Tetraspanin family member, CD82, regulates expression of EZH2 via inactivation of p38 MAPK signaling in leukemia cells

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  Nishioka, Chie ^a   Ikezoe, Takayuki ^a   Yang, Jing ^a   Yokoyama, Akihito ^a  

^a KOCHI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD82 ANTIGEN; HISTONE H3; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR EZH2; CD38 ANTIGEN; CD82 PROTEIN, HUMAN; EZH2 PROTEIN, HUMAN; HISTONE; LYSINE; POLYCOMB REPRESSIVE COMPLEX 2; PTEN PROTEIN, HUMAN; SMALL INTERFERING RNA;

ACUTE MYELOBLASTIC LEUKEMIA; ARTICLE; CONTROLLED STUDY; GENETIC REGULATION; HISTONE METHYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PATHOGENESIS; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METHYLATION; PTEN GENE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; UPREGULATION; ACUTE MYELOID LEUKEMIA; BIOLOGICAL MODEL; DNA METHYLATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; MALE; METABOLISM; POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

ANTIGENS, CD34; ANTIGENS, CD38; ANTIGENS, CD82; CELL LINE, TUMOR; DNA METHYLATION; DOWN-REGULATION; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; ENZYME ACTIVATION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, LEUKEMIC; HISTONES; HUMANS; LEUKEMIA, MYELOID, ACUTE; LYSINE; MALE; MAP KINASE SIGNALING SYSTEM; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; POLYCOMB REPRESSIVE COMPLEX 2; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PTEN PHOSPHOHYDROLASE; RNA, SMALL INTERFERING;

EID: 84951570780     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125017     Document Type: Article

References (56)

1. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nature Med. 1997;3:730-737. PMID: 9212098
2. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, etal. Cancer stem cells-perspectives on current status and future directions: AACR Workshop on cancer stem cells. Cancer Res. 2006;66:9339-9344. PMID: 16990346
3. Ishikawa F, Yoshida S, Saito Y, Hijikata A, Kitamura H, Tanaka S, et al. Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol. 2007;25:1315-1321. PMID: 17952057
4. Ikezoe T, Yang J, Nishioka C, Kojima S, Takeuchi A, Phillip Koeffler H, etal. Inhibition of signal transducer and activator of transcription 5 by the inhibitor of janus kinases stimulates dormant human leukemia CD34+/CD38-cells and sensitizes them to antileukemia agents. Int J Cancer. 2011;128:2317-2325. doi: 10.1002/ijc.25806 PMID: 21128225
5. Geest CR, Coffer PJ. MAPK signaling pathways in the regulation of hematopoiesis. J LeukocBiol. 2009;86:237-250. doi: 10.1189/jlb.0209097 PMID: 19498045
6. Wada T, Penninger JM. Mitogen-activated protein kinases in apoptosis regulation. Oncogene. 2004;23:2838-2849. PMID: 15077147
7. Zarubin T, Han J. Activation and signaling of the p38 MAP kinase pathway. Cell Res. 2005;15:11-18. PMID: 15686620
8. Wang Y, Liu L, Zhou D. Inhibition of p38 MAPK attenuates ionizing radiation-induced hematopoietic cell senescence and residual bone marrow injury. Radiat Res. 2011;176:743-752. PMID: 22014293
9. Xiao Y, Zou P, Wang J, Song H, Zou J, Liu L. Lower phosphorylation of p38 MAPK blocks the oxidative stress-induced senescence in myeloid leukemic CD34 (+) CD38 (-) cells. J Huazhong Univ Sci Technolog Med Sci. 2012;32:328-333. doi: 10.1007/s 11596-012-0057-z PMID: 22684553
10. Konuma T, Oguro H, Iwama A. Role of the polycomb group proteins in hematopoietic stem cells. Dev Growth Differ. 2010;52:505-516. doi: 10.1111/j.1440-169X.2010.01191.x PMID: 20646023
11. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev. 2002;16:2893-2905. PMID: 12435631
12. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298:1039-1043. PMID: 12351676
13. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R, etal. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 2010;42:181-185. doi: 10.1038/ng.518 PMID: 20081860
14. Xu F, Li X. The role of histone methyltransferase EZH2 in myelodysplastic syndromes. Expert Rev Hematol. 2012;5:177-185. doi: 10.1586/ehm.12.5 PMID: 22475286
15. Nikoloski G I, Langemeijer SM, Kuiper RP, Knops R, Massop M, Tönnissen ER, etal. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat Genet. 2010;42:665-667. doi: 10.1038/ng.620 PMID: 20601954
16. Jankowska AM, Makishima H, Tiu RV, Szpurka H, Huang Y, Traina F, etal. Mutational spectrum analysis of chronic myelomonocytic leukemia includes genes associated with epigenetic regulation: UTX, EZH2, and DNMT3A. Blood. 2011;118:3932-3941. doi: 10.1182/blood-2010-10-311019 PMID: 21828135
17. Wang X, Dai H, Wang Q, Wang Q, Xu Y, Wang Y, etal. EZH2 mutations are related to low blast percentage in bone marrow and -7/del (7q) in de novo acute myeloid leukemia. PLoS One. 2013;8:e61341. doi: 10.1371/journal.pone.0061341 PMID: 23613835
18. Khan SN, Jankowska AM, Mahfouz R, Dunbar AJ, Sugimoto Y, Hosono N, etal. Multiple mechanisms deregulate EZH2 and histone H3 lysine 27 epigenetic changes in myeloid malignancies. Leukemia. 2013;27:1301-1309. doi: 10.1038/leu.2013.80 PMID: 23486531
19. Nishioka C, Ikezoe T, Yang J, Udaka K, Yokoyama A. Imatinib causes epigenetic alterations of PTEN gene via upregulation of DNA methyltransferases and polycomb group proteins. Blood Cancer J. 2011;1:e48. doi: 10.1038/bcj.2011.33 PMID: 22829096
20. Nishioka C, Ikezoe T, Yang J, Yokoyama A. Long-term exposure of leukemia cells to multi-targeted tyrosine kinase inhibitor induces activations of AKT, ERK and STAT5 signaling via epigenetic silencing of the PTENgene. Leukemia. 2010;24:1631-1640. doi: 10.1038/leu.2010.145 PMID: 20596030
