Nucleophosmin mediates mammalian target of rapamycin-dependent actin cytoskeleton dynamics and proliferation in neurofibromin-deficient astrocytes

Cancer Research

Volumn 67, Issue 10, 2007, Pages 4790-4799

  Sandsmark, Danielle K ^a   Zhang, Huabiao ^a   Hegedus, Balazs ^a   Pelletier, Corey L ^a   Weber, Jason D ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ELONGATION FACTOR 1; MAMMALIAN TARGET OF RAPAMYCIN; NUCLEOPHOSMIN; PROTEIN SERINE THREONINE KINASE; RAC1 PROTEIN; RAS PROTEIN; S6 KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; BIOGENESIS; CELL GROWTH; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STRESS FIBER;

ACTINS; ANIMALS; ASTROCYTES; CARRIER PROTEINS; CELL GROWTH PROCESSES; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; ENZYME ACTIVATION; MICE; NEUROPEPTIDES; NUCLEAR PROTEINS; PHOSPHOPROTEINS; PROTEIN KINASE C-ALPHA; PROTEIN KINASES; RAC GTP-BINDING PROTEINS; RIBOSOMAL PROTEIN S6 KINASES;

EID: 34250379843     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-4470     Document Type: Article

References (47)

1. Listernick R, Charrow J, Gutmann DH. Intracranial gliomas in neurofibromatosis type 1. Am J Hum Genet 1999;89:38-44.
2. DeClue JE, Papageorge AG, Fletcher JA, et al. Abnormal regulation of mammalian p21ras contributes to malignant tumor growth in von Recklinghausen (type 1) neurofibromatosis. Cell 1992;69:265-73.
3. Basu TN, Gutmann DH, Fletcher JA, et al. Aberrant regulation of ras proteins in malignant tumour cells from type 1 neurofibromatosis patients. Nature 1992; 356:713-5.
4. Bollag G, Clapp DW, Shih S, et al. Loss of NF1 results in activation of the Ras signaling pathway and leads to aberrant growth in haematopoietic cells. Nat Genet 1996;12:144-8.
5. Largaespada DA, Brannan CI, Jenkins NA, Copeland NG. Nf1 deficiency causes Ras-mediated granulocyte/macrophage colony stimulating factor hypersensitivity and chronic myeloid leukaemia. Nat Genet 1996;12: 137-43.
6. Sherman LS, Atit R, Rosenbaum T, Cox AD, Ratner N. Single cell Ras-GTP analysis reveals altered Ras activity in a subpopulation of neurofibroma Schwann cells but not fibroblasts. J Biol Chem 2000;275:30740-5.
7. Bajenaru ML, Hernandez MR, Perry A, et al. Optic nerve glioma in mice requires astrocyte Nf1 gene inactivation and Nf1 brain heterozygosity. Cancer Res 2003;63:8573-7.
8. Bajenaru ML, Zhu Y, Hedrick NM, et al. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol Cell Biol 2002;22:5100-13.
9. Dasgupta B, Li W, Perry A, Gutmann DH. Glioma formation in neurofibromatosis 1 reflects preferential activation of K-RAS in astrocytes. Cancer Res 2005;65: 236-45.
10. Dasgupta B, Yi Y, Chen DY, Weber JD, Gutmann DH. Proteomic analysis reveals hyperactivation of the mammalian target of rapamycin pathway in neurofibromatosis 1-associated human and mouse brain tumors. Cancer Res 2005;65:2755-60.
11. Johannessen CM, Reczek EE, James MF, et al. The NF1 tumor suppressor critically regulates TSC2 and mTOR Proc Natl Acad Sci U S A 2005;102:8573-8.
12. Huang Y, Rangwala F, Fulkerson PC, et al. Role of TC21/R-Ras2 in enhanced migration of neurofibromin-deficient Schwann cells. Oncogene 2004;23:368-78.
13. Zhu Y, Romero MI, Ghosh P, et al. Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Genes Dev 2001;15:859-76.
14. Uhlmann EJ, Li W, Scheidenhelm DK, et al. Loss of tuberous sclerosis complex 1 (Tsc1) expression results in increased Rheb/S6K pathway signaling important for astrocyte cell size regulation. Glia 2004;47:180-8.
15. Bajenaru ML, Donahoe J, Corral T, et al. Neurofibromatosis 1 (NF1) heterozygosity results in a cell-autonomous growth advantage for astrocytes. Glia 2001;33: 314-23.
16. Jacinto E, Loewith R, Schmidt A, et al. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 2004;6:1122-8.
17. Sarbassov DD, Ali SM, Kim D-H, et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 2004;14:1296-302.
18. Sechler JL, Corbett SA, Wenk MB, Schwarzbauer JE. Modulation of cell-extracellular matrix interactions. Ann N Y Acad Sci 1998;857:143-54.
19. Geiger B, Tokuyasu KT, Dutton AH, Singer SJ. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A 1980;77:4127-31.
20. Gingras A-C, Gygi SP, Raught B, et al. Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 1999;13:1422-37.
21. Nakashima S. Protein kinase Cα: regulation and biological function. J Biochem (Tokyo) 2002;132:669-75.
