Sox-2 Positive Neural Progenitors in the Primate Striatum Undergo Dynamic Changes after Dopamine Denervation

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Ordoñez, Cristina ^a   Moreno Murciano, Paz ^b   Hernandez, Maria ^a   Di Caudo, Carla ^a   Carril Mundiñano, Iñaki ^a   Vazquez, Nerea ^c   Garcia Verdugo, Jose Manuel ^d   Sanchez Pernaute, Rosario ^c   Luquin, Maria Rosario ^a  

^a UNIVERSITY OF NAVARRA   (Spain)

^b CENTRO DE INVESTIGACIÓN PRÍNCIPE FELIPE   (Spain)

^c Cell Reprogramming Unit   (Spain)

^d UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BROXURIDINE; CALRETININ; DOPAMINE; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL COUNT; CELL LEVEL; CELL POPULATION; CELL PROLIFERATION; CELL RENEWAL; CONTROLLED STUDY; CORPUS STRIATUM; DENERVATION; MACACA FASCICULARIS; MALE; NEURAL STEM CELL; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; SUBSTANTIA NIGRA;

ANIMALIA; HARNESS; MACACA FASCICULARIS; PARKINSONIA; PRIMATES;

ANIMALS; CORPUS STRIATUM; DENERVATION; DOPAMINE; FLUORESCENT ANTIBODY TECHNIQUE; MACACA FASCICULARIS; MALE; NEURAL STEM CELLS; SOXB1 TRANSCRIPTION FACTORS; SUBSTANTIA NIGRA;

EID: 84879181160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066377     Document Type: Article

References (61)

