Axl, a prognostic and therapeutic target in acute myeloid leukemia mediates paracrine crosstalk of leukemia cells with bone marrow stroma

Blood

Volumn 122, Issue 14, 2013, Pages 2443-2452

  Ben Batalla, Isabel ^a,b   Schultze, Alexander ^a,b   Wroblewski, Mark ^a,b   Erdmann, Robert ^a,b   Heuser, Michael ^c   Waizenegger, Jonas S ^a,b   Riecken, Kristoffer ^a   Binder, Mascha ^a   Schewe, Denis ^d   Sawall, Stefanie ^a,b   Witzke, Victoria ^a,b   Cubas Cordova, Miguel ^a,b   Janning, Melanie ^a,b   Wellbrock, Jasmin ^a   Fehse, Boris ^a   Hagel, Christian ^a   Krauter, Jurgen ^c   Ganser, Arnold ^c   Lorens, James B ^e   Fiedler, Walter ^a   Carmeliet, Peter ^f,g   Pantel, Klaus ^b   Bokemeyer, Carsten ^a   Loges, Sonja ^a,b   more..

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b Center of Experimental Medicine   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e UNIVERSITY OF BERGEN   (Norway)

^f DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^g UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH ARREST SPECIFIC PROTEIN 6; PROTEIN AXL; PROTEIN TYROSINE KINASE; SMALL MOLECULE TRANSPORT AGENT; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; AXL RECEPTOR TYROSINE KINASE; GROWTH ARREST-SPECIFIC PROTEIN 6; ONCOPROTEIN; SIGNAL PEPTIDE;

ACUTE MYELOID LEUKEMIA; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW STROMA CELL; CANCER PROGNOSIS; CANCER RESISTANCE; CELL PROLIFERATION; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; LEUKEMIA CELL; MULTICENTER STUDY (TOPIC); NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STEM CELL NICHE; TUMOR CELL; ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL; BONE MARROW CELL; CLINICAL TRIAL (TOPIC); DISEASE MODEL; DRUG SCREENING; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENETICS; KAPLAN MEIER METHOD; MALE; METABOLISM; MOUSE; PHYSIOLOGY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL; WESTERN BLOTTING;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOTTING, WESTERN; BONE MARROW CELLS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; KAPLAN-MEIER ESTIMATE; LEUKEMIA, MYELOID, ACUTE; MALE; MICE; PARACRINE COMMUNICATION; PROGNOSIS; PROTO-ONCOGENE PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR CROSS-TALK; RECEPTOR PROTEIN-TYROSINE KINASES; STROMAL CELLS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84887743438     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-03-491431     Document Type: Article

References (49)

