aging 1994, 15:329-335.
21. Furuse M., Hirase T., Itoh M., Nagafuchi A., Yonemura S., Tsukita S., et al. (1993). Occludin: a novel integral membrane protein localizing at tight junctions. J. Cell Biol. 1993, 123:1777-1788.
22. Glickstein S.B., Ilch C.P., Reis D.J., Golanov E.V. Stimulation of the subthalamic vasodilator area and fastigial nucleus independently protects the brain against focal ischemia. Brain Res. 2001, 912:47-59.
23. Guan J., Pavlovic D., Dalkie N., Waldvogel H.J., O'Carroll S.J., Green C.R., et al. Vascular degeneration in Parkinson's disease. Brain Pathol. 2012, 23:154-164.
24. Gupta D., Kurivilla A. Vascular parkinsonism: what makes it different?. Postgrad. Med. J. 2011, 87:829-836.
25. Harb R., Whiteus C., Freitas C., Grutzendler J. In vivo imaging of cerebral microvascular plasticity from birth to death. J. Cereb. Blood Flow Metab. 2013, 33:146-156.
26. Heinzer S., Kuhn G., Krucker T., Meyer E., Ulmann-Schuler A., Stamanoni M., et al. Novel three-dimensional analysis tool for vascular trees indicates complete micro-networks, not single capillaries, as the angiogenic endpoint in mice overexpressing human VEGF(165) in the brain. Neuroimage 2008, 39:1549-1558.
27. Hellsten J., Wennstrom M., Bengzon J., Mohapel P., Tingstrom A. Electroconvulsive seizures induce endothelial cell proliferation in adult rat hippocampus. Biol. Psychiatry 2004, 55:420-427.
28. Hill K.K., Campbell M.C., McNeely M.E., Karimi M., Ushe M., Tabbal S.D., et al. Cerebral blood flow responses to dorsal and ventral STN DBS correlate with gait and balance responses in Parkinson's disease. Exp. Neurol. 2013, 241:105-112.
29. Hu M.T.M., Taylor-Robinson S.D., Chaudhuri K.R., Bell J.D., Labbé C., Cunningham V.J., et al. Cortical dysfunction in non-demented Parkinson's disease patients. A combined 31P-MRS and 18FDG-PET study. Brain 2000, 123:340-352.
30. Kanaan N.M., Kordower J.H., Collier T.J. Age and region-specific responses of microglia, but not astrocytes, suggest a role in selective vulnerability of dopamine neurons after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure in monkeys. Glia 2008, 56:1199-1214.
31. Kreutzberg G.W. Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 1996, 19:312-318.
32. Lax N.Z., Pienaar I.S., Reeve A.K., Hepplewhite P.D., Jaros E., Taylor R.W., et al. Microangiopathy in the cerebellum of patients with mitochondrial DNA disease. Brain 2012, 135:1736-1750.
33. Lee S., Pienaar I.S. Disruption of the blood-brain barrier in Parkinson's disease: curse or route to a cure?. Front. Biosci. 2014, 19:272-280.
34. Limousin P., Krack P., Pollak P., Benazzouz A., Ardouin C., Hoffmann D., et al. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 1998, 339:1105-1111.
35. Lindvall O., Wahlberg L.U. Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson's disease?. Exp. Neurol. 2008, 209:82-88.
36. Marchesi V.T. Alzheimer's dementia begins as a disease of small blood vessels, damaged by oxidative-induced inflammation and dysregulated amyloid metabolism: implications for early detection and therapy. FASEB J. 2011, 25:5-13.
37. McGeer P.L., McGeer E.G. Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat. Disord. 2004, 10(Suppl. 1):S3-S7.
38. Miller W.C., DeLong M.R. Altered tonic activity of neurons in the globus pallidus and subthalamic nucleus in the primate MPTP model of parkinsonism. Vol. 32 of Advances in behavioural biology 1987, 415-427. Plenum Press, New York. M.B. Carpenter, A. Jayaraman (Eds.).
