NDRG4 is a novel oncogenic protein and p53 associated regulator of apoptosis in malignant meningioma cells

Oncotarget

Volumn 6, Issue 19, 2015, Pages 17594-17604

  Kotipatruni, Rama P ^a   Ren, Xuan ^a   Thotala, Dinesh ^a,b   Jaboin, Jerry J ^a,b  

^a WASHINGTON UNIVERSITY   (United States)

^b Washington University in St Louis School of Medicine   (United States)

Author keywords

Lentiviral shRNA; Meningioma; Mitochondrial apoptosis; NDRG4; p53

Indexed keywords

CASPASE 3; CASPASE 9; CYTOCHROME C; N MYC DOWNSTREAM REGULATED GENE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; ONCOPROTEIN; PIFITHRIN ALPHA; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53; UNCLASSIFIED DRUG; MUSCLE PROTEIN; NDRG4 PROTEIN, HUMAN; NERVE PROTEIN; TP53 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; CANCER GROWTH; CELL DEATH; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOCHEMISTRY; DOWN REGULATION; FLOW CYTOMETRY; GENE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MALIGNANT MENINGIOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; NDRG4 GENE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; UPREGULATION; CELL MOTION; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; IMMUNOBLOTTING; MENINGIOMA; METABOLISM; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE KNOCKDOWN TECHNIQUES; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MENINGEAL NEOPLASMS; MENINGIOMA; MUSCLE PROTEINS; NERVE TISSUE PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84938235049     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.4009     Document Type: Article

References (58)

