Spred1, a negative regulator of Ras-MAPK-ERK, is enriched in CNS germinal zones, dampens NSC proliferation, and maintains ventricular zone structure

Genes and Development

Volumn 24, Issue 1, 2010, Pages 45-56

  Phoenix, Timothy N ^a,b   Temple, Sally ^a,b  

^a New York Neural Stem Cell Institute   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

Author keywords

MAPK ERK signaling; Neural stem cells; Periventricular heterotopia; Self renewal; Spredl

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SPRED1; RAS PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL RENEWAL; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME ACTIVITY; FOREBRAIN; GENE MUTATION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PERIVENTRICULAR HETEROTOPIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUBVENTRICULAR ZONE;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBRAL CORTEX; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GENES, RAS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEURONS; PERIVENTRICULAR NODULAR HETEROTOPIA; PREGNANCY; REPRESSOR PROTEINS; STEM CELLS;

EID: 73549106328     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1839510     Document Type: Article

References (47)

1. Abramova N, Charniga C, Goderie SK, Temple S. 2005. Stage-specific changes in gene expression in acutely isolated mouse CNS progenitor cells. Dev Biol 283: 269-281.
2. 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.
3. Barnabe-Heider F, Miller FD. 2003. Endogenously produced neurotrophins regulate survival and differentiation of cortical progenitors via distinct signaling pathways. J Neurosci 23: 5149-5160.
4. Barnabe-Heider F, Wasylnka JA, Fernandes KJ, Porsche C, Sendtner M, Kaplan DR, Miller FD. 2005. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 48: 253-265.
5. Bayer SA, Altman J, Russo RJ, Dai XF, Simmons JA. 1991. Cell migration in the rat embryonic neocortex. J Comp Neurol 307: 499-516.
6. Brems H, Chmara M, Sahbatou M, Denayer E, Taniguchi K, Kato R, Somers R, Messiaen L, De Schepper S, Fryns JP, et al. 2007. Germline loss-of-function mutations in SPRED1 cause a neurofibromatosis 1-like phenotype. Nat Genet 39: 1120-1126.
7. Bundschu K, Walter U, Schuh K. 2007. Getting a first clue about SPRED functions. Bioessays 29: 897-907.
8. Burrows RC, Wancio D, Levitt P, Lillien L. 1997. Response diversity and the timing of progenitor cell maturation are regulated by developmental changes in EGFR expression in the cortex. Neuron 19: 251-267.
9. Cichowski K, Jacks T. 2001. NF1 tumor suppressor gene function: Narrowing the GAP. Cell 104: 593-604.
10. Costa RM, Federov NB, Kogan JH, Murphy GG, Stern J, Ohno M, Kucherlapati R, Jacks T, Silva AJ. 2002. Mechanism for the learning deficits in a mouse model of neurofibromatosis type 1. Nature 415: 526-530.
11. 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.
12. Dasgupta B, Gutmann DH. 2005. Neurofibromin regulates neural stem cell proliferation, survival, and astroglial differentiation in vitro and in vivo. J Neurosci 25: 5584-5594.
13. Denayer E, Ahmed T, Brems H, Van Woerden G, Borgesius NZ, Callaerts-Vegh Z, Yoshimura A, Hartmann D, Elgersma Y, D'Hooge R, et al. 2008. Spred1 is required for synaptic plasticity and hippocampus-dependent learning. J Neurosci 28: 14443-14449.
14. Engelhardt CM, Bundschu K, Messerschmitt M, Renne T, Walter U, Reinhard M, Schuh K. 2004. Expression and subcellular localization of Spred proteins in mouse and human tissues. Histochem Cell Biol 122: 527-538.
15. Englund C, Fink A, Lau C, Pham D, Daza R, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in the developing neocortex. J Neurosci 25: 247-251.
16. Fasano CA, Dimos JT, Ivanova NB, Lowry N, Lemischka IR, Temple S. 2007. shRNA knockdown of Bmi-1 reveals a critical role for p21-Rb pathway in NSC self-renewal during development. Cell Stem Cell 1: 87-99.
17. Fedi M, Anne Mitchell L, Kalnins RM, Gutmann DH, Perry A, Newton M, Brodtmann A, Berkovic SF. 2004. Glioneuronal tumours in neurofibromatosis type 1: MRI-pathological study. J Clin Neurosci 11: 745-747.
18. Ferland RJ, Batiz LF, Neal J, Lian G, Bundock E, Lu J, Hsiao YC, Diamond R, Mei D, Banham AH, et al. 2009. Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia. Hum Mol Genet 18: 497-516.
19. Gauthier AS, Furstoss O, Araki T, Chan R, Neel BG, Kaplan DR, Miller FD. 2007. Control of CNS cell-fate decisions by SHP-2 and its dysregulation in Noonan syndrome. Neuron 54: 245-262.
20. Goh KL, Cai L, Cepko CL, Gertler FB. 2002. Ena/VASP proteins regulate cortical neuronal positioning. Curr Biol 2: 565-569.
