Widespread proliferation impairment and hypocellularity in the cerebellum of fetuses with down syndrome

Brain Pathology

Volumn 21, Issue 4, 2011, Pages 361-373

  Guidi, Sandra ^a   Ciani, Elisabetta ^a   Bonasoni, Paola ^b   Santini, Donatella ^c   Bartesaghi, Renata ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

^b G GASLINI INSTITUTE   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

cerebellum; mental retardation; neurogenesis; trisomy 21

Indexed keywords

KI 67 ANTIGEN;

APOPTOSIS; BRAIN SIZE; BRAIN VENTRICLE; CELL PROLIFERATION; CEREBELLUM; CEREBELLUM HYPOPLASIA; CLINICAL FEATURE; CONTROLLED STUDY; DOWN SYNDROME; FEMALE; FETUS; HUMAN; HUMAN TISSUE; HYPOTROPHY; IMMUNOHISTOCHEMISTRY; MALE; MOTOR DYSFUNCTION; NERVOUS SYSTEM DEVELOPMENT; PRECURSOR; REVIEW; TRISOMY;

CELL PROLIFERATION; CEREBELLUM; DOWN SYNDROME; FEMALE; FETUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEUROGENESIS;

EID: 79953113713     PISSN: 10156305     EISSN: 17503639     Source Type: Journal    
DOI: 10.1111/j.1750-3639.2010.00459.x     Document Type: Review

References (55)