22. Yang C, Liu Y, Leskow FC, Weaver VM, Kazanietz MG. Rac-GAP-dependent inhibition of breast cancer cell proliferation by β2-chimerin. J Biol Chem 2005;280: 24363-70.
23. Wang G, Beier F. Rac1/Cdc42 and RhoA GTPases antagonistically regulate chondrocyte proliferation, hypertrophy, and apoptosis. J Bone Miner Res 2005;20: 1022-31.
24. Vidali L, Chen F, Cicchetti G, Ohta Y, Kwiatkowski DJ. Rac1-null mouse embryonic fibroblasts are motile and respond to platelet-derived growth factor. Mol Biol Cell 2006;17:2377-90.
25. Grisendi S, Bernardi R, Rossi M, et al. Role of nucleophosmin in embryonic development and tumorigenesis. Nature 2005;437:147-53.
26. Yu Y, Maggi LB, Jr., Brady SN, et al. Nucleophosmin is essential for ribosomal protein L5 nuclear export. Mol Cell Biol 2006;26:3798-809.
27. Pelletier CL, Maggi LB, Jr., Scheidenhelm DK, Gutmann DH, Weber JD. Tsc1 sets the rate of ribosome export and protein synthesis through nucleophosmin translation. Cancer Res 2007;67:1609-17.
28. Kudo N, Matsumori N, Taoka H, et al. Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc Natl Acad Sci U S A 1999;96:9112-7.
29. Nelen MR, Padberg GW, Peeters EAJ, et al. Localization of the gene for Cowden disease to chromosome 10q22-23. Nat Genet 1996;13:114-6.
30. Ohgaki H, Dessen P, Jourde B, et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res 2004;64:6892-9.
31. Fraser MM, Zhu X, Kwon CH, et al. Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res 2004;64:7773-9.
32. Xiao A, Yin C, Yang C, et al. Somatic induction of Pten loss in a preclinical astrocytoma model reveals major roles in disease progression and avenues for target discovery and validation. Cancer Res 2005;65: 5172-80.
33. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. Rheb binds and regulates the mTOR kinase. Curr Biol 2005;15:702-13.
34. Inoki K, Li Y, Zhu T, Wu J, Guan K-L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 2002;4:648-57.
35. Kwiatkowski DJ, Zhang H, Bandura JL, et al. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells. Hum Mol Genet 2002;11: 525-34.
36. Benvenuto G, Li S, Brown SJ, et al. The tuberous sclerosis-1 (TSC1) gene product hamartin suppresses cell growth and augments the expression of the TSC2 product tuberin by inhibiting its ubiquitination. Oncogene 2000;19:6306-16.
37. Miloloza A, Rosner M, Nellist M, et al. The TSC1 gene product, hamartin, negatively regulates cell proliferation. Hum Mol Genet 2000;9:1721-7.
38. Soucek T, Rosner M, Miloloza A, et al. Tuberous sclerosis causing mutants of the TSC2 gene product affect proliferation and p27 expression. Oncogene 2001; 20:4904-9.
39. Goncharova E, Goncharov D, Noonan D, Krymskaya VP. TSC2 modulates actin cytoskeleton and focal adhesion through TSC1-binding domain and the Rac1 GTPase. J Cell Biol 2004;167:1171-82.
40. Astrinidis A, Cash TP, Hunter DS, et al. Tuberin, the tuberous sclerosis complex 2 tumor suppressor gene product, regulates Rho activation, cell adhesion, and migration. Oncogene 2002;21:8470-6.
41. Lamb RF, Roy C, Diefenbach TJ, et al. The TSC1 tumour suppressor hamartin regulates cell adhesion through ERM proteins and the GTPase Rho. Nat Cell Biol 2000;2:281-7.
42. Pende M, Um SH, Mieulet V, et al. S6K1-/-/S6K2-/-mice exhibit perinatal lethality and rapamycin-sensitive 5′-terminal oligopyrimidine mTOR translation and reveal a mitogen activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 2004;24:3112-24.
43. Chalhoub N, Kozma SC, Baker SJ. S6k1 is not required for Pten-deficient neuronal hypertrophy. Brain Res 2006;1100:32-41.
44. Feuerstein N, Spiegel S, Mond JJ. The nuclear matrix protein, numatrin (B23), is associated with growth factor-induced mitogenesis in Swiss 3T3 fibroblasts and with T lymphocyte proliferation stimulated by lectins and anti-T cell antigen receptor antibody. J Cell Biol 1988;107:1629-42.
45. Feuerstein N, Chan PK, Mond JJ. Identification of numatrin, the nuclear matrix protein associated with induction of mitogenesis, as the nucleolar protein B23. Implication for the role of the nucleolus in early transduction of mitogenic signals. J Biol Chem 1988; 263:10608-12.
46. Rajasekhar VK, Viale A, Socci ND, et al. Oncogenic Ras and Akt signaling contribute to glioblastoma formation by differential recruitment of existing mRNAs to polysomes. Mol Cell 2003;12:889-901.
47. Riemenschneider MJ, Betensky RA, Pasedag SM, Louis DN. Akt activation in human glioblastomas enhances proliferation via TSC2 and S6 kinase signaling. Cancer Res 2006;66:5618-23.