1. Brundin P, Barker RA, Parmar M, (2010) Neural grafting in Parkinson's disease Problems and possibilities. Prog Brain Res 184: 265-294.
2. Ganz J, Lev N, Melamed E, Offen D, (2011) Cell replacement therapy for Parkinson's disease: how close are we to the clinic? Expert Rev Neurother 11: 1325-1339.
3. Politis M, (2010) Dyskinesias after neural transplantation in Parkinson's disease: what do we know and what is next? BMC Med 8: 80.
4. Alvarez-Buylla A, Lim DA, (2004) For the long run: maintaining germinal niches in the adult brain. Neuron 41: 683-686.
5. Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A, (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci U S A 99: 11464-11469.
6. Gould E, Reeves AJ, Graziano MS, Gross CG, (1999) Neurogenesis in the neocortex of adult primates. Science 286: 548-552.
7. Zhao M, Momma S, Delfani K, Carlen M, Cassidy RM, et al. (2003) Evidence for neurogenesis in the adult mammalian substantia nigra. Proc Natl Acad Sci U S A 100: 7925-7930.
8. Lie DC, Dziewczapolski G, Willhoite AR, Kaspar BK, Shults CW, et al. (2002) The adult substantia nigra contains progenitor cells with neurogenic potential. J Neurosci 22: 6639-6649.
9. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH, (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19: 8487-8497.
10. Palmer TD, Ray J, Gage FH, (1995) FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci 6: 474-486.
11. Reynolds BA, Weiss S, (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710.
12. Shihabuddin LS, Ray J, Gage FH, (1997) FGF-2 is sufficient to isolate progenitors found in the adult mammalian spinal cord. Exp Neurol 148: 577-586.
13. Weiss S, Dunne C, Hewson J, Wohl C, Wheatley M, et al. (1996) Multipotent CNS stem cells are present in the adult mammalian spinal cord and ventricular neuroaxis. J Neurosci 16: 7599-7609.
14. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA, (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168: 415-427.
15. Luzzati F, De Marchis S, Fasolo A, Peretto P, (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26: 609-621.
16. 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.
17. Gu W, Brannstrom T, Wester P, (2000) Cortical neurogenesis in adult rats after reversible photothrombotic stroke. J Cereb Blood Flow Metab 20: 1166-1173.
18. Magavi SS, Leavitt BR, Macklis JD, (2000) Induction of neurogenesis in the neocortex of adult mice. Nature 405: 951-955.
19. Tande D, Hoglinger 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.
20. Vessal M, Darian-Smith C, (2010) Adult neurogenesis occurs in primate sensorimotor cortex following cervical dorsal rhizotomy. J Neurosci 30: 8613-8623.
21. Bihel E, Pro-Sistiaga P, Letourneur A, Toutain J, Saulnier R, et al. (2010) Permanent or transient chronic ischemic stroke in the non-human primate: behavioral, neuroimaging, histological, and immunohistochemical investigations. J Cereb Blood Flow Metab 30: 273-285.
22. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, et al. (2003) Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 17: 126-140.
23. Ferri AL, Cavallaro M, Braida D, Di Cristofano A, Canta A, et al. (2004) Sox2 deficiency causes neurodegeneration and impaired neurogenesis in the adult mouse brain. Development 131: 3805-3819.
24. Bylund M, Andersson E, Novitch BG, Muhr J, (2003) Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6: 1162-1168.
25. Graham V, Khudyakov J, Ellis P, Pevny L, (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39: 749-765.
26. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, et al. (2010) L1 retrotransposition in neurons is modulated by MeCP2. Nature 468: 443-446.
27. Brazel CY, Limke TL, Osborne JK, Miura T, Cai J, et al. (2005) Sox2 expression defines a heterogeneous population of neurosphere-forming cells in the adult murine brain. Aging Cell 4: 197-207.
28. Suh H, Consiglio A, Ray J, Sawai T, D'Amour KA, et al. (2007) In vivo fate analysis reveals the multipotent and self-renewal capacities of Sox2+ neural stem cells in the adult hippocampus. Cell Stem Cell 1: 515-528.
29. Arnold K, Sarkar A, Yram MA, Polo JM, Bronson R, et al. (2011) Sox2(+) adult stem and progenitor cells are important for tissue regeneration and survival of mice. Cell Stem Cell 9: 317-329.
30. Hattiangady B, Shetty AK, (2008) Aging does not alter the number or phenotype of putative stem/progenitor cells in the neurogenic region of the hippocampus. Neurobiol Aging 29: 129-147.
31. Komitova M, Eriksson PS, (2004) Sox-2 is expressed by neural progenitors and astroglia in the adult rat brain. Neurosci Lett 369: 24-27.
32. Komitova M, Zhao LR, Gido G, Johansson BB, Eriksson P, (2005) Postischemic exercise attenuates whereas enriched environment has certain enhancing effects on lesion-induced subventricular zone activation in the adult rat. Eur J Neurosci 21: 2397-2405.