21. 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 Ras-dependent mechanisms. Cell Stem Cell 1: 443-457.
22. Inoue H, Kato R, Fukuyama S, Nonami A, Taniguchi K, Matsumoto K, Nakano T, Tsuda M, Matsumura M, Kubo M, et al. 2005. Spred-1 negatively regulates allergen-induced airway eosinophilia and hyperresponsiveness. J Exp Med 201: 73-82.
23. Jin K, Zhu Y, Sun Y, Mao XO, Xie L, Greenberg DA. 2002. Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci 99: 11946-11950.
24. Kato R, Nonami A, Taketomi T, Wakioka T, Kuroiwa A, Matsuda Y, Yoshimura A. 2003. Molecular cloning of mammalian Spred-3 which suppresses tyrosine kinase-mediated Erk activation. Biochem Biophys Res Commun 302: 767-772.
25. Korf BR, Schneider G, Poussaint TY. 1999. Structural anomalies revealed by neuroimaging studies in the brains of patients with neurofibromatosis type 1 and large deletions. Genet Med 1: 136-140.
26. 2+ switch. Am J Cell Physiol 282: 1235-1245.
27. Liu G, Thomas L, Warren RA, Enns CA, Cunningham CC, Harwig JH, Thomas G. 1997. Cytoskeletal protein ABP-280 directs the intracellular trafficking of furin and modulates proprotein processing in the endocytic pathway. J Cell Biol 139: 1719-1733.
28. Lush ME, Li Y, Kwon CH, Chen J, Parada LF. 2008. Neuro-fibromin is required for barrel formation in the mouse somatosensory cortex. J Neurosci 28: 1580-1587.
29. 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.
30. Mbarek O, Marouillat S, Martineau J, Barthelemy C, Muh JP, Andres C. 1999. Association study of the NF1 gene and autistic disorder. Am J Med Genet 88: 729-732.
31. Miller FD, Gauthier AS. 2007. Timing is everything: Making neurons versus glia in the developing cortex. Neuron 54: 357-369.
32. Miyoshi K, Wakioka T, Nishinakamura H, Kamio M, Yang L, Inoue M, Hasegawa M, Yonemitsu Y, Komiya S, Yoshimura A. 2004. The Sprouty-related protein, Spred, inhibits cell motility, metastasis, and Rho-mediated actin reorganization. Oncogene 23: 5567-5576.
33. Nonami A, Kato R, Taniguchi K, Yoshiga D, Taketomi T, Fukuyama S, Harada M, Sasaki A, Yoshimura A. 2004. Spred-1 negatively regulates interleukin-3-mediated ERK/ mitogen-activated protein (MAP) kinase activation in hematopoietic cells. J Biol Chem 279: 52543-52551.
34. Noonan JA. 1994. Noonan syndrome. An update and review for the primary pediatrician. Clin Pediatr (Phila) 33: 548-555.
35. Qian X, Goderie SK, Shen Q, Stern JH, Temple S. 1998. Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125: 3143-3152.
36. Samuels IS, Karlo JC, Faruzzi AN, Pickering K, Herrup K, Sweatt JD, Saitta SC, Landreth GE. 2008. Deletion of ERK2 mitogen-activated protein kinase identifies its key roles in cortical neurogenesis and cognitive function. J Neurosci 28: 6983-6995.
37. Sarkisian MR, Bartley CM, Chi H, Nakamura F, Hashimoto-Torii K, Torii M, Flavell RA, Rakic P. 2006. MEKK4 signaling regulates filamin expression and neuronal migration. Neuron 52: 789-801.
38. Sasaki A, Taketomi T, Kato R, Saeki K, Nonami A, Sasaki M, Kuriyama M, Saito N, Shibuya M, Yoshimura A. 2003. Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat Cell Biol 5: 427-432.
39. Schubbert S, Shannon K, Bollag G. 2007. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer 7: 295-308.
40. Shen Q,Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S. 2006. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9: 743-751.
41. Trivier E, De Cesare D, Jacquot S, Pannetier S, Zackai E, Young I, Mandel JL, Sassone-Corsi P, Hanauer A. 1996. Mutations in the kinase Rsk-2 associated with Coffin-Lowry syndrome. Nature 384: 567-570.
42. Vaccarino FM, Schwartz ML, Raballo R, Nilsen J, Rhee J, Zhou M, Doetschman T, Coffin JD, Wyland JJ, Hung YT. 1999. Changes in cerebral cortex size are governed by fibroblast growth factor during embryogenesis. Nat Neurosci 2: 848. doi: 10.1038/12226.
43. Vivarelli R, Grosso S, Calabrese F, Farnetani M, Di Bartolo R, Morgese G, Balestri P. 2003. Epilepsy in neurofibromatosis 1. J Child Neurol 18: 338-342.
44. Wakioka T, Sasaki A, Kato R, Shouda T, Matsumoto A, Miyoshi K, Tsuneoka M, Komiya S, Baron R, Yoshimura A. 2001. Spred is a Sprouty-related suppressor of Ras signalling. Nature 412: 647-651.
45. Zhu Y, Parada LF. 2001. Neurofibromin, a tumor suppressor in the nervous system. Exp Cell Res 264: 19-28.
46. 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.
47. Zhu Y, Harada T, Liu L, Lush ME, Guignard F, Harada C, Burns DK, Bajenaru ML, Gutmann DH, Parada LF. 2005. Inactivation of NF1 in CNS causes increased glial progenitor proliferation and optic glioma formation. Development 132: 5577-5588.