AML1-ETO mediates hematopoietic self-renewal and leukemogenesis through a COX/β-catenin signaling pathway

Blood

Volumn 121, Issue 24, 2013, Pages 4906-4916

  Zhang, Yiyun ^a,b   Wang, Jianfeng ^a,b   Wheat, Justin ^a   Chen, Xi ^a   Jin, Shan ^a,b   Sadrzadeh, Hossein ^c   Fathi, Amir T ^b,c   Peterson, Randall T ^a,b,d   Kung, Andrew L ^d,e   Sweetser, David A ^a,b   Yeh, Jing Ruey Joanna ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AML1 ETO PROTEIN; BETA CATENIN; CYCLOOXYGENASE 2; HYBRID PROTEIN; NIMESULIDE; ONCOPROTEIN; UNCLASSIFIED DRUG; AML1 ETO FUSION PROTEIN, HUMAN; AML1-ETO FUSION PROTEIN, HUMAN; PROSTAGLANDIN SYNTHASE INHIBITOR; PTGS2 PROTEIN, HUMAN; PTGS2 PROTEIN, MOUSE; SULFONAMIDE; TRANSCRIPTION FACTOR RUNX1;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL GROWTH; CELL RENEWAL; CLONOGENESIS; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME INDUCTION; ENZYME INHIBITION; GENE ACTIVATION; GENE SILENCING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VIVO STUDY; LEUKEMIA; LEUKEMIA CELL; LEUKEMOGENESIS; MOUSE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL; BIOSYNTHESIS; CANCER STEM CELL; CANCER TRANSPLANTATION; CELL PROLIFERATION; CELL STRAIN K 562; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE; XENOGRAFT; ZEBRA FISH;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, LEUKEMIC; HEMATOPOIETIC STEM CELLS; HUMANS; K562 CELLS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; ONCOGENE PROTEINS, FUSION; SIGNAL TRANSDUCTION; SULFONAMIDES; TRANSPLANTATION, HETEROLOGOUS; ZEBRAFISH;

MLCS; MLOWN;

EID: 84881294677     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-08-447763     Document Type: Article

References (50)