1. Abraham H, Tornoczky T, Kosztolanyi G, Seress L, (2001) Cell formation in the cortical layers of the developing human cerebellum. Int J Dev Neurosci 19: 53-62. (Pubitemid 32156974)
2. Aylward EH, Habbak R, Warren AC, Pulsifer MB, Barta PE, Jerram M, Pearlson GD, (1997) Cerebellar volume in adults with Down syndrome. Arch Neurol 54: 209-212. (Pubitemid 27078729)
3. Aylward EH, Li Q, Honeycutt NA, Warren AC, Pulsifer MB, Barta PE, et al, (1999) MRI volumes of the hippocampus and amygdala in adults with Down's syndrome with and without dementia. Am J Psychiatry 156: 564-568. (Pubitemid 29162977)
4. Baxter LL, Moran TH, Richtsmeier JT, Troncoso J, Reeves RH, (2000) Discovery and genetic localization of Down syndrome cerebellar phenotypes using the Ts65Dn mouse. Hum Mol Genet 9: 195-202. (Pubitemid 30052743)
5. Bianchi P, Ciani E, Contestabile A, Guidi S, Bartesaghi R, (2010) Lithium restores neurogenesis in the subventricular zone of the Ts65Dn mouse, a model for Down syndrome. Brain Pathol 20: 106-118.
6. Brazel CY, Romanko MJ, Rothstein RP, Levison SW, (2003) Roles of the mammalian subventricular zone in brain development. Prog Neurobiol 69: 49-69. (Pubitemid 36293991)
7. Choi BH, Lapham LW, (1980) Evolution of Bergmann glia in developing human fetal cerebellum: a Golgi, electron microscopic and immunofluorescent study. Brain Res 190: 369-383. (Pubitemid 10079185)
8. Clark S, Schwalbe J, Stasko MR, Yarowsky PJ, Costa AC, (2006) Fluoxetine rescues deficient neurogenesis in hippocampus of the Ts65Dn mouse model for Down syndrome. Exp Neurol 200: 256-261. (Pubitemid 44080763)
9. Contestabile A, Fila T, Ceccarelli C, Bonasoni P, Bonapace L, Santini D, et al, (2007) Cell cycle alteration and decreased cell proliferation in the hippocampal dentate gyrus and in the neocortical germinal matrix of fetuses with Down syndrome and in Ts65Dn mice. Hippocampus 17: 665-678. (Pubitemid 47292037)
10. Contestabile A, Fila T, Bartesaghi R, Ciani E, (2009) Cell cycle elongation impairs proliferation of cerebellar granule cell precursors in the Ts65Dn mouse, an animal model for Down syndrome. Brain Pathol 19: 224-237.
11. Corrales JD, Blaess S, Mahoney EM, Joyner AL, (2006) The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133: 1811-1821. (Pubitemid 43810987)
12. Dauphinot L, Lyle R, Rivals I, Dang MT, Moldrich RX, Golfier G, et al, (2005) The cerebellar transcriptome during postnatal development of the Ts1Cje mouse, a segmental trisomy model for Down syndrome. Hum Mol Genet 14: 373-384. (Pubitemid 40220654)
13. de la Monte SM, Hedley-Whyte ET, (1990) Small cerebral hemispheres in adults with Down's syndrome: contributions of developmental arrest and lesions of Alzheimer's disease. J Neuropathol Exp Neurol 49: 509-520. (Pubitemid 20264005)
14. Engidawork E, Balic N, Juranville JF, Fountoulakis M, Dierssen M, Lubec G, (2001) Unaltered expression of Fas (CD95/APO-1), caspase-3, Bcl-2 and annexins in brains of fetal Down syndrome: evidence against increased apoptosis. J Neural Transm Suppl 61: 149-162. (Pubitemid 38085079)
15. Golden JA, Hyman BT, (1994) Development of the superior temporal neocortex is anomalous in trisomy 21. J Neuropathol Exp Neurol 53: 513-520. (Pubitemid 24276810)
16. Guidi S, Bonasoni P, Ceccarelli C, Santini D, Gualtieri F, Ciani E, Bartesaghi R, (2008) Neurogenesis impairment and increased cell death reduce total neuron number in the hippocampal region of fetuses with Down syndrome. Brain Pathol 18: 180-197. (Pubitemid 351430398)
17. Guihard-Costa AM, Khung S, Delbecque K, Menez F, Delezoide AL, (2005) Biometry of face and brain in fetuses with trisomy 21. Pediatr Res 59: 33-38.
18. Gundersen H, Jensen E, (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147: 229-263.
19. Haydar TF, Nowakowski RS, Yarowsky PJ, Krueger BK, (2000) Role of founder cell deficit and delayed neuronogenesis in microencephaly of the trisomy 16 mouse. J Neurosci 20: 4156-4164. (Pubitemid 30365686)
20. Helguera P, Pelsman A, Pigino G, Wolvetang E, Head E, Busciglio J, (2005) ets-2 Promotes the activation of a mitochondrial death pathway in Down's syndrome neurons. J Neurosci 25: 2295-2303. (Pubitemid 40322270)
21. Hewitt CA, Ling KH, Merson TD, Simpson KM, Ritchie ME, King SL, et al, (2010) Gene network disruptions and neurogenesis defects in the adult Ts1Cje mouse model of Down syndrome. PLoS One 5: e11561.
22. Ieshima A, Kisa T, Yoshino K, Takashima S, Takeshita K, (1984) A morphometric CT study of Down's syndrome showing small posterior fossa and calcification of basal ganglia. Neuroradiology 26: 493-498. (Pubitemid 15211148)
23. Jernigan TL, Bellugi U, Sowell E, Doherty S, Hesselink JR, (1993) Cerebral morphologic distinctions between Williams and Down syndromes. Arch Neurol 50: 186-191. (Pubitemid 23054803)
24. Lorenzi HA, Reeves RH, (2006) Hippocampal hypocellularity in the Ts65Dn mouse originates early in development. Brain Res 1104: 153-159. (Pubitemid 44148518)
25. Noble J, (1998) Natural history of Down's syndrome: a brief review for those involved in antenatal screening. J Med Screen 5: 172-177. (Pubitemid 29035306)
