Aberrant growth and differentiation of oligodendrocyte progenitors in neurofibromatosis type 1 mutants

Journal of Neuroscience

Volumn 23, Issue 18, 2003, Pages 7207-7217

  Bennett, Michael R ^a   Rizvi, Tilat A ^a   Karyala, Saikumar ^a   McKinnon, Randall D ^b   Ratner, Nancy ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Brain; FGF; NF1; Oligodendrocyte; Progenitor; Ras

Indexed keywords

NEUROFIBROMIN; PROTEIN FARNESYLTRANSFERASE INHIBITOR; RAS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CELL DIFFERENTIATION; CELL GROWTH; CONTROLLED STUDY; FEMALE; HEMIZYGOSITY; MOUSE; NEUROEPITHELIUM; NEUROFIBROMATOSIS; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SPINAL CORD; STEM CELL;

EID: 0041624494     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-18-07207.2003     Document Type: Article

References (86)

1. Armstrong RC, Le TQ, Frost EE, Borke RC, Vana AC (2002) Absence of fibroblast growth factor 2 promotes oligodendroglial repopulation of demyelinated white matter. J Neurosci 22:8574-8585.
2. Atit RP, Crowe M, Greenhalgh D, Wenstrup R, Ratner N (1999) The Nf1 tumor suppressor is required for mouse skin wound healing, fibroblast proliferation and collagen deposited by fibroblasts. J Invest Dermatol 112:835-842.
3. Bajenaru ML, Donahoe J, Corral T, Reilly KM, Brophy S, Pellicer A, Gutmann DH (2001) Neurofibromatosis 1 (NF1) heterozygosity results in a cell-autonomous growth advantage for astrocytes. Glia 33:314-323.
4. Belachew S, Chittajallu R, Aguirre AA, Yuan X, Kirby M, Anderson S, Gallo V (2003) Postnatal NG2 proteoglycan-expressing progenitor cells are intrinsically multipotent and generate functional neurons. J Cell Biol 161:169-186.
5. Birnbaum RA, O'Marcaigh A, Wardak Z, Zhang YY, Dranoff G, Jacks T, Clapp DW, Shannon KM (2000) Nf1 and Gmcsf interact in myeloid leukemogenesis. Mol Cell 5:189-195.
6. Bogler O, Wren D, Barnett SC, Land H, Noble M (1990) Cooperation between two growth factors promotes extended self-renewal and inhibits differentiation of oligodendrocyte-type-2 astrocyte (O-2A) progenitor cells. Proc Natl Acad Sci USA 87:6368-6372.
7. Bollag G, Clapp DW, Shih S, Adler F, Zhang YY, Thompson P, Lange BJ, Freedman MH, McCormick F, Jacks T, Shannon K (1996) Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nat Genet 12:144-148.
8. Brannan CI, Perkins AS, Vogel KS, Ratner N, Nordlund ML, Reid SW, Buchberg AM, Jenkins NA, Parada LF, Copeland NG (1994) Targeted-disruption of the neurofibromatosis type-1 gene leads to developmental abnormalities in heart and various neural crest-derived tissues. Genes Dev 8:1019-1029.
9. Chang A, Nishiyama A, Peterson J, Prineas J, Trapp D (2000) NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci 20:6404-6412.
10. Cichowski K, Jacks T (2001) NF1 tumor suppressor gene function: narrowing the GAP. Cell 104:593-604.
11. 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.
12. Daston MM, Ratner N (1992) Neurofibromin, a predominantly neuronal GTPase activating protein in the adult, is ubiquitously expressed during development. Dev Dyn 195:216-226.
13. Daston MM, Scrable H, Nordlund M, Sturbaum AK, Nissen LM, Ratner N (1992) The protein product of the neurofibromatosis type I gene is expressed at highest abundance in neurons, Schwann cells, and oligodendrocytes. Neuron 8:415-428.
14. DiPaolo DP, Zimmerman RA, Rorke LB, Zackai EH, Bilaniuk LT, Yachnis AT (1995) Neurofibromatosis type 1: pathologic substrate of high-signal-intensity foci in the brain. Radiology 195:721-724.
15. Donovan S, Shannon KM, Bollag G (2002) GTPase activating proteins: critical regulators of intracellular signaling. Biochim Biophys Acta 1602:23-45.
16. Dyer CA, Kendler A, Jean-Guillaume D, Awatramani R, Lee A, Mason LM, Kamholz J (2000) GFAP-positive and myelin marker-positive glia in normal and pathologic environments. J Neurosci Res 60:412-426.