1. Perry A, Scheithauer BW, Stafford SL, Lohse CM, Wollan PC. "Malignancy" in meningiomas: a clinicopathologic study of 116 patients, with grading implications. Cancer. 1999; 85:2046-56.
2. Kepes J.J. Presidential address: the histopathology of meningiomas. A reflection of origins and expected behavior? J Neuropathol Exp Neurol. 1986; 45:95-107.
3. O'Rahilly R, F. Muller. The meninges in human development. JNeuropathol Exp Neurol. 1986; 45:588-608.
4. Dziuk TW, Woo S, Butler EB, Thornby J, Grossman R, Dennis WS, Lu H, Carpenter LS, Chiu JK. Malignant meningioma: an indication for initial aggressive surgery and adjuvant radiotherapy. J Neurooncol. 1998; 37:177-88.
5. Morantz RA, Wara WW. Gamma Knife Radiosurgery in the Treatment of Brain Tumors. Cancer Control. 1995; 2:300-308.
6. Coke CC, Corn BW, Werner-Wasik M, Xie Y, Curran WJ Jr. Atypical and malignant meningiomas: an outcome report of seventeen cases. J Neurooncol. 1998; 39:65-70.
7. Hug EB, Devries A, Thornton AF, Munzenride JE, Pardo FS, Hedley-Whyte ET, Bussiere MR, Ojemann R. Management of atypical and malignant meningiomas: role of high-dose, 3D-conformal radiation therapy. J Neurooncol. 2000; 48:151-60.
8. Moazzam AA, Wagle N, Zada G. Recent developments in chemotherapy for meningiomas: a review. Neurosurg Focus. 2013; 35:E18.
9. Kotipatruni RP, Ferraro DJ, Ren X, Vanderwaal RP, Thotala DK, Hallahan DE, Jaboin JJ. NDRG, the N-Myc downstream regulated gene, is important for cell survival, tumor invasion and angiogenesis in meningiomas. Integr Biol (Camb). 2012; 4:1185-97.
10. Zhou RH, Kokame K, Tsukamoto Y, Yutani C, Kato H, Miyata T. Characterization of the human NDRG gene family: a newly identified member, NDRG4, is specifically expressed in brain and heart. Genomics. 2001; 73:86-97.
11. Qu X, Zhai Y, Wei H, Zhang C, Xing G, Yu Y, He F. Characterization and expression of three novel differentiation-related genes belong to the human NDRG gene family. Mol Cell Biochem. 2002; 229:35-44.
12. Hwang J, Kim Y, Kang HB, Jaroszewski L, Deacon AM, Lee H, Choi WC, Kim KJ, Kim CH, Kang BS, Lee JO, Oh TK, Kim JW, Wilson IA, Kim MH. Crystal structure of the human N-Myc downstream-regulated gene 2 protein provides insight into its role as a tumor suppressor. J Biol Chem. 2011; 286:12450-60.
13. Benesh EC, Miller PM, Pfaltzgraff ER, Grega-Larson NE, Hager HA, Sung BH, Qu X, Baldwin HS, Weaver AM, Bader DM. Bves and NDRG4 regulate directional epicardial cell migration through autocrine extracellular matrix deposition. Mol Biol Cell. 2013; 24:3496-510.
14. Shimono A, Okuda T, Kondoh H. N-myc-dependent repression of ndr1, a gene identified by direct subtraction of whole mouse embryo cDNAs between wild type and N-myc mutant. Mech Dev. 1999; 83:39-52.
15. Liu W, Xing F, Iiizumi-Gairani M, Okuda H, Watabe M, Pai SK, Pandey PR, Hirota S, Kobayashi A, Mo YY, Fukuda K, Li Y, Watabe K. N-myc downstream regulated gene 1 modulates Wnt-beta-catenin signalling and pleiotropically suppresses metastasis. EMBO Mol Med. 2012; 4:93-108.
16. Mao Z, Sun J, Feng B, Ma J, Zang L, Dong F, Zhang D, Zheng M. The metastasis suppressor, N-myc downregulated gene 1 (NDRG1), is a prognostic biomarker for human colorectal cancer. PLoS One. 2013; 8:e68206.
17. Choi SC, Kim KD, Kim JT, Kim JW, Yoon DY, Choe YK, Chang YS, Paik SG, Lim JS. Expression and regulation of NDRG2 (N-myc downstream regulated gene 2) during the differentiation of dendritic cells. FEBS Lett. 2003; 553:413-8.
18. Sugiki T, Murakami M, Taketomi Y, Kikuchi-Yanoshita R, Kudo I. N-myc downregulated gene 1 is a phosphorylated protein in mast cells. Biol Pharm Bull. 2004; 27:624-7.
19. Kyuno J, Fukui A, Michiue T, Asashima M. Identification and characterization of Xenopus NDRG1. Biochem Biophys Res Commun. 2003; 309:52-7.
