Calbindin content and differential vulnerability of midbrain efferent dopaminergic neurons in macaques

Frontiers in Neuroanatomy

Volumn 8, Issue DEC, 2014, Pages

  Dopeso Reyes, Iria G ^a,b   Rico, Alberto J ^a,b   Roda, Elvira ^a,b   Sierra, Salvador ^a,b   Pignataro, Diego ^a,b   Lanz, Maria ^a   Sucunza, Diego ^a   Chang Azancot, Luis ^a   Lanciego, Jose L ^a,b  

^a UNIVERSITY OF NAVARRA   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED SOBRE ENFERMEDADES NEURODEGENERATIVAS CIBERNED   (Spain)

Author keywords

Calbindin; MPTP; Neuronal tracers; Neuroprotection; Nigroextrastriatal pathway; Parkinson s disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CALBINDIN; CHOLERA TOXIN; FLUOROGOLD; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAUDATE NUCLEUS; CENTRAL NERVOUS SYSTEM; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EFFERENT NERVE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MACACA FASCICULARIS; MALE; MESENCEPHALON; NEUROPROTECTION; NIGROEXTRASTRIATAL SYSTEM; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PALLIDOTOMY; PARKINSON DISEASE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PUTAMEN; SUBSTANTIA NIGRA PARS COMPACTA; VENTRAL TEGMENTUM;

EID: 84938054206     PISSN: 16625129     EISSN: 16625129     Source Type: Journal    
DOI: 10.3389/fnana.2014.00146     Document Type: Article

References (58)

