Galectin-3 mediates bone marrow microenvironment-induced drug resistance in acute leukemia cells via Wnt/β-catenin signaling pathway

Journal of Hematology and Oncology

Volumn 8, Issue 1, 2015, Pages

  Hu, Kaimin ^a,b   Gu, Yanjun ^a   Lou, Lixia ^a   Liu, Lizhen ^a   Hu, Yongxian ^a   Wang, Binsheng ^a   Luo, Yi ^a   Shi, Jimin ^a   Yu, Xiaohong ^a   Huang, He ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Acute leukemia; Bone marrow mesenchymal stromal cell (BM MSC); Drug resistance; Galectin 3; catenin

Indexed keywords

BETA CATENIN; GALECTIN 3; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; SHORT HAIRPIN RNA; WNT PROTEIN; SMALL INTERFERING RNA;

ACUTE LEUKEMIA; APOPTOSIS; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKEMIA CELL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UPREGULATION; COCULTURE; DRUG RESISTANCE; LEUKEMIA; MESENCHYMAL STROMA CELL; METABOLISM; PATHOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; TUMOR MICROENVIRONMENT; WESTERN BLOTTING; WNT SIGNALING PATHWAY;

APOPTOSIS; BLOTTING, WESTERN; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DRUG RESISTANCE, NEOPLASM; GALECTIN 3; HUMANS; LEUKEMIA; MESENCHYMAL STROMAL CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; TRANSFECTION; TUMOR MICROENVIRONMENT; UP-REGULATION; WNT SIGNALING PATHWAY;

EID: 84924066022     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/s13045-014-0099-8     Document Type: Article

References (48)