17. Eastwood JD, Fiorella DJ, MacFall JF, Delong DM, Provenzale JM, Greenwood RS (2001) Increased brain apparent diffusion coefficient in children with neurofibromatosis type 1. Radiology 219:354-358.
18. Ebner S, Dunbar M, McKinnon RD (2000) Distinct roles for PI3K in proliferation and survival of oligodendrocyte progenitor cells. J Neurosci Res 62:336-345.
19. Eisenbarth GS, Walsh FS, Nirenberg M (1979) Monoclonal antibody to a plasma membrane antigen of neurons. Proc Natl Acad Sci USA 76:4913-4917.
20. Frost EE, Nielsen JA, Le TQ, Armstrong RC (2003) PDGF and FGF2 regulate oligodendrocyte progenitor responses to demyelination. J Neurobiol 54:457-472.
21. Gard AL, Pfeiffer SE (1990) Two proliferative stages of the oligodendrocyte lineage (A2B5+04- and 04+GalC-) under different mitogenic control. Neuron 5:615-625.
22. Giordano MJ, Mahadeo DK, He YY, Geist RT, Hsu C, Gutmann DH (1996) Increased expression of the neurofibromatosis 1 (NF1) gene product, neurofibromin, in astrocytes in response to cerebral ischemia. J Neurosci Res 43:246-253.
23. Godfraind C, Friedrich VL, Holmes KV, Dubois-Dalcq M (1989) In vivo analysis of glial cell phenotypes during a viral demyelinating disease in mice. J Cell Biol 109:2405-2416.
24. Gregori N, Proschel C, Noble M, Mayer-Proschel M (2002) The tripotential glial-restricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J Neurosci 22:248-256.
25. Griesser J, Kaufmann D, Maier B, Mailhammer R, Kuehl P, Krone W (1997) Post-transcriptional regulation of neurofibromin level in cultured human melanocytes in response to growth factors. J Invest Dermatol 108:275-280.
26. Guo HF, The I, Hannan F, Bernards A, Zhong Y (1997) Requirement for Drosophila NF1 for activation of adenylyl cyclase by PACAP38-like neuropeptides. Science 276:795-798.
27. Guo HF, Tong J, Hannan F, Luo L, Zhong Y (2000) A neurofibromatosis-1-regulated pathway is required for learning in Drosophila. Nature 403:895-898.
28. Gutmann DH, Loehr A, Zhang Y, Kim J, Henkemeyer M, Cashen A (1999) Haploinsufficiency for the neurofibromatosis 1 (NF1) tumor suppressor results in increased astrocyte proliferation. Oncogene 18:4450-4459.
29. Gutmann DH, Donahoe J, Brown T, James CD, Perry A (2000) Loss of neurofibromatosis 1 (NF1) gene expression in NF1-associated pilocytic astrocytomas. Neuropathol Appl Neurobiol 26:361-367.
30. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, Mayer-Proschel M (2001) Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21.
31. Jacks T, Shih TS, Schmitt EM, Bronson RT, Bernards A, Weinberg RA (1994) Tumour predisposition in mice heterozygous for a targeted mutation in Nf1. Nat Genet 7:353-361.
32. Johnson MR, Look AT, DeClue JE, Valentine MB, Lowy DR (1993) Inactivation of the NF1 gene in human melanoma and neuroblastoma cell lines without impaired regulation of GTP-Ras. Proc Natl Acad Sci USA 90:5539-5543.
33. Johnson MR, DeClue JE, Felzmann S, Vass WC, Xu G, White R, Lowy DR (1994) Neurofibromin can inhibit ras-dependent growth by a mechanism independent of its GTPase-accelerating function. Mol Cell Biol 14:641-645.
34. Kalyani A, Hobson K, Rao MS (1997) Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol 186:202-223.
35. Kaufmann D, Junge I, Bartelt B, Lattke H, Muller R (1999) On the lysosomal degradation of neurofibromin and its phosphorylation in cultured melanocytes. Biol Chem 380:1071-1078.
36. ras inhibition of Schwann cell proliferation and morphologic changes. Oncogene 11:325-335.
37. Kim H, Ling B, Ratner N (1997) Nf1-deficient mouse Schwann cells are angiogenic and invasive and can be induced to hyperproliferate: reversion of some phenotypes by an inhibitor of farnesyl protein transferase. Mol Cell Biol 17:862-872.
38. Kitano Y, Okamoto E, Saito K, Okano Y (1992) Effects of several growth factors on cultured neurofibroma cells. J Dermatol Sci 3:137-144.
39. Kluwe L, Hagel C, Tatagiba M, Thomas S, Stavrou D, Ostertag H, von Deimling A, Mautner VF (2001) Loss of NF1 alleles distinguish sporadic from NF1-associated pilocytic astrocytomas. J Neuropathol Exp Neurol 60:917-920.