21. Liggett WH Jr, Sidransky D. Role of the p16 tumor suppressor gene in cancer. J Clin Oncol. 1998;16:1197-2064. PMID: 9508208
22. Esteller M, Corn PG, Baylin SB, Herman JG. A gene hypermethylation profile of human cancer. Cancer Res. 2001;61:3225-3229. PMID: 11309270
23. Lind GE, Thorstensen L, Løvig T, Meling GI, Hamelin R. ACpG island hypermethylation profile of primary colorectal carcinomas and colon cancercells lines. Mol Cancer. 2004;3:28. PMID: 15476557
24. Lee S, Hwang KS, Lee HJ, Kim JS, Kang GH. Aberrant CpG island hypermethylation of multiple genes in colorectal neoplasia. Lab Invest. 2004;84:884-893. PMID: 15122305
25. Su YI, Xu H, Xu Y, Yu J, Xian Y, Luo Q. Azacytidine inhibits the proliferation of human promyelocytic leukemia cells (HL60) by demethylation of MGMT, DAPKandp16genes. Hematology. 2012;17:41-46. doi: 10.1179/102453312X13221316477624 PMID: 22549447
26. Nakayama K, Nakayama N, Katagiri H, Miyazaki K. Mechanisms of Ovarian Cancer Metastasis: Biochemical Pathways. Int J Mol Sci. 2012;13:11705-11717. doi: 10.3390/ijms130911705 PMID: 23109879
27. Maecker HT, Todd SC, Levy S. The tetraspanin superfamily: molecular facilitators. FASEB J. 1997;11:428-442. PMID: 9194523
28. Hemler ME. Specific tetraspanin functions. J Cell Biol. 2001;155:1103-1107. PMID: 11756464
29. Stipp CS, Kolesnikova TV, Hemler ME. Functional domains in tetraspanin proteins. Trends Biochem Sci. 2003;28:106-112. PMID: 12575999
30. Nishioka C, Ikezoe T, Furihata M, Yang J, Serada S, Naka T, etal. CD347CD38∼ acute myelogenous leukemia cells aberrantly express CD82 which regulates adhesion and survival of leukemia stem cells. Int J Cancer. 2013;132;2006-2019. doi: 10.1002/ijc.27904 PMID: 23055153
31. Nishioka C, Ikezoe T, Yang J, Nobumoto A, Kataoka S, Tsuda M, et al. CD82 regulates STAT5/IL-10 and supports survival of acute myelogenous leukemia cells. Int J Cancer. 2014;134:55-64. doi: 10. 1002/ijc.28348 PMID: 23797738
32. Matsuo Y, MacLeod RA, Uphoff CC, Drexler HG, Nishizaki C, Katayama Y, et al. Two acute monocytic leukemia (AML-M5a) cell lines (MOLM-13 and MOLM-14) with interclonal phenotypic heterogeneity showing MLL-AF9 fusion resulting from an occult chromosome insertion, ins (11;9) (q23;p22p23). Leukemia. 1997;11:1469-1477. PMID: 9305600
33. Ikezoe T, Tanosaki S, Krug U, Liu B, Cohen P, Taguchi H, etal. Insulin-like growth factor binding protein-3 antagonizes the effects of retinoids in myeloid leukemia cells. Blood. 2004;104:237-242. PMID: 15026318
34. Cakouros D, Isenmann S, Cooper L, Zannettino A, Anderson P, Glackin C, et al. Twist-1 induces Ezh2 recruitment regulating histone methylation along the Ink4A/Arf locus in mesenchymal stem cells. Mol Cell Biol. 2012;32:1433-1441. doi: 10.1128/MCB.06315-11 PMID: 22290439
35. Hua WF, Fu YS, Liao YJ, Xia WJ, Chen YC, Zeng YX, etal. Curcumin induces down-regulation of EZH2 expression through the MAPK pathway in MDA-MB-435 human breast cancer cells. Eur J Pharmacol. 2010;2637:16-21.
36. Ueda K, Yoshimi A, Kagoya Y, Nishikawa S, Marquez VE, Nakagawa M, etal. Inhibition of histone methyltransferase EZH2 depletes leukemia stem cell of mixed lineage leukemia fusion leukemia through upregulation of p16. Cancer Sci. 2014;105:512-519. doi: 10.1111/cas.12386 PMID: 24612037
37. Chen S, Bohrer LR, Rai AN, Pan Y, Gan L, Zhou X, etal. Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nat Cell Biol. 2010;12:1108-1114. doi: 10.1038/ncb2116 PMID: 20935635
38. Tanaka S, Miyagi S, Sashida G, Chiba T, Yuan J, Mochizuki-Kashio M, etal. Ezh2 augments leukemogenicity by reinforcing differentiation blockage in acute myeloid leukemia. Blood. 2012;120:1107-1117. doi: 10.1182/blood-2011-11-394932 PMID: 22677129
39. Di Cristofano A, Pandolfi PP. The multiple roles of PTEN in tumor suppression. Cell. 2000;100:387-390. PMID: 10693755