26. Pinter JD, Eliez S, Schmitt JE, Capone GT, Reiss AL, (2001) Neuroanatomy of Down's syndrome: a high-resolution MRI study. Am J Psychiatry 158: 1659-1665. (Pubitemid 32923659)
27. Pixley S, de Vellis J, (1984) Transition between immature radial glia and mature astrocytes studied with a monoclonal antibody to vimentin. Brain Res 317: 201-209. (Pubitemid 14060846)
28. Rachidi M, Lopes C, (2008) Mental retardation and associated neurological dysfunctions in Down syndrome: a consequence of dysregulation in critical chromosome 21 genes and associated molecular pathways. Eur J Paediatr Neurol 12: 168-182. (Pubitemid 351545848)
29. Rakic P, (2003) Developmental and evolutionary adaptations of cortical radial glia. Cereb Cortex 13: 541-549. (Pubitemid 36613160)
30. Rakic P, Sidman RL, (1970) Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 139: 473-500.
31. Roizen NJ, Patterson D, (2003) Down's syndrome. Lancet 361: 1281-1289. (Pubitemid 36428586)
32. Roper RJ, Baxter LL, Saran NG, Klinedinst DK, Beachy PA, Reeves RH, (2006) Defective cerebellar response to mitogenic Hedgehog signaling in Down [corrected] syndrome mice. Proc Natl Acad Sci U S A 103: 1452-1456. (Pubitemid 43191186)
33. Roper RJ, St John HK, Philip J, Lawler A, Reeves RH, (2006) Perinatal loss of TS65DN "Down Syndrome" mice. Genetics 172: 437-443. (Pubitemid 43345504)
34. Roper RJ, VanHorn JF, Cain CC, Reeves RH, (2009) A neural crest deficit in Down syndrome mice is associated with deficient mitotic response to Sonic hedgehog. Mech Dev 126: 212-219.
35. Rose DS, Maddox PH, Brown DC, (1994) Which proliferation markers for routine immunohistology? A comparison of five antibodies. J Clin Pathol 47: 1010-1014.
36. Ross MH, Galaburda AM, Kemper TL, (1984) Down's syndrome: is there a decreased population of neurons? Neurology 34: 909-916. (Pubitemid 14076456)
37. Rotmensch S, Goldstein I, Liberati M, Shalev J, Ben-Rafael Z, Copel JA, (1997) Fetal transcerebellar diameter in Down syndrome. Obstet Gynecol 89: 534-537. (Pubitemid 27133525)
38. Rueda N, Mostany R, Pazos A, Florez J, Martinez-Cue C, (2005) Cell proliferation is reduced in the dentate gyrus of aged but not young Ts65Dn mice, a model of Down syndrome. Neurosci Lett 380: 197-201. (Pubitemid 40602355)
39. Schmahmann JD, (2004) Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 16: 367-378. (Pubitemid 39244566)
40. Schmidt-Sidor B, Wisniewski KE, Shepard TH, Sersen EA, (1990) Brain growth in Down syndrome subjects 15 to 22 weeks of gestational age and birth to 60 months. Clin Neuropathol 9: 181-190. (Pubitemid 20287898)
41. Scholzen T, Gerdes J, (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182: 311-322. (Pubitemid 30054364)
42. Seidl R, Bidmon B, Bajo M, Yoo PC, Cairns N, LaCasse EC, Lubec G, (2001) Evidence for apoptosis in the fetal Down syndrome brain. J Child Neurol 16: 438-442. (Pubitemid 32631741)
43. Sekiguchi M, Shimai K, Guo H, Nowakowski RS, (1992) Cytoarchitectonic abnormalities in hippocampal formation and cerebellum of dreher mutant mouse. Brain Res Dev Brain Res 67: 105-112.
44. Seress L, Abraham H, Tornoczky T, Kosztolanyi G, (2001) Cell formation in the human hippocampal formation from mid-gestation to the late postnatal period. Neuroscience 105: 831-843. (Pubitemid 32786796)
45. Sillitoe RV, Joyner AL, (2007) Morphology, molecular codes, and circuitry produce the three-dimensional complexity of the cerebellum. Annu Rev Cell Dev Biol 23: 549-577.
46. Sudarov A, Joyner AL, (2007) Cerebellum morphogenesis: the foliation pattern is orchestrated by multi-cellular anchoring centers. Neural Dev 2: 26.
47. Sylvester PE, (1983) The hippocampus in Down's syndrome. J Ment Defic Res 27: 227-236. (Pubitemid 14234708)
48. Tavano A, Grasso R, Gagliardi C, Triulzi F, Bresolin N, Fabbro F, Borgatti R, (2007) Disorders of cognitive and affective development in cerebellar malformations. Brain 130: 2646-2660. (Pubitemid 47515322)
49. Teipel SJ, Schapiro MB, Alexander GE, Krasuski JS, Horwitz B, Hoehne C, et al, (2003) Relation of corpus callosum and hippocampal size to age in nondemented adults with Down's syndrome. Am J Psychiatry 160: 1870-1878. (Pubitemid 41103323)
50. ten Donkelaar HJ, Lammens M, Wesseling P, Thijssen HO, Renier WO, (2003) Development and developmental disorders of the human cerebellum. J Neurol 250: 1025-1036. (Pubitemid 37152550)
51. Weis S, Weber G, Neuhold A, Rett A, (1991) Down syndrome: MR quantification of brain structures and comparison with normal control subjects. AJNR Am J Neuroradiol 12: 1207-1211.
52. Weisheit G, Gliem M, Endl E, Pfeffer PL, Busslinger M, Schilling K, (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24: 466-478. (Pubitemid 44100338)
53. West MJ, Gundersen HJ, (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296: 1-22. (Pubitemid 20174971)
54. Winter TC, Ostrovsky AA, Komarniski CA, Uhrich SB, (2000) Cerebellar and frontal lobe hypoplasia in fetuses with trisomy 21: usefulness as combined US markers. Radiology 214: 533-538. (Pubitemid 30077715)
55. Wisniewski KE, (1990) Down syndrome children often have brain with maturation delay, retardation of growth, and cortical dysgenesis. Am J Med Genet Suppl 7: 274-281.