Cortical hypoplasia and ventriculomegaly of p73-deficient mice: Developmental and adult analysis

Journal of Comparative Neurology

Volumn 522, Issue 11, 2014, Pages 2663-2679

  Medina Bolívar, Carolina ^a   González Arnay, Emilio ^a   Talos, Flaminia ^b   González Gómez, Miriam ^a   Moll, Ute M ^b   Meyer, Gundela ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

Apoptosis; Cerebral cortex; Cerebrospinal fluid; Cilia; Ependyma; Lateral ventricles

Indexed keywords

PROTEIN P73; DNA BINDING PROTEIN; NUCLEAR PROTEIN; TUMOR SUPPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN P73;

ADULT; ADULTHOOD; AMYGDALOID NUCLEUS; ANATOMIC LANDMARK; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN ATROPHY; BRAIN DEVELOPMENT; BRAIN DISEASE; BRAIN MALFORMATION; BRAIN SIZE; BRAIN THICKNESS; BRAIN VENTRICLE DILATATION; CONTROLLED STUDY; CORPUS STRIATUM; CORTICAL HYPOPLASIA; DISEASE ASSOCIATION; DISEASE SEVERITY; EMBRYO; EPENDYMA CELL; HIPPOCAMPUS; HYPOPLASIA; KNOCKOUT MOUSE; MOLECULAR DYNAMICS; MOUSE; NEOCORTEX; NERVOUS SYSTEM PARAMETERS; NEUROANATOMY; NONHUMAN; PATHOLOGICAL ANATOMY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; REGULATORY MECHANISM; SEPTUM PELLUCIDUM; SURVIVAL RATE; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL COUNT; CHOROID PLEXUS; CONFOCAL MICROSCOPY; DEFICIENCY; EPENDYMA; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; HYDROCEPHALUS; IMMUNOHISTOCHEMISTRY; NICK END LABELING; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL COUNT; CHOROID PLEXUS; DNA-BINDING PROTEINS; EPENDYMA; FLUORESCENT ANTIBODY TECHNIQUE; HIPPOCAMPUS; HYDROCEPHALUS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; NEOCORTEX; NUCLEAR PROTEINS; PHENOTYPE; TUMOR SUPPRESSOR PROTEINS;

EID: 84901661347     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23556     Document Type: Article

References (49)