40. Cheong JW, Eom JI, Maeng HY, Lee ST, Hahn JS, Ko YW, et al. Phosphatase and tensin homologue phosphorylation in the C-terminal regulatory domain is frequently observed in acute myeloid leukaemia and associated with poor clinical outcome. Br J Haematol. 2013;122:454-456.
41. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, etal. Pten dependence distinguishes hematopoietic stem cells from leukemia-initiating cells. Nature. 2006;441:475-482. PMID: 16598206
42. Peng C, Chen Y, Yang Z, Zhang H, Osterby L, Rosmarin AG, etal. PTEN is a tumor suppressor in CML stem cells and BCR-ABL-induced leukemias in mice. Blood. 2010;115:626-635. doi: 10.1182/blood-2009-06-228130 PMID: 19965668
43. Zou J, Zou P, Wang J, Li L, Wang Y, Zhou D, etal. Inhibition of p38 MAPK activity promotes ex vivo expansion of human cord blood hematopoietic stem cells. Ann Hematol. 2012;91:813-823. doi: 10. 1007/s00277-011-1397-7 PMID: 22258328
44. Ito K, Hirao A, Arai F, Takubo K, Matsuoka S, Miyamoto K, etal. Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat Med. 2006;12:446-451. PMID: 16565722
45. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I, et al. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature. 2004;431:997-1002. PMID: 15496926
46. Zhang Y, Herbert BS, Rajashekhar G, Ingram DA, Yoder MC, Clauss M, etal. Premature senescence of highly proliferative endothelial progenitor cells is induced by tumor necrosis factoralpha via the p38 mitogen-activated protein kinase pathway. FASEB J. 2009;23:1358-1365. doi: 10.1096/fj.08-110296 PMID: 19124561
47. Kwong J, Hong L, Liao R, Deng Q, Han J, Sun P. p38 alpha and p38 gamma mediate oncogenic rasinduced senescence through differential mechanisms. J BiolChem. 2009;284:11237-11246. doi: 10. 1074/jbc. M808327200 PMID: 19251701
48. Ohtani N, Yamakoshi K, Takahashi A, Hara E. The p16INK4a-RB pathway: molecular link between cellular senescence and tumor suppression. J Med Invest. 2004;51:146-153. PMID: 15460900
49. Yap DB, Chu J, Berg T, Schapira M, Cheng SW, Moradian A, etal. Somatic mutations at EZH2Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood. 2011;117:2451-2459. doi: 10.1182/blood-2010-11-321208 PMID: 21190999
50. Sahasrabuddhe AA, Chen X, Chung F, Velusamy T, Lim MS, Elenitoba-Johnson KS. Oncogenic Y641 mutations in EZH2 prevent Jak2/p-TrCP-mediated degradation. Oncogene. 2015;34:445-454. doi: 10.1038/onc.2013.571 PMID: 24469040
51. Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM, Richon VM, etal. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci USA. 2010;107:20980-20985. doi: 10. 1073/pnas.1012525107 PMID: 21078963
52. Berg T, Thoene S, Yap D, Wee T, Schoeler N, Rosten P, et al. A transgenic mouse model demonstrating the oncogenic role of mutations in the polycomb-group gene EZH2 in lymphomagenesis. Blood. 2014;123:3914-3924. doi: 10.1182/blood-2012-12-473439 PMID: 24802772
53. Tam WF, Hähnel PS, Schüler A, Lee BH, Okabe R, Zhu N, etal. STAT5 is crucial to maintain leukemic stem cells in acute myeloid leukemias induced by MOZ-TIF2. Cancer Res. 2013;73:373-384. doi: 10. 1158/0008-5472. CAN-12-0255 PMID: 23149921
54. Delgado-Olguín P, Dang LT, He D, Thomas S, Chi L, Sukonnik T, etal. Ezh2-mediated repression of a transcriptional pathway upstream of Mmp9 maintains integrity of the developing vasculature. Development. 2014;141:4610-4617. doi: 10.1242/dev. 112607 PMID: 25359725
55. Duarte S, Shen XD, Fondevila C, Busuttil RW, Coito AJ. Fibronectin-a4p1 Interactions in Hepatic Cold Ischemia and Reperfusion Injury: Regulation of MMP-9and MT1-MMP viathep38 MAPK Pathway. Am J Transplant. 2012;12:2689-2699. doi: 10.1111/j.1600-6143.2012.04161.x PMID: 22812390
56. Jacamo R, Chen Y, Wang Z, Ma W, Zhang M, Spaeth EL, etal. Reciprocal leukemia-stromaVCAM-1/VLA-4-dependent activation of NF-kB mediates chemoresistance. Blood. 2014;123:2691-2702. doi: 10.1182/blood-2013-06-511527 PMID: 24599548