AXL is an essential factor and therapeutic target for metastatic ovarian cancer

Cancer Research

Volumn 70, Issue 19, 2010, Pages 7570-7579

  Rankin, Erinn B ^a   Fuh, Katherine C ^a   Taylor, Tiffany E ^a   Krieg, Adam J ^a   Musser, Margaret ^c   Yuan, Jenny ^a   Wei, Kevin ^a   Kuo, Calvin J ^a   Longacre, Teri A ^b   Giaccia, Amato J ^a  

^a STANFORD UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX METALLOPROTEINASE; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE AXL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER STAGING; CARCINOGENESIS; DRUG TARGETING; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; OVARY CANCER; OVARY METASTASIS; PRIORITY JOURNAL; TUMOR XENOGRAFT;

ADENOVIRIDAE; ANIMALS; CELL LINE, TUMOR; FEMALE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, NUDE; NEOPLASM METASTASIS; OVARIAN NEOPLASMS; PLASMIDS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 77957375963     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-10-1267     Document Type: Article

References (46)

1. Naora H, Montell DJ. Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat Rev Cancer 2005;5:355-66.
2. Tan DS, Agarwal R, Kaye SB. Mechanisms of transcoelomic metastasis in ovarian cancer. Lancet Oncol 2006;7:925-34.
3. Shan W, Liu J. Inflammation: a hidden path to breaking the spell of ovarian cancer. Cell Cycle 2009;8:3107-11.
4. Kim MY, Oskarsson T, Acharyya S, et al. Tumor self-seeding by circulating cancer cells. Cell 2009;139:1315-26.
5. Sahai E. Illuminating the metastatic process. Nat Rev Cancer 2007;7: 737-49.
6. Bonome T, Lee JY, Park DC, et al. Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary. Cancer Res 2005;65:10602-12.
7. Lancaster JM, Dressman HK, Clarke JP, et al. Identification of genes associated with ovarian cancer metastasis using microarray expression analysis. Int J Gynecol Cancer 2006;16:1733-45.
8. Liu AX, Testa JR, Hamilton TC, Jove R, Nicosia SV, Cheng JQ. AKT2, a member of the protein kinase B family, is activated by growth factors, v-Ha-ras, and v-src through phosphatidylinositol 3-kinase in human ovarian epithelial cancer cells. Cancer Res 1998;58:2973-7.
9. 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;11:5016-31.
10. Nagata K, Ohashi K, Nakano T, et al. Identification of the product of growth arrest-specific gene 6 as a common ligand for Axl, Sky, and Mer receptor tyrosine kinases. J Biol Chem 1996;271:30022-7.
11. Linger RM, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008;100:35-83.
12. Zhang YX, Knyazev PG, Cheburkin YV, et al. AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res 2008;68:1905-15.
13. Shieh YS, Lai CY, Kao YR, et al. Expression of axl in lung adenocarcinoma and correlation with tumor progression. Neoplasia 2005;7: 1058-64.
14. Tai KY, Shieh YS, Lee CS, Shiah SG, Wu CW. Axl promotes cell invasion by inducing MMP-9 activity through activation of NF-κB and Brg-1. Oncogene 2008;27:4044-55.
15. Vajkoczy P, Knyazev P, Kunkel A, et al. Dominant-negative inhibition of the Axl receptor tyrosine kinase suppresses brain tumor cell growth and invasion and prolongs survival. Proc Natl Acad Sci U S A 2006;103:5799-804.
16. Koorstra JB, Karikari CA, Feldmann G, et al. The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target. Cancer Biol Ther 2009;8:618-26.
17. Li Y, Ye X, Tan C, et al. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009;28:3442-55.
18. Gjerdrum C, Tiron C, Hoiby T, et al. Axl is an essential epithelial-to- mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci U S A 107: 1124-9.