1. Agostini M, Tucci P, Chen H, Knight RA, Bano D, Nicotera P, McKeon F, Melino G. 2010. p73 Regulates maintenance of neural stem cell. Biochem Biophys Res Commun 403:13-17.
2. Agostini M, Tucci P, Killick R, Candi E, Sayan BS, Rivetti di Val Cervo P, Nicotera P, McKeon F, Knight RA, Mak TW, Melino G. 2011. Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proc Natl Acad Sci U S A 108:21093-21098.
3. Banizs B, Pike MM, Millican CL, Ferguson WB, Komlosi P, Sheetz J, Bell PD, Schwiebert EM, Yoder BK. 2005. Dysfunctional cilia lead to altered ependyma and choroid plexus function, and result in the formation of hydrocephalus. Development 132:5329-5339.
4. Barinka F, Druga R. 2010. Calretinin expression in the mammalian neocortex: a review. Physiol Res 59:665-677.
5. Bosch M, Pineda JR, Sunol C, Petriz J, Cattaneo E, Alberch J, Canals JM. 2004. Induction of GABAergic phenotype in a neural stem cell line for transplantation in an excitotoxic model of Huntington's disease. Exp Neurol 190:42-58.
6. Cabrera-Socorro A, Pueyo Morlans M, Suarez Sola ML, Gonzalez Delgado FJ, Castañeyra-Perdomo A, Marin MC, Meyer G. 2006. Multiple isoforms of the tumor protein p73 are expressed in the adult human telencephalon and choroid plexus and present in the cerebrospinal fluid. Eur J Neurosci 23:2109-2118.
7. Cai Y, Zhang Q, Wang C, Zhang Y, Ma T, Zhou X, Tian M, Rubenstein JL, Yang Z. 2013. Nuclear receptor COUP-TFII-expressing neocortical interneurons are derived from the medial and lateral/caudal ganglionic eminence and define specific subsets of mature interneurons. J Comp Neurol 521:479-497.
8. Canals JM, Checa N, Marco S, Akerud P, Michels A, Perez-Navarro E, Tolosa E, Arenas E, Alberch J. 2001. Expression of brain-derived neurotrophic factor in cortical neurons is regulated by striatal target area. J Neurosci 21:117-124.
9. DeFelipe J. 1997. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
10. Delaunay D, Heydon K, Miguez A, Schwab M, Nave KA, Thomas JL, Spassky N, Martinez S, Zalc B. 2009. Genetic tracing of subpopulation neurons in the prethalamus of mice (Mus musculus). J Comp Neurol 512:74-83.
11. Fitzgerald ML, Lupica CR, Pickel VM. 2011. Decreased parvalbumin immunoreactivity in the cortex and striatum of mice lacking the CB1 receptor. Synapse 65:827-831.
12. González-Cano L, Herreros-Villanueva M, Fernandez-Alonso R, Ayuso-Sacido A, Meyer G, Garcia-Verdugo JM, Silva A, Marques MM, Marin MC. 2010. p73 Deficiency results in impaired self renewal and premature neuronal differentiation of mouse neural progenitors independently of p53. Cell Death 16:e109.
13. Hernández-Acosta NC, Cabrera-Socorro A, Morlans MP, Delgado FJ, Suárez-Solá ML, Sottocornola R, Lu X, González-Gómez M, Meyer G. 2010. Dynamic expression of the p53 family members p63 and p73 in the mouse and human telencephalon during development and in adulthood. Brain Res 1372:29-40.
14. Hof PR, Glezer II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM. 1999. Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77-116.
15. Hof PR, Young WG, Bloom FE, Belichenko PV, Celio MR. 2000. Comparative cytoarchitectonic atlas of the C57BL/6 and 129/Sv mouse brains. New York: Elsevier.
16. Hooper C, Tavassoli M, Chapple JP, Uwanogho D, Goodyear R, Melino G, Lovestone S, Killick R. 2006. TAp73 isoforms antagonize Notch signalling in SH-SY5Y neuroblastomas and in primary neurones. J Neurochem 99:989-999.
17. Ibañez-Tallon I, Pagenstecher A, Fliegauf M, Olbrich H, Kispert A, Ketelsen UP, North A, Heintz N, Omran H. 2004. Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet 13:2133-2141.
18. Jiménez AJ, García-Verdugo JM, González CA, Bátiz LF, Rodríguez-Pérez LM, Páez P, Soriano-Navarro M, Roales-Buján R, Rivera P, Rodríguez S, Rodríguez EM, Pérez-Fígares JM. 2009. Disruption of the neurogenic niche in the subventricular zone of postnatal hydrocephalic hyh mice. J Neuropathol Exp Neurol 68:1006-1020.
19. Johanson CE, Duncan JA 3rd, Klinge PM, Brinker T, Stopa EG, Silverberg GD. 2008. Multiplicity of cerebrospinal fluid functions: new challenges in health and disease. Cerebrospinal Fluid Res 5:1-32.
20. Kaghad M, Bonnet H, Yang A, Creancier L, Biscan JC, Valent A, Minty A, Chalon P, Lelias JM, Dumont X, Ferrara P, McKeon F, Caput D. 1997. Monoallelically expressed gene related to p53 at 1p36, a region frequently deleted in neuroblastoma and other human cancers. Cell 90:809-819.
21. Kinney JW, Davis CN, Tabarean I, Conti B, Bartfai T, Behrens MM. 2006. A specific role for NR2A-containing NMDA receptors in the maintenance of parvalbumin and GAD67 immunoreactivity in cultured interneurons. J Neurosci 26:1604-1615.
22. Lavado A, Oliver G. 2011. Six3 is required for ependymal cell maturation. Development 138:5291-5300.
23. Lee AF, Ho DK, Zanassi P, Walsh GS, Kaplan DR, Miller FD. 2004. Evidence that DeltaNp73 promotes neuronal survival by p53-dependent and p53-independent mechanisms. J Neurosci 24:9174-9184.
24. Lim DA, Tramontin AD, Trevejo JM, Herrera DG, García-Verdugo JM, Alvarez-Buylla Noggin A. 2000. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28:713-726.
25. Lloyd-Burton S, Roskams AJ. 2012. SPARC-like 1 (SC1) is a diversely expressed and developmentally regulated matricellular protein that does not compensate for the absence of SPARC in the CNS. J Comp Neurol 520:2575-2590.
