Protein 4.1B/differentially expressed in adenocarcinoma of the lung-1 functions as a growth suppressor in meningioma cells by activating Rac1-dependent c-Jun-NH2-kinase signaling

Cancer Research

Volumn 66, Issue 10, 2006, Pages 5295-5303

  Gerber, Mark A ^a   Bahr, Scott M ^a   Gutmann, David H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A; ERYTHROCYTE BAND 4.1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 9; MIXED LINEAGE KINASE 3; RAC PROTEIN; STEROID RECEPTOR COACTIVATOR 1;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE CONTROL; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ADENOCARCINOMA; MENINGIOMA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CELL GROWTH PROCESSES; CYCLIN A; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASES; MEMBRANE PROTEINS; MENINGIOMA; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 33744939725     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-1628     Document Type: Article

References (51)

1. Ruttledge MH, Sarrazin J, Rangaratnam S, et al. Evidence for the complete inactivation of the NF2 gene in the majority of sporadic meningiomas. Nat Genet 1994;6:180-4.
2. Gutmann DH, Giordano MJ, Fishback AS, Guha A. Loss of merlin expression in sporadic meningiomas, ependymomas and schwannomas. Neurology 1997;49:267-70.
3. Huynh DP, Mautner V, Baser ME, Stavrou D, Pulst SM. Immunohistochemical detection of schwannomin and neurofibromin in vestibular schwannomas, ependymomas and meningiomas. J Neuropathol Exp Neurol 1997; 56:382-90.
4. Leone PE, Bello MJ, de Campos JM, et al. NF2 gene mutations and allelic status of 1p, 14q and 22q in sporadic meningiomas. Oncogene 1999;18:2231-9.
5. Ueki K, Wen-Bin C, Narita Y, Asai A, Kirino T. Tight association of loss of merlin expression with loss of heterozygosity at chromosome 22q in sporadic meningiomas. Cancer Res 1999;59:5995-8.
6. Trofatter JA, MacCollin MM, Rutter JL, et al. A novel moesin-, ezrin-, radixin-like gene is a candidate for the neurofibromatosis 2 tumor suppressor. Cell 1993;72: 791-800.
7. Rouleau GA, Merel P, Lutchman M, et al. Alteration in a new gene encoding a putative membrane-organizing protein causes neuro-fibromatosis type 2. Nature 1993; 363:495-6.
8. Hoover KB, Bryant PJ. The genetics of the protein 4.1 family: organizers of the membrane and cytoskeleton. Curr Opin Cell Biol 2000;12:229-34.
9. Sun CX, Robb VA, Gutmann DH. Protein 4.1 tumor suppressors: getting a PERM grip on growth regulation. J Cell Sci 2002;115:3991-4000.
10. Tran YK, Bogler O, Gorse KM, Wieland I, Green MR, Newsham IF. A novel member of the NF2/ERM/4.1 superfamily with growth suppressing properties in lung cancer. Cancer Res 1999;59:35-43.
11. Singh PK, Gutmann DH, Fuller CE, Newsham IF, Perry A. Differential involvement of protein 4.1 family members DAL-1 and NF2 in intracranial and intraspinal ependymomas. Mod Pathol 2002;15:526-31.
12. Ohno N, Terada N, Murata S, et al. Immunolocalization of protein 4.1B/DAL-1 during neoplastic transformation of mouse and human intestinal epithelium. Histochem Cell Biol 2004;122:579-86.
13. Kikuchi S, Yamada D, Fukami T, et al. Promoter methylation of DAL-1/4.1B predicts poor prognosis in non-small cell lung cancer. Clin Cancer Res 2005;11: 2954-61.
14. Gutmann DH, Donahoe J, Perry A, et al. Loss of DAL-1, a protein 4.1-related tumor suppressor, is an important early event in the pathogenesis of meningiomas. Hum Mol Genet 2000;9:1495-500.
15. Perry A, Cai DX, Scheithauer BW, et al. Merlin, DAL-1, and Progesterone receptor expression in clinicopathologic subsets of meningioma: a correlative immunohistochemical study of 175 cases. J Neuropathol Exp Neurol 2000;59:872-9.
16. Gutmann DH, Hirbe AC, Huang Z-y, Haipck CA. The protein 4.1 tumor suppressor, DAL-1, impairs cell motility, but regulates proliferation in a cell-type-specific fashion. Neurobiol Dis 2001;8:266-78.
17. Robb VA, Gerber MA, Hart-Mahon EK, Gutmann DH. Membrane localization of the U2 domain of protein 4.1B is necessary and sufficient for meningioma growth suppression. Oncogene 2005;24:1946-57.
18. Parra M, Gascard P, Walensky LD, et al. Molecular and Functional characterization of protein 4.1B, a novel member of the protein 4.1 family with high level, focal expression in brain. J Biol Chem 2000;275: 3247-55.
19. Lee WH. Characterization of a newly established malignant meningioma cell line of the human brain: IOMM-Lee. Neurosurgery 1990;27:389-95.
20. Robb VA, Li W, Gutmann DH. Disruption of 14-3-3 binding does not impair protein 4.1B growth suppression. Oncogene 2004;23:3589-96.
21. Charboneau AL, Singh V, Yu T, Newsham IF. Suppression of growth and increased cellular attachment after expression of DAL-1 in MCF-7 breast cancer cells. Int J Cancer 2002;100:181-8.
22. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Genet Dev 2002;12:14-21.