1. Afonso-Oramas, D., Cruz-Muros, I., Alvarez de la Rosa, D., Abreu, P., Giraldez, T., Castro-Hernandez, J., et al. (2009). Dopamine transporter glycosylation correlates with the vulnerability of midbrain dopaminergic cells in Parkinson’s disease. Neurobiol Dis. 36, 494-508. doi: 10.1016/j.nbd.2009.09.002
2. Anaya-Martinez, V., Martinez-Marcos, A., Martinez-Fong, D., Aceves, J., and Erlij, D. (2006). Substantia nigra compacta neurons that innervate the reticular thalamic nucleus in the rat also project to striatum or globus pallidus: implica­tions for abnormal motor behavior. Neuroscience 143, 477-486. doi: 10.1016/j.neuroscience.2006.08.033
3. Caudle, W. M., Richardson, J. R., Wang, M. Z., Taylor, T. N., Guillot, T. S., McCormack, A. L., et al. (2007). Reduced vesicular storage of dopamine causes progressive nigrostriatal neurodegeneration. J. Neurosci. 27, 8138-8148. doi: 10. 1523/jneurosci.0319-07.2007
4. Choi, W. S., Lee, E., Lim, J., and Oh, Y. J. (2008). Calbindin-D28K prevents drug-induced dopaminergic neuronal death byinhibiting caspase and calpain activity. Biochem. Biophys. Res. Commun. 371, 127-131. doi: 10.1016/j.bbrc.2008.04.020
5. Cossette, M., Levesque, M., and Parent, A. (1999). Extrastriatal dopaminer­gic innervation of human basal ganglia. Neurosci. Res. 34, 51-54. doi: 10. 1016/s0168-0102(99)00029-2
6. Cragg, S. J., Baufreton, J., Xue, Y., Bolam, J. P., and Bevan, M. D. (2004). Synaptic release of dopamine in the subthalamic nucleus. Eur. J. Neurosci. 20, 1788-1802. doi: 10.1111/j.1460-9568.2004.03629.x
7. Damier, P., Hirsch, E. C., Agid, Y., and Gaybriel, A. M. (1999a). The substantia nigra of the human brain. I. Nigrosomes and the nigral matrix, a compartmental organization based on calbindin D(28K) immunohistochemistry. Brain 122, 1421-1436. doi: 10.1093/brain/122.8.1421
8. Damier, P., Hirsch, E. C., Agid, Y., and Gaybriel, A. M. (1999b). The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 122, 1437-1448. doi: 10.1093/brain/122.8.1437
9. Davey, G. P., and Bolanos, J. P. (2013). Peroxiredoxin 5 links mitocondrial redox signalling with calcium dynamics: impacto n Parkinson’s disease. J. Neurochem. 125, 332-333. doi: 10.1111/jnc.12171
10. Fallon, J. H., and Moore, R. Y. (1978). Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180, 545-580. doi: 10.1002/cne.901800310
11. Fitzpatrick, E., Ashkan, K., Wallace, B. A., Benabid, A. L., and Mitrofanis, J. (2005). Differential survival patterns among midbrain dopaminergic cells of MPTP-treated monkeys and 6OHDA-lesioned rats. Anat. Embryol. (Berl) 210, 101-123. doi: 10.1007/s00429-005-0003-y
12. Francis, C., Savy, C., Jan, C., Tande, D., Hirsch, E. C., and Yelnik, J. (2000). Dopaminergic innervation of the subthalamic nucleus in the normal state, in MPTP-treated monkeys and in Parkinson’s disease patients. J. Comp. Neurol. 425, 121-129. doi: 10.1002/1096-9861(20000911)425:1<121::aid-cne10>3.0. co;2-g
13. Gerfen, C. R., Baimbridge, K. G., and Miller, J. J. (1985). The neostriatal mosaic: compartmental distribution ofcalcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. Proc. Natl. Acad. Sci. USA 82, 8780-8784. doi: 10.1073/pnas.82.24.8780
14. Gerfen, C. R., Baimbridge, K. G., and Thibault, J. (1987). The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J. Neurosci. 7, 3935-3944
15. German, D. C., Dubach, M., Askari, S., Speciale, S. G., and Bowden, D. M. (1988). 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced parkinsonian syndrome in Macaca fascicularis: which midbrain dopaminergic neurons are lost? Neu­roscience 24, 161-174. doi: 10.1016/0306-4522(88)90320-x
16. German, D. C., Manave, K., Smith, W. K., Woodward, D. J., andSaper, C. B. (1989). Midbrain dopaminergic cell loss in Parkinson’s disease: computer visualization. Ann. Neurol. 26, 507-514. doi: 10.1002/ana.410260403
17. German, D. C., Manaye, K. F., Sonsalla, P. K., and Brooks, B. A. (1992). Midbrain dopaminergic cell loss in Parkinson’s disease and MPTP-induced parkinsonism: sparing of calbindin-D28k-containing cells. Ann. N Y Acad. Sci. 648, 42-62. doi: 10.1111/j.1749-6632.1992.tb24523.x
18. German, D. C., Nelson, E. L., Liang, C. L., Speciale, S. G., Sinton, C. M., and Sonsalla, P. K. (1996). The neurotoxin MPTP causes degeneration of specific nucleus A8, A9 and A10 dopaminergic neurons in the mouse. Neurodegeneration 5, 299-312. doi: 10.1006/neur.1996.0041