1. Burnett A, Wetzler M, Lowenberg B. Therapeutic advances in acute myeloid leukemia. J Clin Oncol 2011;29(5):487-494.
2. Hafizi S, Dahlback B. Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J. 2006;273(23):5231-5244.
3. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol. 2008;8(5):327-336.
4. Schmidt T, Ben-Batalla I, Schultze A, Loges S. Macrophage-Tumor crosstalk: Role of TAMR tyrosine kinase receptors and of their ligands. Cell Mol Life Sci. 2012;69(9):1391-1414.
5. Zhang QK, Boast S, de los Santos K, Begemann M, Goff SP. Transforming activity of retroviral genomes encoding Gag-Axl fusion proteins. J Virol. 1996;70(11):8089-8097.
6. O'Bryan JP, Frye RA, Cogswell PC, et al. axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol. 1991;11(10): 5016-5031.
7. Sawabu T, Seno H, Kawashima T, et al. Growth arrest-specific gene 6 and Axl signaling enhances gastric cancer cell survival via Akt pathway. Mol Carcinog. 2007;46(2):155-164.
8. Craven RJ, Xu LH, Weiner TM, et al. Receptor tyrosine kinases expressed in metastatic colon cancer. Int J Cancer. 1995;60(6):791-797.
9. Meric F, Lee WP, Sahin A, Zhang H, Kung HJ, Hung MC. Expression profile of tyrosine kinases in breast cancer. Clin Cancer Res. 2002;8(2): 361-367.
10. Sun W, Fujimoto J, Tamaya T. Coexpression of Gas6/Axl in human ovarian cancers. Oncology. 2004;66(6):450-457.
11. Angelillo-Scherrer A, Burnier L, Flores N, et al. Role of Gas6 receptors in platelet signaling during thrombus stabilization and implications for antithrombotic therapy. J Clin Invest. 2005;115(2): 237-246.
12. Angelillo-Scherrer A, de Frutos P, Aparicio C, et al. Deficiency or inhibition of Gas6 causes platelet dysfunction and protects mice against thrombosis. Nat Med. 2001;7(2):215-221.
13. Angelillo-Scherrer A, Burnier L, Lambrechts D, et al. Role of Gas6 in erythropoiesis and anemia in mice. J Clin Invest. 2008;118(2): 583-596.
14. Tjwa M, Bellido-Martin L, Lin Y, et al. Gas6 promotes inflammation by enhancing interactions between endothelial cells, platelets, and leukocytes. Blood. 2008;111(8):4096-4105.
15. Fernandez-Fernandez L, Bellido-Martin L, Garcia de Frutos P. Growth arrest-specific gene 6 (GAS6). An outline of its role in haemostasis and inflammation. Thromb Haemost. 2008;100(4): 604-610.
16. Sainaghi PP, Castello L, Bergamasco L, Galletti M, Bellosta P, Avanzi GC. Gas6 induces proliferation in prostate carcinoma cell lines expressing the Axl receptor. J Cell Physiol. 2005; 204(1):36-44.
17. Bellosta P, Zhang Q, Goff SP, Basilico C. Signaling through the ARK tyrosine kinase receptor protects from apoptosis in the absence of growth stimulation. Oncogene. 1997;15(20): 2387-2397.
18. Loges S, Schmidt T, Tjwa M, et al. Malignant cells fuel tumor growth by educating infiltrating leukocytes to produce the mitogen Gas6. Blood. 2010;115(11):2264-2273.
19. Crosier PS, Freeman SA, Orlic D, Bodine DM, Crosier KE. The Dtk receptor tyrosine kinase, which binds protein S, is expressed during hematopoiesis. Exp Hematol. 1996;24(2): 318-323.
20. Brandao L, Migdall-Wilson J, Eisenman K, Graham DK. TAM receptors in leukemia: Expression, signaling, and therapeutic implications. Crit Rev Oncog. 2011;16(1-2):47-63.
21. Park IK, Mishra A, Chandler J, Whitman SP, Marcucci G, Caligiuri MA. Inhibition of the receptor tyrosine kinase Axl impedes activation of the FLT3 internal tandem duplication in human acute myeloid leukemia: implications for Axl as a potential therapeutic target. Blood. 2013; 121(11):2064-2073.
22. Hong CC, Lay JD, Huang JS, et al. Receptor tyrosine kinase AXL is induced by chemotherapy drugs and overexpression of AXL confers drug resistance in acute myeloid leukemia. Cancer Lett. 2008;268(2):314-324.
23. Rochlitz C, Lohri A, Bacchi M, et al. Axl expression is associated with adverse prognosis and with expression of Bcl-2 and CD34 in de novo acute myeloid leukemia (AML): Results from a multicenter trial of the Swiss Group for Clinical Cancer Research (SAKK). Leukemia. 1999;13(9): 1352-1358.
24. Auclair D, Miller D, Yatsula V, et al. Antitumor activity of sorafenib in FLT3-driven leukemic cells. Leukemia. 2007;21(3):439-445.
25. Pigazzi M, Manara E, Bresolin S, et al. MicroRNA- 34b promoter hypermethylation induces CREB overexpression and contributes to myeloid transformation. Haematologica. 2013;98(4): 602-610.