23. Manning AM, Davis RJ. Targeting JNK for therapeutic benefit: from junk to gold? Nat Rev Drug Discov 2003;2: 554-65.
24. Kanda H, Masayuki M. Regulatory roles of JNK in programmed cell death. J Biochem 2004;136:1-6.
25. Wang S, Nath N, Minden A, Chellappan S. Regulation of Rb and E2F by signal transduction cascades: divergent effects of JNK1 and p38 kinases. EMBO J 1999;18:1559-70.
26. Chauhan D, Hideshima T, Treon S, et al. Functional interaction between retinoblastoma protein and stress-activated protein kinase in multiple myeloma cells. Cancer Res 1999;59:1192-5.
27. Schulze A, Zerfass K, Spitkovsky D, et al. Cell cycle regulation of the cyclin a gene promoter is mediated by a variant E2F site. Proc Natl Acad Sci U S A 1995;92: 11264-8.
28. Rosenberg AA, Zindy F, Le Deist F, et al. Over-expression of human cyclin A advances entry into S phase. Oncogene 1995;10:1501-9.
29. Sherr CJ. Cancer cell cycles. Science 1996;274:1672-7.
30. Bukholm IR, Bukholm G, Nesland JM. Over-expression of cyclin A is highly associated with early relapse and reduced survival in patients with primary breast carcinomas. Int J Cancer 2001;93:283-7.
31. Runs R, Kissil JL, Newsham IF, Jacks T, Gutmann DH, Sherman LS. Protein 4.1B expression is induced in mammary epithelial cells during pregnancy and regulates their proliferation. Oncogene 2005;24:6502-15.
32. Barr RK, Kendrick TS, Bogoyevitch MA. Identification of the critical features of a small peptide inhibitor of JNK activity. J Biol Chem 2002;277:10987-97.
33. Bonny C, Oberson A, Negri S, Sauser C, Schorderet DF. Cell-permeable peptide inhibitors of JNK: novel blockers of {β}-cell death. Diabetes 2001;50:77-82.
34. Teramoto H, Coso OA, Miyata H, Igishi T, Miki T, Gutkind JS. Signaling from the small GTP-binding proteins Rac1 and Cdc42 to the c-Jun N-terminal kinase/stress-activated protein kinase pathway. A role for mixed lineage kinase 3/protein-tyrosine kinase 1, a novel member of the mixed lineage kinase family. J Biol Chem 1996;271:27225-8.
35. Tobiume K, Matsuzawa A, Takahashi T, et al. ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2001;2:222-8.
36. Pan J, Zhang QG, Zhang GY. The neuroprotective effects of K252a through inhibiting MLK3/MKK7/JNK3 signaling pathway on ischemic brain injury in rat hippocampal CA1 region. Neuroscience 2005;131:147-59.
37. Roux PP, Dorval G, Boudreau M, et al. K252a and CEP1347 Are neuroprotective compounds that inhibit mixed-lineage kinase-3 and induce activation of Akt and ERK. J Biol Chem 2002;277:49473-80.
38. Bock BC, Vacratsis PO, Qamirani E, Gallo KA. Cdc-42-induced activation of the mixed-lineage kinase SPRK in vivo. J Biochem (Tokyo) 2000;275:14231-41.
39. Burbelo PD, Drechsel D, Hall A. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J Biochem (Tokyo) 1995; 270:29071-4.
40. Lambert JM, Karnoub AE, Graves LM, Campbell SL, Der CJ. Role of MLK3-mediated activation of p70 S6 kinase in Rac1 transformation. J Biol Chem 2002;277: 4770-7.
41. Rosso SB, Sussman D, Wynshaw-Boris A, Salinas PC. Wnt signaling through dishevelled, Rac and JNK regulates dendritic development. Nat Neurosci 2005;8:34-42.
42. Minden A, Lin A, Claret FX Abo A, Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995;81:1147-57.
43. Coso OA, Chiariello M, Yu JC, et al. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995;81:1137-46.
44. Schmitt JM, Stork PJS. G(α) and G(β-γ) require distinct Src-dependent pathways to activate Rap1 and Ras. J Biol Chem 2002;277:43024-32.
45. Linseman DA, Hofmann F, Fisher SK. A role for the small molecular weight GTPases, Rho and Cdc42, in muscarinic receptor signaling to focal adhesion kinase. J Neurochem 2000;74:2010-20.
46. Turkson J, Bowman T, Adnane J, et al. Requirement for Ras/Rac1-mediated p38 and c-Jun N-terminal kinase signaling in Stat3 transcriptional activity induced by the Src oncoprotein. Mol Cell Biol 1999;19:7519-28.
47. Servitja J-M, Marinissen MJ, Sodhi A, Bustelo XR, Gutkind JS. Rac1 function is required for Src-induced transformation: evidence for a role of Tiam1 and Vav2 in Rac activation by Src. J Biol Chem 2003;278: 34339-46.
48. Hanke JH, Gardner JP, Dow RL, et al. Discovery of a novel, potent, and Src family-selective tyrosine kinase inhibitor. J Biol Chem 1996;271:695-701.
49. Salazar EP, Rozengurt E. Bombesin and platelet-derived growth factor induce association of endogenous focal adhesion kinase with Src in intact Swiss 3T3 cells. J Biol Chem 1999;274:28371-8.
50. Yu T, Robb VA, Singh V, Gutmann DH, Newsham IF. The 4.1/ezrin/radixin/ moesin domain of the DAL-1/ Protein 4.1B tumour suppressor interacts with 14-3-3 proteins. Biochem J 2002;365:783-9.
51. Singh V, Miranda TB, Jiang W, et al. DAL-1/4.1B tumor suppressor interacts with protein arginine N-methyltransferase 3 (PRMT3) and inhibits its ability to methylate substrates in vitro and in vivo. Oncogene 2004;23:7761-71.