19. Grace, A. A., and Bunney, B. S. (1983). Intracellular and extracellular electrophys­iology of nigral dopaminergic neurons—1, Identification and characterization. Neuroscience 10, 301-315. doi: 10.1016/0306-4522(83)90135-5
20. Haber, S. N., and Fudge, J. L. (1997). The primate substantia nigra and VTA: integrative circuitry and function. Crit. Rev. Neurobiol. 11, 323-342. doi: 10. 1615/critrevneurobiol.v11.i4.40
21. Harrington, K. A., Augood, S. J., Kingsbury, A. E., Foster, O. J., and Emson, P. C. (1996). Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson’s dis­ease. BrainRes. Mol. BrainRes. 36, 157-162. doi: 10.1016/0169-328x(95)00278-z
22. Hassani, O. K., Francis, C., Yelnik, J., and Feger, J. (1997). Evidence for a dopaminergic innervation of the subthalamic nucleus in the rat. Brain Res. 749, 88-94. doi: 10.1016/s0006-8993(96)01167-5
23. Hedreen, J. C. (1999). Tyrosine hydroxylase-immunoreactive elements in the human globus pallidus and subthalamic nucleus. J. Comp. Neurol. 409, 400-410. doi: 10.1002/(sici)1096-9861(19990705)409:3<400::aid-cne5>3.0.co;2-4
24. Hurley, M. J., Brandon, B., Gentleman, S. M., and Dexter, D. T. (2013). Parkinson’s disease is associated with altered expression of CaV1 channels and calcium-binding proteins. Brain 136, 2077-2097. doi: 10.1093/brain/awt134
25. Ito, H., Goto, S., Sakamoto, S., and Hirano, A. (1992). Calbindin-D28k in the basal ganglia of patients with parkinsonism. Ann. Neurol. 32, 543-550. doi: 10. 1002/ana.410320410
26. Jackson-Lewis, V., Jakowec, M., Burke, R. E., and Przedborski, S. (1995). Time course and morphology of dopaminergic neuronal death caused by the neuro­toxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Neurodegeneration 4,257­-269. doi: 10.1016/1055-8330(95)90015-2
27. Jan, C., Francis, C., Tande, D., Yelnik, J., Tremblay, L., Agid, Y., et al. (2000). Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients. Eur. J. Neurosci. 12, 4525-4535. doi: 10. 1111/j.1460-9568.2000.01351.x
28. Kurlan, R., Kim, M. H., and Gash, D.M. (1991). Oral levodopadose-response study in MPTP-induced hemiparkinsonian monkeys: assessment with a new rating scale for monkey parkinsonism. Mov. Disord. 6, 111-118. doi: 10.1002/mds. 870060205
29. Lanciego, J. L., and Vazquez, A. (2012). The basal ganglia and thalamus of the long­tailed macaque in stereotaxic coordinates. A template atlas based on coronal, sagittal and horizontal brain sections. Brain Struct. Funct. 217, 613-666. doi: 10. 1007/s00429-011-0370-5
30. Lavoie, B., and Parent, A. (1991). Dopaminergic neurons expressing calbindin in normal and parkinsonian monkeys. Neuroreport 2, 601-604. doi: 10. 1097/00001756-199110000-00012
31. Lavoie, B., Smith, Y., and Parent, A. (1989). Dopaminergic innervation of the basal ganglia in the squirrel monkey as revealed by tyrosine hydroxylase immunohis-tochemistry. J. Comp. Neurol. 289, 36-52. doi: 10.1002/cne.902890104
32. Liang, C. L., Sinton, C. M., Sonsalla, P. K., and German, D. C. (1996). Mid­brain dopaminergic neurons in the mouse that contain calbindin-D28k exhibit reduced vulnerability to MPTP-induced neurodegeneration. Neurodegeneration 5, 313-318. doi: 10.1006/neur.1996.0042
33. Lindvall, O., and Bjorklund, A. (1979). Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway. Brain Res. 172, 169-173. doi: 10.1016/0006-8993(79)90907-7
34. Liu, Y., Peter, D., Roghani, A., Schuldiner, S., Prive, G. G., Eisenberg, D., et al. (1992). A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell 70, 539-551. doi: 10.1016/0092-8674(92)90425-c
35. Lu, L., Neff, F., Fischer, D. A., Henze, C., Hirsch, E. C., Oertel, W. H., et al. (2006). Regional vulnerability of mesencephalic dopaminergic neurons prone to degenerate in Parkinson’s disease: a post-mortem study in human control subjects. Neurobiol. Dis. 23, 409-421. doi: 10.1016/j.nbd.2006.04.002
36. Mazloom, M., and Smith, Y. (2006). Synaptic microcircuitry of tyrosine hydroxylase-containing neurons and terminals in the striatum of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated monkeys. J. Comp. Neurol. 495, 453-­469. doi: 10.1002/cne.20894
37. Miller, G. W., Erickson, J. D., Perez, J. T., Penland, S. N., Mash, D. C., Rye, D. B., et al. (1999). Immunochemical analysis of vesicular monoamine transporter (VMAT2) protein in Parkinson’s disease. Exp. Neurol. 156, 138-148. doi: 10. 1006/exnr.1998.7008
38. Ng, M. C., Iacopino, A. M., Quintero, E. M., Marches, F., Sonsalla, P. K., Liang, L., et al. (1996). The neurotoxin MPTP increases calbindin-D28k levels in mouse midbrain dopaminergic neurons. Brain Res. Mol. Brain Res. 36, 329-336. doi: 10.1016/0169-328x(95)00266-u