33. Luzzati F, De Marchis S, Parlato R, Gribaudo S, Schutz G, et al. (2011) New striatal neurons in a mouse model of progressive striatal degeneration are generated in both the subventricular zone and the striatal parenchyma. PLoS One 6: e25088.
34. Aizawa K, Ageyama N, Terao K, Hisatsune T, (2011) Primate-specific alterations in neural stem/progenitor cells in the aged hippocampus. Neurobiol Aging 32: 140-150.
35. Tonchev AB, Yamashima T, Sawamoto K, Okano H, (2006) Transcription factor protein expression patterns by neural or neuronal progenitor cells of adult monkey subventricular zone. Neuroscience 139: 1355-1367.
36. Gould E, Vail N, Wagers M, Gross CG, (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci U S A 98: 10910-10917.
37. Ngwenya LB, Peters A, Rosene DL, (2006) Maturational sequence of newly generated neurons in the dentate gyrus of the young adult rhesus monkey. J Comp Neurol 498: 204-216.
38. Sirerol-Piquer MS, Cebrian-Silla A, Alfaro-Cervello C, Gomez-Pinedo U, Soriano-Navarro M, et al. (2012) GFP immunogold staining, from light to electron microscopy, in mammalian cells. Micron 43: 589-599.
39. Martin RF, Bowden DM, (1996) A stereotaxic template atlas of the macaque brain for digital imaging and quantitative neuroanatomy. Neuroimage 4: 119-150.
40. Shi SR, Liu C, Balgley BM, Lee C, Taylor CR, (2006) Protein extraction from formalin-fixed, paraffin-embedded tissue sections: quality evaluation by mass spectrometry. J Histochem Cytochem 54: 739-743.
41. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A, (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97: 703-716.
42. Huot P, Levesque M, Parent A, (2007) The fate of striatal dopaminergic neurons in Parkinson's disease and Huntington's chorea. Brain 130: 222-232.
43. Betarbet R, Turner R, Chockkan V, DeLong MR, Allers KA, et al. (1997) Dopaminergic neurons intrinsic to the primate striatum. J Neurosci 17: 6761-6768.
44. San Sebastian W, Guillen J, Manrique M, Belzunegui S, Ciordia E, et al. (2007) Modification of the number and phenotype of striatal dopaminergic cells by carotid body graft. Brain 130: 1306-1316.
45. Goritz C, Frisen J, (2012) Neural stem cells and neurogenesis in the adult. Cell Stem Cell 10: 657-659.
46. Parent A, Fortin M, Cote PY, Cicchetti F, (1996) Calcium-binding proteins in primate basal ganglia. Neurosci Res 25: 309-334.
47. Ulfig N (2002) Calcium-binding proteins in the human developing brain. Adv Anat Embryol Cell Biol 165: III-IX, 1-92.
48. Brandt MD, Jessberger S, Steiner B, Kronenberg G, Reuter K, et al. (2003) Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of mice. Mol Cell Neurosci 24: 603-613.
49. Jiang M, Swann JW, (1997) Expression of calretinin in diverse neuronal populations during development of rat hippocampus. Neuroscience 81: 1137-1154.
50. Kato T, Yokouchi K, Li Z, Fukushima N, Kawagishi K, et al. (1999) Calretinin-immunoreactive neurons in rostral migratory stream: neuronal differentiation. Neuroreport 10: 2769-2772.
51. Kempermann G, Gage FH (2000) Neurogenesis in the adult hippocampus. Novartis Found Symp 231: 220-235; discussion 235-241, 302-226.
52. Knoth R, Singec I, Ditter M, Pantazis G, Capetian P, et al. (2010) Murine features of neurogenesis in the human hippocampus across the lifespan from 0 to 100 years. PLoS One 5: e8809.
53. Yang Z, You Y, Levison SW, (2008) Neonatal hypoxic/ischemic brain injury induces production of calretinin-expressing interneurons in the striatum. J Comp Neurol 511: 19-33.
54. Kay JN, Blum M, (2000) Differential response of ventral midbrain and striatal progenitor cells to lesions of the nigrostriatal dopaminergic projection. Dev Neurosci 22: 56-67.
55. Mao L, Lau YS, Petroske E, Wang JQ, (2001) Profound astrogenesis in the striatum of adult mice following nigrostriatal dopaminergic lesion by repeated MPTP administration. Brain Res Dev Brain Res 131: 57-65.
56. Coronas V, Bantubungi K, Fombonne J, Krantic S, Schiffmann SN, et al. (2004) Dopamine D3 receptor stimulation promotes the proliferation of cells derived from the post-natal subventricular zone. J Neurochem 91: 1292-1301.
57. Freundlieb N, Francois C, Tande 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.
58. Merlo S, Canonico PL, Sortino MA, (2011) Distinct effects of pramipexole on the proliferation of adult mouse sub-ventricular zone-derived cells and the appearance of a neuronal phenotype. Neuropharmacology 60: 892-900.
59. Kornack DR, Rakic P, (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci U S A 96: 5768-5773.
60. Blandini F, Armentero MT, (2012) Animal models of Parkinson's disease. FEBS J 279: 1156-1166.
61. Bankiewicz KS, Sanchez-Pernaute R, Oiwa Y, Kohutnicka M, Cummins A, et al. (2001) Preclinical models of Parkinson's disease. Curr Protoc Neurosci Chapter 9: Unit9 4.