39. Mooradian A.D., Chung H.C., Shah G.N. GLUT-1 expression in the cerebra of patients with Alzheimer's disease. Neurobiol. Aging 1997, 18:469-474.
40. Nagai T., Kajita Y., Maesawa S., Nakatsubo D., Yoshida K., Kato K., et al. Preoperative regional cerebral blood flow and postoperative clinical improvement in patients with Parkinson's disease undergoing subthalamic nucleus deep brain stimulation. Neurol. Med. Chir. (Tokyo) 2012, 52:865-872.
41. Nakajima K., Kohsaka S. Microglia: activation and their significance in the central nervous system. J. Biochem. (Tokyo) 2001, 130:169-175.
42. Ngoga D., Mitchell R., Kausar J., Hodson J., Harries A., Pall H. Deep brain stimulation improves survival in severe Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 2014, 85:17-22.
43. Nitta T., Hata M., Gotoh S., Seo Y., Sasaki H., Hashimoto N., Furuse M., Tsukita S. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 2003, 161:653-660.
44. Otsuka M., Kuwabara Y., Ichiya Y., Hosokawa S., Sasaki M., Yoshida T., et al. Differentiating between multiple system atrophy and Parkinson's disease by positron emission tomography with 18F-dopa and 18F-FDG. Ann. Nucl. Med. 1997, 11:251-257.
45. Peppard R.F., Martin W.R., Clark C.M., Carr G.D., McGeer P.L., Calne D.B. Cortical glucose metabolism in Parkinson's and Alzheimer disease. J. Neurosci. Res. 1990, 27:561-568.
46. Péron J., Le Jeune F., Haegelen C., Dondaine T., Drapier D., Sauleau P., et al. Subthalamic nucleus stimulation affects theory of mind network: a PET study in Parkinson's disease. PLoS One 2010, 5:e9919.
47. Piert M., Koeppe R.A., Giordani B., Minoshima S., Kuhl D.E. Determination of regional rate constants from dynamic FDG-PET studies in Parkinson's disease. J. Nucl. Med. 1996, 37:1115-1122.
48. Pollak P., Benabid A.L., Gross C., Gao D.M., Laurent A., Benazzouz A., et al. Effects of the stimulation of the subthalamic nucleus in Parkinson disease. Rev. Neurol. (Paris) 1993, 149:175-176.
49. Rektor I., Goldemund D., Bednarik P., Sheardova K., Michalkova Z., Telecka S., Dufek M., et al. Impairment of brain vessels may contribute to mortality in patients with Parkinson's disease. Mov. Disord. 2012, 27:1169-1172.
50. Rodriguez M.C., Obeso J.A., Olanow C.W. Subthalamic nucleus-mediated excitotoxicity in Parkinson's disease: a target for neuroprotection. Ann. Neurol. 1998, 44:S175-S188.
51. Romijn H.J., van Uum J.F., Breedijk I., Emmering J., Radu I., Pool C.W. Double immunolabeling of neuropeptides in the human hypothalamus as analyzed by confocal laser scanning fluorescence microscopy. J. Histochem. Cytochem. 1999, 47:229-236.
52. Rosenstein J.M., Mani N., Khaibullina A., Krum J.M. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J. Neurosci. 2003, 23:11036-11044.
53. Schmitz C., Hof P.R. Design-based stereology in neuroscience. Neuroscience 2005, 130:813-831.
54. Schroeder U., Kuehler A., Lange K.W., Haslinger B., Tronnier V.M., Krause M., et al. Subthalamic nucleus stimulation affects a frontotemporal network: a PET study. Ann. Neurol. 2003, 54:445-450.
55. Segi-Nishida E., Warner-Schmidt J.L., Duman R.S. Electroconvulsive seizure and VEGF increase the proliferation of neural stem-like cells in rat hippocampus. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11352-11357.