40. Kohl NE, Omer CA, Conner MW, Anthony NJ, Davide JP, deSolms SJ, Giuliani EA, Gomez RP, Graham SL, Hamilton K, Handt LK, Hartmen GD, Koblan KS, Kral AM, Miller PJ, Mosser SD, O'Neill TJ, Rands E, Schaber MD, Gibbs JB, et al. (1995) Inhibition of farnesyltransferase induces regression of mammary and salivary carcinomas in ras transgenic mice. Nat Med 1:792-797.
41. Largaespada DA, Brannan CI, Jenkins NA, Copeland NG (1996) Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukemia. Nat Genet 12:137-143.
42. Li J, Perry A, James CD, Gutmann DH (2001) Cancer-related gene expression profiles in NF1-associated pilocytic astrocytomas. Neurology 56:885-890.
43. Listernick R, Louis DN, Packer RJ, Gutmann DH (1997) Optic pathway gliomas in children with neurofibromatosis 1: consensus statement from the NF1 Optic Pathway Glioma Task Force. Ann Neurol 41:143-149.
44. Louis JC, Magal E, Muir D, Manthorpe M, Varon S (1992) CG-4, a new bipotential glial cell line from rat brain, is capable of differentiating in vitro into either mature oligodendrocytes or type-2 astrocytes. J Neurosci Res 31:193-204.
45. Lu QR, Sun T, Zhu Z, Ma N, Garcia M, Stiles CD, Rowitch DH (2002) Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell 109:75-86.
46. McKinnon RD, Zazanis GA (1996) Transplantation of genetically engineered primary cells for the analysis of gene function in CNS development. Methods 10:332-342.
47. McKinnon RD, Matsui T, Dubois-Dalcq M, Aaronson SA (1990) FGF modulates the PDGF-driven pathway of oligodendrocyte development. Neuron 5:603-614.
48. McTigue DM, Wei P, Stokes BT (2001) Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci 21:3392-3400.
49. Miller RH, Hayes JE, Dyer KL, Sussman CR (1999) Mechanisms of oligodendrocyte commitment in the vertebrate CNS. Int J Dev Neurosci 17:753-763.
50. Mujtaba T, Piper DR, Kalyani A, Groves AK, Lucero MT, Rao MS (1999) Lineage-restricted neural precursors can be isolated from both the mouse neural tube and cultured ES cells. Dev Biol 214:113-127.
51. Nordlund M, Gu X, Shipley MT, Ratner N (1993) Neurofibromin is enriched in the endoplasmic reticulum of CNS neurons. J Neurosci 13:1588-1600.
52. Nordlund ML, Rizvi TA, Brannan CI, Ratner N (1995) Neurofibromin expression and astrogliosis in neurofibromatosis (Type 1) brains. J Neuropathol Exp Neurol 54:588-600.
53. North K, Ratner N (2003) The central nervous system in neurofibromatosis type 1. In: Genetics and genomics of neurobehavioral disorders (Fisch GS, ed), pp 97-131. Totowa, NJ: Humana.
54. Oh LY, Denninger A, Colvin JS, Vyas A, Tole S, Ornitz DM, Bansal R (2003) Fibroblast growth factor receptor 3 signaling regulates the onset of oligodendrocyte terminal differentiation. J Neurosci 23:883-894.
55. Osterhout DJ, Ebner S, Xu J, Ornitz DM, Zazanis GA, McKinnon RD (1997) Transplanted oligodendrocyte progenitor cells expressing a dominant-negative FGF receptor transgene fail to migrate in vivo. J Neurosci 17:9122-9132.
56. Ozonoff S (1999) Cognitive impairment in neurofibromatosis type 1. Am J Med Genet 89:45-52.
57. Prendergast GC (2000) Farnesyltransferase inhibitors: antineoplastic mechanism and clinical prospects. Curr Opin Cell Biol 12:166-173.
58. Rakic P (1995) A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci 18:383-388.
59. Rao MS (1999) Multipotent and restricted precursors in the central nervous system. Anat Rec 257:137-148.
60. Rao MS, Mayer-Proschel M (1997) Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 188:48-63.
61. Rao MS, Noble M, Mayer-Proschel M (1998) A tripotential glial precursor is present in the developing spinal cord. Proc Natl Acad Sci USA 95:3996-4001.
62. Redwine JM, Armstrong RC (1998) In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 37:413-428.
63. Rizvi TA, Akunuru S, de Courten-Myers G, Switzer III RC, Nordlund ML, Ratner N (1999) Region-specific astrogliosis in brains of mice heterozygous for mutations in the neurofibromatosis type 1 (Nf1) tumor suppressor. Brain Res 816:111-123.