26. Mendez-Gomez HR, Vergano-Vera E, Abad JL, Bulfone A, Moratalla R, de Pablo F, Vicario-Abejon C. 2011. The T-box brain 1 (Tbr1) transcription factor inhibits astrocyte formation in the olfactory bulb and regulates neural stem cell fate. Mol Cell Neurosci 46:108-121.
27. Meyer G, Perez-Garcia CG, Abraham H, Caput D. 2002. Expression of p73 and Reelin in the developing human cortex. J Neurosci 22:4973-4986.
28. Meyer G, Cabrera Socorro A, Perez Garcia CG, Martinez Millan L, Walker N, Caput D. 2004. Developmental roles of p73 in Cajal-Retzius cells and cortical patterning. J Neurosci 24:9878-9887.
29. Miller MN, Okaty BW, Kato S, Nelson SB. 2011. Activity-dependent changes in the firing properties of neocortical fast-spiking interneurons in the absence of large changes in gene expression. Dev Neurobiol 71:62-70.
30. Nemajerova A, Petrenko O, Trümper L, Palacios G, Moll UM. 2010. Loss of p73 promotes dissemination of Myc-induced B cell lymphomas in mice. J Clin Invest 120:2070-2080.
31. Parker J, Sarlang S, Thavagnanam S, Williamson G, O'donoghue D, Villenave R, Power U, Shields M, Heaney L, Skibinski G. 2010. A 3-D well-differentiated model of pediatric bronchial epithelium demonstrates unstimulated morphological differences between asthmatic and nonasthmatic cells. Pediatr Res 67:17-22.
32. Patz S, Grabert J, Gorba T, Wirth MJ, Wahle P. 2004. Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an early period of postnatal development. Cereb Cortex 14:342-351.
33. Pozniak CD, Radinovic S, Yang A, McKeon F, Kaplan DR, Miller FD. 2000. An anti-apoptotic role for the p53 family member, p73, during developmental neuron death. Science 289:304-306.
34. Pozniak CD, Barnabé-Heider F, Rymar VV, Lee AF, Sadikot AF, Miller FD. 2002. p73 Is required for survival and maintenance of CNS neurons. J Neurosci 22:9800-9809.
35. Ravni A, Tissir F, Goffinet AM. 2010. DeltaNp73 transcription factors modulate cell survival and tumor development. Cell Cycle 9:1523-1527.
36. Sasaki Y, Ishida S, Morimoto I, Yamashita T, Kojima T, Kihara C, Tanaka T, Imai K, Nakamura Y, Tokino T. 2002. The p53 family member genes are involved in the Notch signal pathway. J Biol Chem 277:719-724.
37. Sawamoto K, Wichterle H, Gonzalez-Perez O, Cholfin JA, Yamada M, Spassky N, Murcia NS, Garcia-Verdugo JM, Marin O, Rubenstein JL, Tessier-Lavigne M, Okano H, Alvarez-Buylla A. 2006. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science 311:629-632.
38. Shi L, Li M, Lin Q, Qi X, Su B. 2013. Functional divergence of the brain-size regulating gene MCPH1 during primate evolution and the origin of humans. BMC Biol 11:62.
39. Spassky N, Merkle FT, Flames N, Tramontin AD, García-Verdugo JM, Alvarez-Buylla A. 2005. Adult ependymal cells are postmitotic and are derived from radial glial cells during embryogenesis. J Neurosci 25:10-18.
40. Talos DM, Fishman RE, Park H, Folkerth RD, Follett PL, Volpe JJ, Jensen FE. 2006. Developmental regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor subunit expression in forebrain and relationship to regional susceptibility to hypoxic/ischemic injury. I. Rodent cerebral white matter and cortex. J Comp Neurol 497:42-60.
41. Talos F, Abraham A, Vaseva AV, Holembowski L, Tsirka SE, Scheel A, Bode D, Dobbelstein M, Brück W, Moll UM. 2010. p73 Is an essential regulator of neural stem cell maintenance in embryonal and adult CNS neurogernesis. Cell Death Differ 17:1816-1829.
42. Tissir F, Ravni A, Achouri Y, Riethmacher D, Meyer G, Goffinet AM. 2009. DeltaNp73 regulates neuronal survival in vivo. Proc Natl Acad Sci U S A 106:16871-16876.
43. Tissir F, Qu Y, Montcouquiol M, Zhou L, Komatsu K, Shi D, Fujimori T, Labeau J, Tyteca D, Courtoy P, Poumay Y, Uemura T, Goffinet AM. 2010. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci 13:700-707.
44. Tomasini R, Tsuchihara K, Wilhelm M, Fujitani M, Rufini A, Cheung CC, Khan F, Itie-Youten A, Wakeham A, Tsao MS, Iovanna JL, Squire J, Jurisica I, Kaplan D, Melino G, Jurisicova A, Mak TW. 2008. TAp73 knockout shows genomic instability with infertility and tumor suppressor functions. Genes Dev 22:2677-2691.
45. Wilhelm MT, Rufini A, Wetzel MK, Tsuchihara K, Inoue S, Tomasini R, Itie-Youten A, Wakeham A, Arsenian-Henriksson M, Melino G, Kaplan DR, Miller FD, Mak TW. 2010. Isoform-specific p73 knockout mice reveal a novel role for Delta Np73 in the DNA damage response pathway. Genes Dev 24:549-560.
46. Wodarczyk C, Rowe I, Chiaravalli M, Pema M, Qian F, Boletta A. 2009. A novel mouse model reveals that polycystin-1 deficiency in ependyma and choroid plexus results in dysfunctional cilia and hydrocephalus. PLoS One 4:e7137.
47. Xu Q, Tam M, Anderson SA. 2008. Fate mapping Nkx2.1-line-age cells in the mouse telencephalon. J Comp Neurol 506:16-29.
48. Xu X, Roby KD, Callaway EM. 2010. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404.
49. Yang A, Walker N, Bronson R, Kaghad M, Oosterwegel M, Bonnin J, Vagner C, Bonnet H, Dikkes P, Sharpe A, McKeon F, Caput D. 2000. p73-Deficient mice have neurological, pheromonal and inflammatory defects but lack spontaneous tumours. Nature 404:99-103.