20. Nakada N, Hongo S, Ohki T, Maeda A, Takeda M. Molecular characterization of NDRG4/Bdm1 protein isoforms that are differentially regulated during rat brain development. Brain Res Dev Brain Res. 2002; 135:45-53.
21. Melotte V, Qu X, Ongenaert M, van Criekinge W, de Bruine AP, Baldwin HS, van Engeland M. The N-myc downstream regulated gene (NDRG) family: diverse functions, multiple applications. FASEB J. 2010; 24:4153-66.
22. Ohki T, Hongo S, Nakada N, Maeda A, Takeda M. Inhibition of neurite outgrowth by reduced level of NDRG4 protein in antisense transfected PC12 cells. Brain Res Dev Brain Res. 2002; 135:55-63.
23. Takahashi K, Yamada M, Ohata H, Honda K, Yamada M. Ndrg2 promotes neurite outgrowth of NGF-differentiated PC12 cells. Neurosci Lett. 2005; 388:157-62.
24. Hongo S, Watanabe T, Takahashi K, Miyazaki A. Ndrg4 enhances NGF-induced ERK activation uncoupled with Elk-1 activation. J Cell Biochem. 2006; 98:185-93.
25. Li Y, Xu N, Cai L, Gao Z, Shen L, Zhang Q, Hou W, Zhong H, Wang Q, Xiong L. NDRG2 is a novel p53-associated regulator of apoptosis in C6-originated astrocytes exposed to oxygen-glucose deprivation. PLoS One. 2013; 8:e57130.
26. Liu N, Wang L, Li X, Yang Q, Liu X, Zhang J, Zhang J, Wu Y, Ji S, Zhang Y, Yang A, Han H, Yao L. N-Myc downstream-regulated gene 2 is involved in p53-mediated apoptosis. Nucleic Acids Res. 2008; 36:5335-49.
27. Yamamoto H, Kokame K, Okuda T, Nakajo Y, Yanamoto H, Miyata T. NDRG4 protein-deficient mice exhibit spatial learning deficits and vulnerabilities to cerebral ischemia. J Biol Chem. 2011; 286:26158-65.
28. Melotte V, Lentjes MH, van den Bosch SM, Hellebrekers DM, de Hoon JP, Wouters KA, Daenen KL, Partouns-HendriksI E, Stessels F, Louwagie J, Smits KM, Weijenberg MP, Sanduleanu S, Khalid-de Bakker CA, Oort FA, Meijer GA, Jonkers DM, Herman JG, de Bruine AP, van Engeland M. N-Myc downstream-regulated gene 4 (NDRG4): a candidate tumor suppressor gene and potential biomarker for colorectal cancer. J Natl Cancer Inst. 2009; 101:916-27.
29. Schilling SH, Hjelmeland AB, Radiloff DR, Liu IM, Wakeman TP, Fielhauer JR, Foster EH, Lathia JD, Rich JN, Wang XF, Datto MB. NDRG4 is required for cell cycle progression and survival in glioblastoma cells. J Biol Chem. 2009; 284:25160-9.
30. Merino JJ, Cordero-Campana MI. Molecular bases of the programmed cell death process: implications of tumor suppressor protein p53 and other proteins in the control of cell cycle. Mechanisms of apoptotic action. Review. Invest Clin. 1998; 39:323-58.
31. Laptenko O, Prives C. Transcriptional regulation by p53: one protein, many possibilities. Cell Death Differ. 2006; 13:951-61.
32. Nagashima G, Aoyagi M, Yamamoto M, Yamamoto S, Wakimoto H, Ohno K, Yamamoto K, Hirakawa K. P53 overexpression and proliferative potential in malignant meningiomas. Acta Neurochir (Wien). 1999; 141:53-61. discussion 60-1.
33. Levine AJ. p53, the cellular gatekeeper for growth and division. Cell. 1997; 88:323-31.
34. Chipuk JE, Fisher JC, Dillon CP, Kriwacki RW, Kuwana T, Green DR. Mechanism of apoptosis induction by inhibition of the anti-apoptotic BCL-2 proteins. Proc Natl Acad Sci U S A. 2008; 105:20327-32.
35. Adams JM, Cory S. The Bcl-2 protein family: arbiters of cell survival. Science. 1998; 281:1322-6.
36. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med. 2000; 6:513-9.
37. Malet G, Martin AG, Orzaez M, Vicent MJ, Masip I, Sanclimens G, Ferrer-Montiel A, Mingarro I, Messeguer A, Fearnhead HO, Perez-Paya E. Small molecule inhibitors of Apaf-1-related caspase-3/-9 activation that control mitochondrial-dependent apoptosis. Cell Death Differ. 2006; 13:1523-32.
38. McCaffrey AP, Meuse L, Pham TT, Conklin DS, Hannon GJ, Kay MA. RNA interference in adult mice. Nature. 2002; 418:38-9.