1. Pui CH, Evans WE. Treatment of acute lymphoblastic leukemia. N Engl J Med. 2006;354(2):166-78.
2. Zhao Y, Huang H, Wei G. Novel agents and biomarkers for acute lymphoid leukemia. J Hematol Oncol. 2013;6:40.
3. Patel JP, Gonen M, Figueroa ME, Fernandez H, Sun Z, Racevskis J, et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med. 2012;366(12):1079-89.
4. Estey EH. Acute myeloid leukemia: 2013 update on risk-stratification and management. Am J Hematol. 2013;88(4):318-27.
5. Kern W, Danhauser-Riedl S, Ratei R, Schnittger S, Schoch C, Kolb HJ, et al. Detection of minimal residual disease in unselected patients with acute myeloid leukemia using multiparameter flow cytometry for definition of leukemia-associated immunophenotypes and determination of their frequencies in normal bone marrow. Haematologica. 2003;88(6):646-53.
6. Ladetto M, Bruggemann M, Monitillo L, Ferrero S, Pepin F, Drandi D, et al. Next-generation sequencing and real-time quantitative PCR for minimal residual disease detection in B-cell disorders. Leukemia. 2014;28(6):1299-307.
7. Nagafuji K, Miyamoto T, Eto T, Kamimura T, Taniguchi S, Okamura T, et al. Monitoring of minimal residual disease (MRD) is useful to predict prognosis of adult patients with Ph-negative ALL: results of a prospective study (ALL MRD2002 Study). J Hematol Oncol. 2013;6:14.
8. Azizidoost S, Babashah S, Rahim F, Shahjahani M, Saki N. Bone marrow neoplastic niche in leukemia. Hematology. 2014;19(4):232-8.
9. Malfuson JV, Boutin L, Clay D, Thepenier C, Desterke C, Torossian F, et al. SP/drug efflux functionality of hematopoietic progenitors is controlled by mesenchymal niche through VLA-4/CD44 axis. Leukemia. 2014;28(4):853-64.
10. Burger JA, Kipps TJ. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood. 2006;107(5):1761-7.
11. Nwabo Kamdje AH, Mosna F, Bifari F, Lisi V, Bassi G, Malpeli G, et al. Notch-3 and Notch-4 signaling rescue from apoptosis human B-ALL cells in contact with human bone marrow-derived mesenchymal stromal cells. Blood. 2011;118(2):380-9.
12. Sun Z, Wang S, Zhao RC. The roles of mesenchymal stem cells in tumor inflammatory microenvironment. J Hematol Oncol. 2014;7:14.
13. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143-7.
14. Dumic J, Dabelic S, Flogel M. Galectin-3: an open-ended story. Biochim Biophys Acta. 2006;1760(4):616-35.
15. Newlaczyl AU, Yu LG. Galectin-3-A jack-of-all-trades in cancer. Cancer Lett. 2011;313(2):123-8.
16. Yamamoto-Sugitani M, Kuroda J, Ashihara E, Nagoshi H, Kobayashi T, Matsumoto Y, et al. Galectin-3 (Gal-3) induced by leukemia microenvironment promotes drug resistance and bone marrow lodgment in chronic myelogenous leukemia. Proc Natl Acad Sci U S A. 2011;108(42):17468-73.
17. Fei F, Abdel-Azim H, Lim M, Arutyunyan A, von Itzstein M, Groffen J, et al. Galectin-3 in pre-B acute lymphoblastic leukemia. Leukemia. 2013;27(12):2385-8.
18. Cheng CL, Hou HA, Lee MC, Liu CY, Jhuang JY, Lai YJ, et al. Higher bone marrow LGALS3 expression is an independent unfavorable prognostic factor for overall survival in patients with acute myeloid leukemia. Blood. 2013;121(16):3172-80.
19. Song S, Mazurek N, Liu C, Sun Y, Ding QQ, Liu K, et al. Galectin-3 mediates nuclear beta-catenin accumulation and Wnt signaling in human colon cancer cells by regulation of glycogen synthase kinase-3beta activity. Cancer Res. 2009;69(4):1343-9.
20. Kobayashi T, Shimura T, Yajima T, Kubo N, Araki K, Tsutsumi S, et al. Transient gene silencing of galectin-3 suppresses pancreatic cancer cell migration and invasion through degradation of beta-catenin. Int J Cancer. 2011;129(12):2775-86.
21. Ge X, Wang X. Role of Wnt canonical pathway in hematological malignancies. J Hematol Oncol. 2010;3:33.
22. Staal F. Wnt Signaling Strength Regulates Normal Hematopoiesis and Its Deregulation Is Involved in Leukemia Development. Exp Hematol. 2012;40(8):S41-1.
23. Luis TC, Ichii M, Brugman MH, Kincade P, Staal FJT. Wnt signaling strength regulates normal hematopoiesis and its deregulation is involved in leukemia development. Leukemia. 2012;26(3):414-21.
24. Yang Y, Mallampati S, Sun BH, Zhang J, Kim SB, Lee JS, et al. Wnt pathway contributes to the protection by bone marrow stromal cells of acute lymphoblastic leukemia cells and is a potential therapeutic target. Cancer Lett. 2013;333(1):9-17.
25. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, et al. Identification of c-MYC as a target of the APC pathway. Science. 1998;281 (5382):1509-12.
26. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, et al. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A. 1999;96(10):5522-7.
27. Minke KS, Staib P, Puetter A, Gehrke I, Gandhirajan RK, Schlosser A, et al. Small molecule inhibitors of WNT signaling effectively induce apoptosis in acute myeloid leukemia cells. Eur J Haematol. 2009;82(3):165-75.
28. Koh TJ, Bulitta CJ, Fleming JV, Dockray GJ, Varro A, Wang TC. Gastrin is a target of the beta-catenin/TCF-4 growth-signaling pathway in a model of intestinal polyposis. J Clin Investig. 2000;106(4):533-9.
29. Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJH, Rubinfeld B, Polakis P, et al. The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene. 1999;18(18):2883-91.
30. Araki Y, Okamura S, Hussain SP, Nagashima M, He PJ, Shiseki M, et al. Regulation of cyclooxygenase-2 expression by the Wnt and ras pathways. Cancer Res. 2003;63(3):728-34.
31. Lin HM, Pestell RG, Raz A, Kim HRC. Galectin-3 enhances cyclin D-1 promoter activity through SP1 and a cAMP-responsive element in human breast epithelial cells. Oncogene. 2002;21(52):8001-10.
32. Wang YZ, Krivtsov AV, Sinha AU, North TE, Goessling W, Feng ZH, et al. The Wnt/beta-Catenin Pathway Is Required for the Development of Leukemia Stem Cells in AML. Science. 2010;327(5973):1650-3.
33. Morgan RG, Ridsdale J, Tonks A, Darley RL. Factors affecting the nuclear localization of beta-catenin in normal and malignant tissue. J Cell Biochem. 2014;115(8):1351-61.
34. Yamaguchi K, Lee SH, Eling TE, Baek SJ. Identification of nonsteroidal anti-inflammatory drug-activated gene (NAG-1) as a novel downstream target of phosphatidylinositol 3-kinase/AKT/GSK-3beta pathway. J Biol Chem. 2004;279(48):49617-23.
35. Somervaille TC, Linch DC, Khwaja A. Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax. Blood. 2001;98(5):1374-81.
36. Liu J, Han G, Liu H, Qin C. Suppression of cholangiocarcinoma cell growth by human umbilical cord mesenchymal stem cells: a possible role of Wnt and Akt signaling. PLoS One. 2013;8(4):e62844.
37. Chauhan D, Li G, Podar K, Hideshima T, Neri P, He D, et al. A novel carbohydrate-based therapeutic GCS-100 overcomes bortezomib resistance and enhances dexamethasone-induced apoptosis in multiple myeloma cells. Cancer Res. 2005;65(18):8350-8.
38. Streetly MJ, Maharaj L, Joel S, Schey SA, Gribben JG, Cotter FE. GCS-100, a novel galectin-3 antagonist, modulates MCL-1, NOXA, and cell cycle to induce myeloma cell death. Blood. 2010;115(19):3939-48.
39. O'Brien S, Kay NE. Maintenance therapy for B-chronic lymphocytic leukemia. Clin Adv Hematol Oncol. 2011;9(1):22-31.
40. Clark MC, Pang M, Hsu DK, Liu FT, de Vos S, Gascoyne RD, et al. Galectin-3 binds to CD45 on diffuse large B-cell lymphoma cells to regulate susceptibility to cell death. Blood. 2012;120(23):4635-44.
41. Liu GY, Xu Y, Li Y, Wang LH, Liu YJ, Zhu D. Secreted galectin-3 as a possible biomarker for the immunomodulatory potential of human umbilical cord mesenchymal stromal cells. Cytotherapy. 2013;15(10):1208-17.
42. Gutierrez SE, Romero-Oliva FA. Epigenetic changes: a common theme in acute myelogenous leukemogenesis. J Hematol Oncol. 2013;6:57.
43. Ramasamy S, Duraisamy S, Barbashov S, Kawano T, Kharbanda S, Kufe D. The MUC1 and galectin-3 oncoproteins function in a microRNA-dependent regulatory loop. Mol Cell. 2007;27(6):992-1004.
44. Rosenfeld C, Goutner A, Venuat AM, Choquet C, Pico JL, Dore JF, et al. An effect human leukaemic cell line: Reh. Eur J Cancer. 1977;13(4-5):377-9.
45. Clark SS, McLaughlin J, Timmons M, Pendergast AM, Ben-Neriah Y, Dow LW, et al. Expression of a distinctive BCR-ABL oncogene in Ph1-positive acute lymphocytic leukemia (ALL). Science. 1988;239(4841 Pt 1):775-7.
46. Gillis S, Watson J. Biochemical and biological characterization of lymphocyte regulatory molecules. V. Identification of an interleukin 2-producing human leukemia T cell line. J Exp Med. 1980;152(6):1709-19.
47. Asou H, Tashiro S, Hamamoto K, Otsuji A, Kita K, Kamada N. Establishment of a human acute myeloid leukemia cell line (Kasumi-1) with 8;21 chromosome translocation. Blood. 1991;77(9):2031-6.
48. Zhao YM, Li JY, Lan JP, Lai XY, Luo Y, Sun J, et al. Cell cycle dependent telomere regulation by telomerase in human bone marrow mesenchymal stem cells. Biochem Biophys Res Commun. 2008;369(4):1114-9.