64. Rowitch DH, Lu QR, Kessaris N, Richardson WD (2002) An "oligarchy" rules neural development. Trends Neurosci 25:417-422.
65. Sauvageot CM, Stiles CD (2002) Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12:244-249.
66. Schubert D (1974) Induced differentiation of clonal rat nerve and glial cells. Neurobiology 4:376-387.
67. Sebti S, Hamilton AD (1997) Inhibitors of prenyl transferases. Curr Opin Oncol 9:557-561.
68. Sherman LS, Atit R, Rosenbaum T, Cox AD, Ratner N (2000) Single cell Ras-GTP analysis reveals altered Ras activity in a subpopulation of neurofibroma Schwann cells but not fibroblasts. J Biol Chem 275:30740-30745.
69. Silva AJ, Frankland PW, Marowitz Z, Friedman E, Lazlo G, Cioffi D, Jacks T, Bourtchuladze R (1997) A mouse model for the learning and memory deficits associated with neurofibromatosis type I. Nat Genet 15:281-284.
70. Sommer I, Schachner M (1981) Monoclonal antibodies (O1 to O4) to oligodendrocyte cell surfaces: an immunocytological study in the central nervous system. Dev Biol 83:311-327.
71. Steen RG, Taylor JS, Langston JW, Glass JO, Brewer VR, Reddick WE, Mages R, Pivnick EK (2001) Prospective evaluation of the brain in asymptomatic children with neurofibromatosis type 1: relationship of macrocephaly to T1 relaxation changes and structural brain abnormalities. AJNR Am J Neuroradiol 22:810-817.
72. Sun T, Echelard Y, Lu R, Yuk DI, Kaing S, Stiles CD, Rowitch DH (2001) Olig bHLH proteins interact with homeodomain proteins to regulate cell fate acquisition in progenitors of the ventral neural tube. Curr Biol 11:1413-1420.
73. Temple S, Alvarez-Buylla A (1999) Stem cells in the adult mammalian central nervous system. Curr Opin Neurobiol 9:135-141.
74. Tong J, Hannan F, Zhu Y, Bernards A, Zhong Y (2002) Neurofibromin regulates G protein-stimulated adenylyl cyclase activity. Nat Neurosci 5:95-96.
75. Vemuri GS, McMorris FA (1996) Oligodendrocytes and their precursors require phosphatidylinositol 3-kinase signaling for survival. Development 122:2529-2537.
76. Vogel KS, Brannan CI, Jenkins NA, Copeland NG, Parada LF (1995) Loss of neurofibromin results in neurotrophin-independent survival of embryonic sensory and sympathetic neurons. Cell 82:733-742.
77. Vogel KS, El-Afandi M, Parada LF (2000) Neurofibromin negatively regulates neurotrophin signaling through p21ras in embryonic sensory neurons. Mol Cell Neurosci 15:398-407.
78. Wang PY, Kaufmann WE, Koth CW, Denckla MB, Barker PB (2000) Thalamic involvement in neurofibromatosis type 1: evaluation with proton magnetic resonance spectroscopic imaging. Ann Neurol 47:477-484.
79. Watanabe M, Toyama Y, Nishiyama A (2002) Differentiation of proliferated NG2-positive glial progenitor cells in a remyelinating lesion. J Neurosci Res 69:826-836.
80. Wolswijk G, Noble M (1989) Identification of an adult-specific glial progenitor cell. Development 105:387-400.
81. Wu Q, Miller RH, Ransohoff RM, Robinson S, Bu J, Nishiyama A (2000) Elevatated levels of the chemoking GRO-1 correlate with elevated oligodendrocyte progenitor proliferation in the Jimpy mutant. J Neurosci 20:2609-2617.
82. Yan N, Ricca C, Fletcher J, Glover T, Seizinger BR, Manne V (1995) Farnesyl-transferase inhibitors block the neurofibromatosis type I (NF1) malignant phenotype. Cancer Res 55:3569-3575.
83. Yasuda T, Grinspan J, Stern J, Franceschini B, Bannerman P, Pleasure D (1995) Apoptosis occurs in the oligodendroglial lineage, and is prevented by basic fibroblast growth factor. J Neurosci Res 40:306-317.
84. Zhang YY, Vik TA, Ryder JW, Srour EF, Jacks T, Shannon K, Clapp DW (1998) Nf1 regulates hematopoietic progenitor cell growth and ras signaling in response to multiple cytokines. J Exp Med 187:1893-1902.
85. Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61-73.
86. 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.