39. Dirven CM, Grill J, Lamfers ML, Van der Valk P, Leonhart AM, Van Beusechem VW, Haisma HJ, Pinedo HM, Curiel DT, Vandertop WP, Gerritsen WR. Gene therapy for meningioma: improved gene delivery with targeted adenoviruses. J Neurosurg. 2002; 97:441-9.
40. Kim JT, Kim JW, Kang YH, Kim KD, Lee SJ, Choi SC, Kim KS, Chae SK, Kim JW, Lim JS, Lee HG. NDRG2 and PRA1 interact and synergistically inhibit T-cell factor/beta-catenin signaling. FEBS Lett. 2012; 586:3962-8.
41. Ding W, Zhang J, Yoon JG, Shi D, Foltz G, Lin B. NDRG4 is downregulated in glioblastoma and inhibits cell proliferation. OMICS: a journal of integrative biology. 2012; 16:263-7.
42. Haga N, Fujita N, Tsuruo T. Tsuruo, Mitochondrial aggregation precedes cytochrome c release from mitochondria during apoptosis. Oncogene. 2003; 22:5579-85.
43. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nunez G, Peter ME, Piacentini M, Rubinsztein DC, Shi Y, Simon HU, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ. 2012; 19:107-20.
44. Murphy AC, Weyhenmeyer B, Schmid J, Kilbride SM, Rehm M, Huber HJ, Senft C, Weissenberger J, Seifert V, Dunst M, Mittelbronn M, Kogel D, Prehn JH, Murphy BM. Activation of executioner caspases is a predictor of progression-free survival in glioblastoma patients: a systems medicine approach. Cell Death Dis. 2013; 4:e629.
45. Porter PL, Gown AM, Kramp SG, Coltrera MD. Widespread p53 overexpression in human malignant tumors. An immunohistochemical study using methacarn-fixed, embedded tissue. Am J Pathol. 1992; 140:145-53.
46. Miyashita T, Krajewski S, Krajewska M, Wang HG, Lin HK, Liebermann DA, Hoffman B, Reed JC. Tumor suppressor p53 is a regulator of bcl-2 and bax gene expression in vitro and in vivo. Oncogene. 1994; 9:1799-805.
47. Yin C, Knudson CM, Korsmeyer SJ, Van Dyke T. Bax suppresses tumorigenesis and stimulates apoptosis in vivo. Nature. 1997; 385:637-40.
48. Findley HW, Gu L, Yeager AM, Zhou M. Expression and regulation of Bcl-2, Bcl-xl, and Bax correlate with p53 status and sensitivity to apoptosis in childhood acute lymphoblastic leukemia. Blood. 1997; 89:2986-93.
49. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell. 2003; 11:577-90.
50. Sasi N, Hwang M, Jaboin J, Csiki I, Lu B. Regulated cell death pathways: new twists in modulation of BCL2 family function. Mol Cancer Ther. 2009; 8:1421-9.
51. Berns K, Hijmans EM, Mullenders J, Brummelkamp TR, Velds A, Heimerikx M, Kerkhoven RM, Madiredjo M, Nijkamp W, Weigelt B, Agami R, Ge W, Cavet G, Linsley PS, Beijersbergen RL, Bernards R. A large-scale RNAi screen in human cells identifies new components of the p53 pathway. Nature. 2004; 428:431-7.
52. Nakasu S, Nakajima M, Nakazawa T, Nakasu Y, Handa J. p53 accumulation and apoptosis in embolized meningiomas. Acta Neuropathol. 1997; 93:599-605.
53. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science. 2004; 303:1010-4.
54. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell. 1995; 80:293-9.
55. Luu Y, Bush J, Cheung KJ Jr, Li G. The p53 stabilizing compound CP-31398 induces apoptosis by activating the intrinsic Bax/mitochondrial/caspase-9 pathway. Exp Cell Res. 2002; Jun 10;276:214-22.
56. Stein S, Thomas EK, Herzog B, Westfall MD, Rocheleau JV, Jackson RS 2nd, Wang M, Liang P. NDRG1 is necessary for p53-dependent apoptosis. J Biol Chem. 2004; 279:48930-40.
57. Stewart SA, Dykxhoorn DM, Palliser D, Mizuno H, Yu EY, An DS, Sabatini DM, Chen IS, Hahn WC, Sharp PA, Weinberg RA, Novina CD. Lentivirus-delivered stable gene silencing by RNAi in primary cells. RNA. 2003; 9:493-501.
58. Baekelandt V, Eggermont K, Michiels M, Nuttin B, Debyser Z. Optimized lentiviral vector production and purification procedure prevents immune response after transduction of mouse brain. Gene Ther. 2003; 10:1933-40.