56. Sestini S., Scotto di Luzio A., Ammannati F., De Cristofaro M.T., Passeri A., Martini S., et al. Changes in regional cerebral blood flow caused by deep-brain stimulation of the subthalamic nucleus in Parkinson's disease. J. Nucl. Med. 2002, 43:725-732.
57. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86:353-387.
58. Su P.C., Ma Y., Fukuda M., Mentis M.J., Tseng H.M., Yen R.F., et al. Metabolic changes following subthalamotomy for advanced Parkinson's disease. Ann. Neurol. 2001, 50:514-520.
59. Swain R.A., Harris A.B., Wiener E.C., Dutka M.V., Morris H.D., Theien B.E., et al. Prolonged exercise induces angiogenesis and increases cerebral blood volume in primary motor cortex of the rat. Neuroscience 2003, 117:1037-1046.
60. Tagliati M., Martin C., Alterman R. Lack of motor symptoms progression in Parkinson's disease patients with long-term bilateral subthalamic deep brain stimulation. Int. J. Neurosci. 2010, 120:717-723.
61. Tata D.A., Anderson B.J. A new method for the investigation of capillary structure. J. Neurosci. Methods 2002, 113:119-206.
62. Temel Y., Visser-Vandewalle V., Kaplan S., Kozan R., Daemen M.A., Blokland A., et al. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res. 2006, 1120:100-105.
63. Ting P., Masaoka H., Kuroiwa T., Wagner H., Fenton I., Klatzo I. Influence of blood-brain barrier opening to proteins on development of post-ischaemic brain injury. Neurol. Res. 1986, 8:146-151.
64. Vedam-Mai V., Gardner B., Okun M.S., Siebzehnrubl F.A., Kam M., Aponso P., et al. Increased precursor cell proliferation after deep brain stimulation for Parkinson's disease: a human study. PLoS One 2014, 9:e88770.
65. Wada K., Arai H., Takanashi M., Fukae J., Oizumi H., Yasuda T., et al. Expression levels of vascular endothelial growth factor and its receptors in Parkinson's disease. Neuroreport 2006, 17:705-709.
66. Wallace B.A., Ashkan K., Heise C.E., Foote K.D., Torres N., Mitrofanis J., et al. Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP treated monkeys. Brain 2007, 130:2129-2145.
67. Wang Y., Jin K., Mao X.O., Xie L., Banwait S., Marti H.H., et al. VEGF-overexpressing transgenic mice show enhanced post-ischemic neurogenesis and neuromigration. J. Neurosci. Res. 2007, 85:740-747.
68. Wang J., Ma Y.L., Huang Z.M., Sun Z.M., Guan Y.H., Zuo C.T. Modulation of metabolic brain function by bilateral subthalamic nucleus stimulation in the treatment of Parkinson's disease. J. Neurol. 2010, 257:72-78.
69. Warner-Schmidt J.L., Madsen T.M., Duman R.S. Electroconvulsive seizure restores neurogenesis and hippocampus-dependent fear memory after disruption by irradiation. Eur. J. Neurosci. 2008, 27:1485-1493.
70. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 2007, 150:963-976.
71. Wichmann T., DeLong M.R. Pathophysiology of Parkinson's disease: the MPTP primate model of the human disorder. Ann. N. Y. Acad. Sci. 2003, 991:199-213.
72. Wittchen E.S., Haskins J., Stevenson B.R. Protein interactions at the tight junction. Actin has multiple binding partners, and ZO-1 forms independent complexes with ZO-2 and ZO-3. J. Biol. Chem. 1999, 274:35179-35185.
73. Wu Z., Guo H., Chow N., Sallstrom J., Bell R.D., Deane A., et al. Role of MEOX2 homeobox gene in neurovascular dysfunction in Alzheimer's disease. Nat. Med. 2005, 11:959-965.
74. Zlokovic B.V. Neurovascular pathways to neurodegeneration in Alzheimer's disease and other disorders. Nat. Rev. Neurosci. 2011, 12:723-738.