NF1 regulation of RAS/ERK signaling is required for appropriate granule neuron progenitor expansion and migration in cerebellar development

Genes and Development

Volumn 28, Issue 21, 2014, Pages 2407-2420

  Sanchez Ortiz, Efrain ^a,b   Cho, Woosung ^a,b   Nazarenko, Inga ^a,b   Mo, Wei ^a,b   Chen, Jian ^a,b,c   Parada, Luis F ^a,b  

^a Department of Developmental Biology ^*  (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c SOOCHOW UNIVERSITY   (China)

Author keywords

Barrel cortex; Cerebellum; CNS development; Granule neuron progenitor; Neurofibromatosis type 1; NF1

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NEUROFIBROMIN; RAS PROTEIN; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL MIGRATION; CEREBELLAR DEVELOPMENT; CEREBELLUM; CONTROLLED STUDY; GENE INACTIVATION; GRANULE NEURON PROGENITOR; MOUSE; NEURAL STEM CELL; NEUROFIBROMATOSIS; NONHUMAN; SIGNAL TRANSDUCTION; STEM CELL EXPANSION; TUMOR SUPPRESSOR GENE; ANIMAL; CELL MOTION; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; GENE DELETION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; PHYSIOLOGY; STEM CELL;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CEREBELLUM; GENE DELETION; MAP KINASE SIGNALING SYSTEM; MICE; NEUROFIBROMIN 1; NEURONS; PROTEIN KINASE INHIBITORS; RAS PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 84908432902     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.246603.114     Document Type: Article

References (51)