1. Redaelli A, Botteman MF, Stephens JM, Brandt S, Pashos CL. Economic burden of acute myeloid leukemia: a literature review. Cancer Treat Rev. 2004;30(3):237-247. (Pubitemid 38477269)
2. Guan Y, Gerhard B, Hogge DE. Detection, isolation, and stimulation of quiescent primitive leukemic progenitor cells from patients with acute myeloid leukemia (AML). Blood. 2003;101(8):3142-3149. (Pubitemid 36858008)
3. Terpstra W, Ploemacher RE, Prins A, et al. Fluorouracil selectively spares acute myeloid leukemia cells with long-term growth abilities in immunodeficient mice and in culture. Blood. 1996;88(6):1944-1950. (Pubitemid 26307894)
4. Mulloy JC, Cammenga J, Berguido FJ, et al. Maintaining the self-renewal and differentiation potential of human CD34+ hematopoietic cells using a single genetic element. Blood. 2003;102(13):4369-4376. (Pubitemid 37494097)
5. Peterson LF, Zhang DE. The 8;21 translocation in leukemogenesis. Oncogene. 2004;23(24):4255-4262. (Pubitemid 38758592)
6. Link KA, Chou FS, Mulloy JC. Core binding factor at the crossroads: determining the fate of the HSC. J Cell Physiol. 2010;222(1):50-56.
7. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci USA. 2000;97(13):7521-7526. (Pubitemid 30431496)
8. Higuchi M, O'Brien D, Kumaravelu P, Lenny N, Yeoh EJ, Downing JR. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell. 2002;1(1):63-74. (Pubitemid 41039177)
9. Okuda T, Cai Z, Yang S, et al. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood. 1998;91(9):3134-3143. (Pubitemid 28193861)
10. Helenius IT, Yeh JR. Small zebrafish in a big chemical pond. J Cell Biochem. 2012;113(7):2208-2216.
11. Yeh JR, Munson KM, Chao YL, Peterson QP, Macrae CA, Peterson RT. AML1-ETO reprograms hematopoietic cell fate by downregulating scl expression. Development. 2008;135(2):401-410. (Pubitemid 351228431)
12. Yeh JR, Munson KM, Elagib KE, Goldfarb AN, Sweetser DA, Peterson RT. Discovering chemical modifiers of oncogene-regulated hematopoietic differentiation. Nat Chem Biol. 2009;5(4):236-243.
13. Williams CS, Mann M, DuBois RN. The role of cyclooxygenases in inflammation, cancer, and development. Oncogene. 1999;18(55):7908-7916. (Pubitemid 30066236)
14. Goessling W, North TE, Loewer S, et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell. 2009;136(6):1136-1147.
15. Reya T, Duncan AW, Ailles L, et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature. 2003;423(6938):409-414. (Pubitemid 36626987)
16. Chou FS, Griesinger A, Wunderlich M, et al. The thrombopoietin/MPL/Bcl-xL pathway is essential for survival and self-renewal in human preleukemia induced by AML1-ETO. Blood. 2012;120(4):709-719.
17. North TE, Goessling W, Walkley CR, et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature. 2007;447(7147):1007- 1011. (Pubitemid 46975751)
18. Müller-Tidow C, Steffen B, Cauvet T, et al. Translocation products in acute myeloid leukemia activate the Wnt signaling pathway in hematopoietic cells. Mol Cell Biol. 2004;24(7):2890-2904. (Pubitemid 38381278)
19. Kim PJ, Plescia J, Clevers H, Fearon ER, Altieri DC. Survivin and molecular pathogenesis of colorectal cancer. Lancet. 2003;362(9379):205-209. (Pubitemid 36859937)
20. Balkhi MY, Christopeit M, Chen Y, Geletu M, Behre G. AML1/ETO-induced survivin expression inhibits transcriptional regulation of myeloid differentiation. Exp Hematol. 2008;36(11):1449-1460.
21. Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F. Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol. 2002;22(4):1172-1183. (Pubitemid 34094853)
22. Leung JY, Kolligs FT, Wu R, et al. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J Biol Chem. 2002;277(24):21657-21665. (Pubitemid 34952316)
23. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 1999;398(6726):422-426. (Pubitemid 29180374)
24. Jung HC, Kim K. Identification of MYCBP as a beta-catenin/LEF-1 target using DNA microarray analysis. Life Sci. 2005;77(11):1249-1262. (Pubitemid 40898323)
25. Boon EM, van der Neut R, van de Wetering M, Clevers H, Pals ST. Wnt signaling regulates expression of the receptor tyrosine kinase met in colorectal cancer. Cancer Res. 2002;62(18):5126-5128. (Pubitemid 35024579)
26. Roose J, Huls G, van Beest M, et al. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science. 1999;285(5435):1923-1926.
27. Longo KA, Kennell JA, Ochocinska MJ, Ross SE, Wright WS, MacDougald OA. Wnt signaling protects 3T3-L1 preadipocytes from apoptosis through induction of insulin-like growth factors. J Biol Chem. 2002;277(41):38239-38244. (Pubitemid 35154678)