26. Kroon E, Krosl J, Thorsteinsdottir U, Baban S, Buchberg AM, Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J. 1998;17(13):3714-3725.
27. Schmidt T, Kharabi Masouleh B, Loges S, et al. Loss or inhibition of stromal-derived PlGF prolongs survival of mice with imatinib-resistant Bcr-Abl1(1) leukemia. Cancer Cell. 2011;19(6): 740-753.
28. Ben-Batalla I, Seoane S, Garcia-Caballero T, et al. Deregulation of the Pit-1 transcription factor in human breast cancer cells promotes tumor growth and metastasis. J Clin Invest. 2010; 120(12):4289-4302.
29. Weber K, Bartsch U, Stocking C, Fehse B. A multicolor panel of novel lentiviral "gene ontology" (LeGO) vectors for functional gene analysis. Mol Ther. 2008;16(4):698-706.
30. Johannessen CM, Boehm JS, Kim SY, et al. COT drives resistance to RAF inhibition through MAP kinase pathway reactivation. Nature. 2010; 468(7326):968-972.
31. Wang NS, Unkila MT, Reineks EZ, Distelhorst CW. Transient expression of wild-Type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulum-Targeted Bcl-2 is protective against Baxinduced cell death. J Biol Chem. 2001;276(47): 44117-44128.
32. Weber K, Mock U, Petrowitz B, Bartsch U, Fehse B. Lentiviral gene ontology (LeGO) vectors equipped with novel drug-selectable fluorescent proteins: new building blocks for cell marking and multi-gene analysis. Gene Ther. 2010;17(4): 511-520.
33. Jung M, Sabat R, Kratzschmar J, et al. Expression profiling of IL-10-regulated genes in human monocytes and peripheral blood mononuclear cells from psoriatic patients during IL-10 therapy. Eur J Immunol. 2004;34(2): 481-493.
34. Konopleva M, Konoplev S, Hu W, Zaritskey AY, Afanasiev BV, Andreeff M. Stromal cells prevent apoptosis of AML cells by up-regulation of antiapoptotic proteins. Leukemia. 2002;16(9): 1713-1724.
35. Becker PS. Dependence of acute myeloid leukemia on adhesion within the bone marrow microenvironment. Scientific World Journal. 2012; 2012:856467.
36. Dormady SP, Zhang XM, Basch RS. Hematopoietic progenitor cells grow on 3T3 fibroblast monolayers that overexpress growth arrest-specific gene-6 (GAS6). Proc Natl Acad Sci USA. 2000;97(22):12260-12265.
37. Budagian V, Bulanova E, Orinska Z, et al. Soluble Axl is generated by ADAM10-dependent cleavage and associates with Gas6 in mouse serum [retraction appears in Mol Cell Biol. 2011;31(6) 1330]. Mol Cell Biol. 2005;25(21):9324-9339.
38. Holland SJ, Pan A, Franci C, et al. R428, a selective small molecule inhibitor of Axl kinase, blocks tumor spread and prolongs survival in models of metastatic breast cancer. Cancer Res. 2010;70(4):1544-1554.
39. Li P, Goto H, Kasahara K, et al. P90 RSK arranges Chk1 in the nucleus for monitoring of genomic integrity during cell proliferation. Mol Biol Cell. 2012;23(8):1582-1592.
40. Segal MS, Sautina L, Li S, et al. Relaxin increases human endothelial progenitor cell NO and migration and vasculogenesis in mice. Blood. 2012;119(2):629-636.
41. Rogers LD, Brown NF, Fang Y, Pelech S, Foster LJ. Phosphoproteomic analysis of Salmonellainfected cells identifies key kinase regulators and SopB-dependent host phosphorylation events. Sci Signal. 2011;4(191):rs9.
42. Pang L, Sawada T, Decker SJ, Saltiel AR. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor. J Biol Chem. 1995;270(23): 13585-13588.
43. Gan Y, Shi C, Inge L, Hibner M, Balducci J, Huang Y. Differential roles of ERK and Akt pathways in regulation of EGFR-mediated signaling and motility in prostate cancer cells. Oncogene. 2010; 29(35):4947-4958.
44. Ryan KM, Ernst MK, Rice NR, Vousden KH. Role of NF-kappaB in p53-mediated programmed cell death. Nature. 2000;404(6780):892-897.
45. Wald DN, Vermaat HM, Zang S, et al. Identification of 6-benzylthioinosine as a myeloid leukemia differentiation-inducing compound. Cancer Res. 2008;68(11):4369-4376.
46. Hendzel MJ, Wei Y, Mancini MA, et al. Mitosisspecific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma. 1997;106(6): 348-360.
47. Ghosh AK, Secreto C, Boysen J, et al. The novel receptor tyrosine kinase Axl is constitutively active in B-cell chronic lymphocytic leukemia and acts as a docking site of nonreceptor kinases: implications for therapy. Blood. 2011;117(6): 1928-1937.
48. Shiozawa Y, Pedersen EA, Patel LR, et al. GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia. 2010;12(2):116-127.
49. Shiozawa Y, Pedersen EA, Havens AM, et al. Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest. 2011;121(4):1298-1312.