1. Alder J, Cho NK, Hatten ME. 1996. Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 17: 389–399.
2. Anthony TE, Mason HA, Gridley T, Fishell G, Heintz N. 2005. Brain lipid-binding protein is a direct target of Notch signaling in radial glial cells. Genes Dev 19: 1028–1033.
3. Balestri P, Vivarelli R, Grosso S, Santori L, Farnetani MA, Galluzzi P, Vatti GP, Calabrese F, Morgese G. 2003. Malformations of cortical development in neurofibromatosis type 1. Neurology 61: 1799–1801.
4. Basson MA, Wingate RJ. 2013. Congenital hypoplasia of the cerebellum: developmental causes and behavioral consequences. Front Neuroanat 7: 29.
5. Buffo A, Rossi F. 2013. Origin, lineage and function of cerebellar glia. Prog Neurobiol 109: 42–63.
6. Champion JA, Rose KJ, Payne JM, Burns J, North KN. 2014. Relationship between cognitive dysfunction, gait, and motor impairment in children and adolescents with neurofibromatosis type 1. Dev Med Child Neuro 56: 468–474
7. Chanas-Sacre G, Rogister B, Moonen G, Leprince P. 2000. Radial glia phenotype: origin, regulation, and transdifferentiation. J Neurosci Res 61: 357–363.
8. Chang T, Krisman K, Theobald EH, Xu J, Akutagawa J, Lauchle JO, Kogan S, Braun BS, Shannon K. 2013. Sustained MEK inhibition abrogates myeloproliferative disease in NF1 mutant mice. J Clin Invest 123: 335–339.
9. Chen J, Kwon CH, Lin L, Li Y, Parada LF. 2009. Inducible sitespecific recombination in neural stem/progenitor cells. Genesis 47: 122–131.
10. Cichowski K, Jacks T. 2001. NF1 tumor suppressor gene function: narrowing the GAP. Cell 104: 593–604.
11. Costa RM, Silva AJ. 2003. Mouse models of neurofibromatosis type I: bridging the GAP. Trends Mol Med 9: 19–23.
12. Costa DD, de Paula JJ, de Rezende NA, Rodrigues LO, Malloy- Diniz LF, Romano-Silva MA, Miranda DM. 2014. Neuropsychological impairments in elderly Neurofibromatosis type 1 patients. Eur J Med Genet 57: 216–219.
13. Courchesne E, Campbell K, Solso S. 2011. Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res 1380: 138–145.
14. Cui Y, Costa RM, Murphy GG, Elgersma Y, Zhu Y, Gutmann DH, Parada LF, Mody I, Silva AJ. 2008. Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135: 549–560.
15. D’Arca D, Zhao X, Xu W, Ramirez-Martinez NC, Iavarone A, Lasorella A. 2010. Huwe1 ubiquitin ligase is essential to synchronize neuronal and glial differentiation in the developing cerebellum. Proc Natl Acad Sci 107: 5875–5880.
16. Garg S, Green J, Leadbitter K, Emsley R, Lehtonen A, Evans DG, Huson SM. 2013. Neurofibromatosis type 1 and autism spectrum disorder. Pediatrics 132: e1642–1648.
17. Goodrich LV, Milenkovićc L, Higgins KM, Scott MP. 1997. Altered neural cell fates and medulloblastoma in mouse patched mutants. Science 277: 1109–1113.
18. Hatten ME, Heintz N. 1995. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 18: 385–408.
19. Hatten ME, Roussel MF. 2011. Development and cancer of the cerebellum. Trends Neurosci 34: 134–142.
20. Hegedus B, Dasgupta B, Shin JE, Emnett RJ, Hart-Mahon EK, Elghazi L, Bernal-Mizrachi E, Gutmann DH. 2007. Neurofibromatosis- 1 regulates neuronal and glial cell differentiation from neuroglial progenitors in vivo by both cAMP- and Rasdependent mechanisms. Cell Stem Cell 1: 443–457.
21. Hyman SL, Shores A, North KN. 2005. The nature and frequency of cognitive deficits in children with neurofibromatosis type 1. Neurology 65: 1037–1044.
22. Jessen WJ, Miller SJ, Jousma E, Wu J, Rizvi TA, Brundage ME, Eaves D, Widemann B, Kim MO, Dombi E, et al. 2013. MEK inhibition exhibits efficacy in human and mouse neurofibromatosis tumors. J Clin Invest 123: 340–347.
23. Klesse LJ, Parada LF. 1998. P21 ras and phosphatidylinositol-3 kinase are required for survival of wild-type and NF1 mutant sensory neurons. J Neurosci 18: 10420–10428.
24. Lee DY, Yeh TH, Emnett RJ, White CR, Gutmann DH. 2010. Neurofibromatosis-1 regulates neuroglial progenitor proliferation and glial differentiation in a brain region-specific manner. Genes Dev 24: 2317–2329.
25. Li H, Crair MC. 2011. How do barrels form in somatosensory cortex? Ann N Y Acad Sci 1225: 119–129.
26. Li Y, Luikart BW, Birnbaum S, Chen J, Kwon CH, Kernie SG, Bassel-Duby R, Parada LF. 2008. TrkB regulates hippocampal neurogenesis and governs sensitivity to antidepressive treatment. Neuron 59: 399–412.