28. Matozaki S, Nakagawa T, Kawaguchi R, et al. Establishment of a myeloid leukaemic cell line (SKNO-1) from a patient with t(8;21) who acquired monosomy 17 during disease progression. Br J Haematol. 1995;89(4):805-811.
29. Brault V, Moore R, Kutsch S, et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development. 2001;128(8):1253-1264. (Pubitemid 32409648)
30. Gibson T, Zaphiropoulos G, Grove J, Widdop B, Berry D. Kinetics of salicylate metabolism. Br J Clin Pharmacol. 1975;2(3):233-238.
31. Sitar DS, Owen JA, MacDougall B, Hunter T, Mitenko PA. Effects of age and disease on the pharmacokinetics and pharmacodynamics of sulindac. Clin Pharmacol Ther. 1985;38(2):228-234. (Pubitemid 16248177)
32. Krejci O, Wunderlich M, Geiger H, et al. p53 signaling in response to increased DNA damage sensitizes AML1-ETO cells to stress-induced death. Blood. 2008;111(4):2190-2199. (Pubitemid 351451533)
33. Ysebaert L, Chicanne G, Demur C, et al. Expression of beta-catenin by acute myeloid leukemia cells predicts enhanced clonogenic capacities and poor prognosis. Leukemia. 2006;20(7):1211-1216. (Pubitemid 43905823)
34. Heidel FH, Bullinger L, Feng Z, et al. Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell. 2012;10(4):412-424.
35. Zhao C, Blum J, Chen A, et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell. 2007;12(6):528-541. (Pubitemid 350199070)
36. Wang Y, Krivtsov AV, Sinha AU, et al. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science. 2010;327(5973):1650-1653.
37. Steinert G, Oancea C, Roos J, Hagemeyer H, Maier T, Ruthardt M, Puccetti E. Sulindac sulfide reverses aberrant self-renewal of progenitor cells induced by the AML-associated fusion proteins PML/RARα and PLZF/RARα. PLoS ONE. 2011;6(7):e22540.
38. Han JS, Crowe DL. Tumor initiating cancer stem cells from human breast cancer cell lines. Int J Oncol. 2009;34(5):1449-1453.
39. Magnifico A, Albano L, Campaner S, et al. Tumor-initiating cells of HER2-positive carcinoma cell lines express the highest oncoprotein levels and are sensitive to trastuzumab. Clin Cancer Res. 2009;15(6):2010-2021.
40. Cobas M, Wilson A, Ernst B, Mancini SJ, MacDonald HR, Kemler R, Radtke F. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med. 2004;199(2):221-229.
41. Jeannet G, Scheller M, Scarpellino L, et al. Long-term, multilineage hematopoiesis occurs in the combined absence of beta-catenin and gamma-catenin. Blood. 2008;111(1):142-149.
42. Ross JA, Blair CK, Cerhan JR, et al. Nonsteroidal anti-inflammatory drug and acetaminophen use and risk of adult myeloid leukemia. Cancer Epidemiol Biomarkers Prev. 2011;20(8): 1741-1750.
43. Kasum CM, Blair CK, Folsom AR, Ross JA. Nonsteroidal anti-inflammatory drug use and risk of adult leukemia. Cancer Epidemiol Biomarkers Prev. 2003;12(6):534-537. (Pubitemid 36713648)
44. Pogoda JM, Katz J, McKean-Cowdin R, Nichols PW, Ross RK, Preston-Martin S. Prescription drug use and risk of acute myeloid leukemia by French-American-British subtype: results from a Los Angeles County case-control study. Int J Cancer. 2005;114(4):634-638. (Pubitemid 40349623)
45. Tuynman JB, Vermeulen L, Boon EM, Kemper K, Zwinderman AH, Peppelenbosch MP, Richel DJ. Cyclooxygenase-2 inhibition inhibits c-Met kinase activity and Wnt activity in colon cancer. Cancer Res. 2008;68(4):1213-1220. (Pubitemid 351272241)
46. Wu JQ, Seay M, Schulz VP, et al. Tcf7 is an important regulator of the switch of self-renewal and differentiation in a multipotential hematopoietic cell line. PLoS Genet. 2012;8(3):e1002565.
47. Piacibello W, Sanavio F, Garetto L, Severino A, Dané A, Gammaitoni L, Aglietta M. Differential growth factor requirement of primitive cord blood hematopoietic stem cell for self-renewal and amplification vs proliferation and differentiation. Leukemia. 1998;12(5):718-727. (Pubitemid 28220825)
48. Arber N, Eagle CJ, Spicak J, et al; PreSAP Trial Investigators. Celecoxib for the prevention of colorectal adenomatous polyps. N Engl J Med. 2006;355(9):885-895. (Pubitemid 44315981)
49. Bertagnolli MM, Eagle CJ, Zauber AG, et al; APC Study Investigators. Celecoxib for the prevention of sporadic colorectal adenomas. N Engl J Med. 2006;355(9):873-884. (Pubitemid 44315980)
50. Vanhoutte PM. COX-1 and vascular disease. Clin Pharmacol Ther. 2009;86(2):212-215.