39. Obeso, J. A., Rodriguez-Oroz, M. C., Lanciego, J. L., and Rodriguez Diaz, M. (2004). How does Parkinson’s disease begin? The role of compensatory mechanisms. TrendsNeurosci. 27, 125-127. doi: 10.1016/j.tins.2003.12.006
40. Oiwa, Y., Eberling, J. L., Nagy, D., Pivirotto, P., Emborg, M. E., and Bankiewicz, K. S. (2003). Overlesioned hemiparkinsonian non human primate model: correlation between clinical, neurochemical and histochemical changes. Front. Biosci. 8, 155-166. doi: 10.2741/1104
41. Parent, A., Lavoie, B., Smith, Y., and Bedard, P. (1990). The dopaminergic nigropall-idal projection in primates: distinct cellular origin and relative sparingin MPTP-treated monkeys. Adv. Neurol. 53,111-116
42. Reisner, P. D., Christakos, S., and Vanaman, T. C. (1992). In vitro enzyme activa­tion with calbindin-D28k, the vitamin D-dependent 28 kDa calcium binding protein. FEBSLett. 297, 127-131. doi: 10.1016/0014-5793(92)80342-e
43. Rico, A. J., Barroso-Chinea, P., Conte-Perales, L., Roda, E., Gomez-Bautista, V., Gendive, M., et al. (2010). A direct projection from the subthalamic nucleus to the ventral thalamus in monkeys. Neurobiol. Dis. 39, 381-392. doi: 10.1016/j.nbd.2010.05.004
44. Rommelfanger, K. S., and Wichmann, T. (2010). Extrastriatal dopaminergic cir­cuits of the Basal Ganglia. Front. Neuroanat. 4:139. doi: 10.3389/fnana.2010.00139
45. Schapira, A. H., Cooper, J. M., Dexter, D., Clark, J. B., Jenner, P., Marsden, C. D., et al. (1990). Mitochondrial complex I deficiency in Parkinson’s disease. J. Neurochem. 54, 823-827. doi: 10.1111/j.1471-4159.1990.tb02325.x
46. Schneider, J. S., and Dacko, S. (1991). Relative sparing of the dopaminergic inner­vation of the globus pallidus in monkeys made hemi-parkinsonian by intrac­arotid MPTP infusion. Brain Res. 556, 292-296. doi: 10.1016/0006-8993(91) 90318-p
47. Schneider, J. S., Yuwiler, A., and Markham, C. H. (1987). Selective loss of subpop­ulations ofventral mesencephalic dopaminergic neurons in the monkeyfollow-ing exposure to MPTP. Brain Res. 411, 144-150. doi: 10.1016/0006-8993(87) 90691-3
48. Selvaraj, S., Sun, Y., Watt, J. A., Wang, S., Lei, S., Birnbaumer, L., et al. (2012). Neurotoxin-induced ER stress in mouse dopaminergic neurons involves down-regulationofTRPC1 andinhibitionofAKT/mTORsignaling. J. Clin.Invest. 122, 1354-1367. doi: 10.1172/JCI61332
49. Selvaraj, S., Watt, J. A., and Singh, B. B. (2009). TRPC1 inhibits apoptotic cell degeneration induced by dopaminergic neurotoxin MPTP/MPP(+). Cell Cal­cium 46, 209-218. doi: 10.1016/j.ceca.2009.07.008
50. Smidt, M. P., and Burbach, J. P. (2007). Howto make a mesodiencephalic dopamin­ergic neuron. Nat. Rev. Neurosci. 8, 21-32. doi: 10.1038/nrn2039
51. Smith, Y., and Kieval, J. Z. (2000). Anatomy of the dopamine system in the basal ganglia. Trends Neurosci. 23, S28-S33. doi: 10.1016/s1471-1931(00)00023-9
52. Smith, Y., Lavoie, B., Dumas, J., and Parent, A. (1989). Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey. Brain Res. 482, 381-386. doi: 10.1016/0006-8993(89)91205-5
53. Smits, S. M., Burbach, J. P., and Smidt, M. P. (2006). Developmental origin and fate ofmeso-diencephalic dopamine neurons. Prog. Neurobiol. 78, 1-16. doi: 10. 1016/j.pneurobio.2005.12.003
54. Surmeier, D. J., Guzman, J. N., Sanchez-Padilla, J., and Schumacker, P. T. (2011). The role of calcium and mitochondrial oxidant stress in the loss of substantia nigra pars compacta dopaminergic neurons in Parkinson’s disease. Neuroscience 198, 221-231. doi: 10.1016/j.neuroscience.2011.08.045
55. Varastet, M., Riche, D., Maziere, M., and Hantraye, P. (1994). Chronic MPTP treatment reproduces in baboons the differential vulnerability of mesencephalic dopaminergic neurons observed in Parkinson’s disease. Neuroscience 63, 47-56. doi: 10.1016/0306-4522(94)90006-x
56. Wilson, C. J., and Callaway, J. C. (2000). Coupled oscillator model of the dopamin­ergic neuron of the substantia nigra. J. Neurophysiol. 83, 3084-3100
57. Yamada, T., McGeer, P. L., Baimbridge, K. G., and McGeer, E. G. (1990). Relative sparing in Parkinson’s disease of substantia nigra dopamine neurons con­taining calbindin-D28K. Brain Res. 526, 303-307. doi: 10.1016/0006-8993(90) 91236-a
58. Yuan, H. H., Chen, R. J., Zhu, Y. H., Peng, C. L., and Zhu, X. R. (2013). The neuroprotective effect of overexpression of calbindin-D(28k) in an animal model ofParkinson’s disease. Mol. Neurobiol. 47, 117-122. doi: 10.1007/s12035-012-8332-3