27. Li Y, Li Y, McKay RM, Riethmacher D, Parada LF. 2012. Neurofibromin modulates adult hippocampal neurogenesis and behavioral effects of antidepressants. J Neurosci 32: 3529–3539.
28. Lorenzo J, Barton B, Arnold SS, North KN. 2013. Cognitive features that distinguish preschool-age children with neurofibromatosis type 1 from their peers: a matched case-control study. Pediatrics 163: 1479–1483 e1471.
29. Luikart BW, Nef S, Virmani T, Lush ME, Liu Y, Kavalali ET, Parada LF. 2005. TrkB has a cell-autonomous role in the establishment of hippocampal Schaffer collateral synapses. J Neurosci 25: 3774–3786.
30. Lush ME, Li Y, Kwon CH, Chen J, Parada LF. 2008. Neurofibromin is required for barrel formation in the mouse somatosensory cortex. J Neurosci 28: 1580–1587.
31. Marui T, Hashimoto O, Nanba E, Kato C, Tochigi M, Umekage T, Ishijima M, Kohda K, Kato N, Sasaki T. 2004. Association between the neurofibromatosis-1 (NF1) locus and autism in the Japanese population. Am J Med Genet B Neuropsychiatr Genet 131B: 43–47.
32. Mathis C, Collin L, Borrelli E. 2003. Oligodendrocyte ablation impairs cerebellum development. Development 130: 4709–4718.
33. Nissan MH, Pratilas CA, Jones AM, Ramirez R, Won H, Liu C, Tiwari S, Kong L, Hanrahan AJ, Yao Z, et al. 2014. Loss of NF1 in cutaneous melanoma is associated with RAS activation and MEK dependence. Cancer Res 74: 2340–2350.
34. Novak A, Guo C, Yang W, Nagy A, Lobe CG. 2000. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 28: 147–155.
35. Reith RM, McKenna J, Wu H, Hashmi SS, Cho SH, Dash PK, Gambello MJ. 2013. Loss of Tsc2 in Purkinje cells is associated with autistic-like behavior in a mouse model of tuberous sclerosis complex. Neurobiol Dis 51: 93–103.
36. Roussel MF, Hatten ME. 2011. Cerebellum development and medulloblastoma. Curr Top Dev Biol 94: 235–282.
37. Samuels IS, Saitta SC, Landreth GE. 2009. MAP’ing CNS development and cognition: an ERKsome process. Neuron 61: 160–167.
38. Schubbert S, Shannon K, Bollag G. 2007. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7: 295–308.
39. Shukla V, Coumoul X, Wang R-H, Kim H-S, Deng C-X. 2007. RNA interference and inhibition of MEK-ERK signaling prevent abnormal skeletal phenotypes in a mouse model of craniosynostosis. Nat Genet 39: 1145–1150.
40. Skefos J, Cummings C, Enzer K, Holiday J, Weed K, Levy E, Yuce T, Kemper T, Bauman M. 2014. Regional alterations in purkinje cell density in patients with autism. PLoS ONE 9: e81255.
41. Staser K, Park SJ, Rhodes SD, Zeng Y, He YZ, Shew MA, Gehlhausen JR, Cerabona D, Menon K, Chen S, et al. 2013. Normal hematopoiesis and neurofibromin-deficient myeloproliferative disease require Erk. J Clin Invest 123: 329–334.
42. Steinlin M. 2008. Cerebellar disorders in childhood: cognitive problems. Cerebellum 7: 607–610.
43. Tidyman WE, Rauen KA. 2009. The RASopathies: developmental syndromes of Ras/MAPK pathway dysregulation. Curr Opin Genet Dev 19: 230–236.
44. Timmann D, Drepper J, Frings M, Maschke M, Richter S, Gerwig M, Kolb FP. 2010. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex 46: 845–857.
45. Tsai PT, Hull C, Chu Y, Greene-Colozzi E, Sadowski AR, Leech JM, Steinberg J, Crawley JN, Regehr WG, Sahin M. 2012. Autistic-like behaviour and cerebellar dysfunction in Purkinje cell Tsc1 mutant mice. Nature 488: 647–651.
46. Wang VY, Rose MF, Zoghbi HY. 2005. Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48: 31–43.
47. Wang Y, Kim E, Wang X, Novitch BG, Yoshikawa K, Chang LS, Zhu Y. 2012. ERK inhibition rescues defects in fate specification of NF1-deficient neural progenitors and brain abnormalities. Cell 150: 816–830.
48. Wechsler-Reya RJ, Scott MP. 1999. Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22: 103–114.
49. Xu H, Yang Y, Tang X, Zhao M, Liang F, Xu P, Hou B, Xing Y, Bao X, Fan X. 2013. Bergmann glia function in granule cell migration during cerebellum development. Mol Neurobiol 47: 833–844.
50. Zhu Y, Romero MI, Ghosh P, Ye Z, Charnay P, Rushing EJ, Marth JD, Parada LF. 2001. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 15: 859–876.
51. Zhuo L, Theis M, Alvarez-Maya I, Brenner M, Willecke K, Messing A. 2001. HGFAP-cre transgenic mice for manipulation of glial and neuronal function in vivo. Genesis 31: 85–94.