19. 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 70:1544-54.
20. Holland SJ, Powell MJ, Franci C, et al. Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 2005;65: 9294-303.
21. Kuo CJ, Farnebo F, Yu EY, et al. Comparative evaluation of the antitumor activity of antiangiogenic proteins delivered by gene transfer. Proc Natl Acad Sci U S A 2001;98:4605-10.
22. Feeley KM, Wells M. Precursor lesions of ovarian epithelial malignancy. Histopathology 2001;38:87-95.
23. Kurman RJ, Shih Ie M. The origin and pathogenesis of epithelial ovarian cancer: a proposed unifying theory. Am J Surg Pathol 2010; 34:433-43.
24. Yoneda J, Kuniyasu H, Crispens MA, Price JE, Bucana CD, Fidler IJ. Expression of angiogenesis-related genes and progression of human ovarian carcinomas in nude mice. J Natl Cancer Inst 1998;90:447-54.
25. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002;2:161-74.
26. Nielsen-Preiss SM, Allen MP, Xu M, et al. Adhesion-related kinase induction of migration requires phosphatidylinositol-3-kinase and ras stimulation of rac activity in immortalized gonadotropin-releasing hormone neuronal cells. Endocrinology 2007;148:2806-14.
27. Choi JH, Choi KC, Auersperg N, Leung PC. Gonadotropins activate proteolysis and increase invasion through protein kinase A and phosphatidylinositol 3-kinase pathways in human epithelial ovarian cancer cells. Cancer Res 2006;66:3912-20.
28. Sasaki T, Knyazev PG, Cheburkin Y, et al. Crystal structure of a C-terminal fragment of growth arrest-specific protein Gas6. Receptor tyrosine kinase activation by laminin G-like domains. J Biol Chem 2002;277:44164-70.
29. Budagian V, Bulanova E, Orinska Z, et al. Soluble Axl is generated by ADAM10-dependent cleavage and associates with Gas6 in mouse serum. Mol Cell Biol 2005;25:9324-39.
30. Kuhnert F, Tam BY, Sennino B, et al. Soluble receptor-mediated selective inhibition of VEGFR and PDGFRβ signaling during physiologic and tumor angiogenesis. Proc Natl Acad Sci U S A 2008;105: 10185-90.
31. Mills GB, Lu Y, Fang X, et al. The role of genetic abnormalities of PTEN and the phosphatidylinositol 3-kinase pathway in breast and ovarian tumorigenesis, prognosis, and therapy. Semin Oncol 2001; 28:125-41.
32. Yuan ZQ, Sun M, Feldman RI, et al. Frequent activation of AKT2 and induction of apoptosis by inhibition of phosphoinositide-3-OH kinase/Akt pathway in human ovarian cancer. Oncogene 2000;19: 2324-30.
33. Guo RX, Qiao YH, Zhou Y, Li LX, Shi HR, Chen KS. Increased staining for phosphorylated AKT and nuclear factor-κB p65 and their relationship with prognosis in epithelial ovarian cancer. Pathol Int 2008;58:749-56.
34. Marone R, Cmiljanovic V, Giese B, Wymann MP. Targeting phosphoinositide 3-kinase: moving towards therapy. Biochim Biophys Acta 2008;1784:159-85.
35. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295: 2387-92.
36. Fridell YW, Villa J, Jr., Attar EC, Liu ET. GAS6 induces Axl-mediated chemotaxis of vascular smooth muscle cells. J Biol Chem 1998;273: 7123-6.
37. Caraux A, Lu Q, Fernandez N, et al. Natural killer cell differentiation driven by Tyro3 receptor tyrosine kinases. Nat Immunol 2006;7: 747-54.
38. Prieto AL, Weber JL, Lai C. Expression of the receptor proteintyrosine kinases Tyro-3, Axl, and mer in the developing rat central nervous system. J Comp Neurol 2000;425:295-314.
39. Sharif MN, Sosic D, Rothlin CV, et al. Twist mediates suppression of inflammation by type I IFNs and Axl. J Exp Med 2006;203:1891-901.
40. Lu Q, Lemke G. Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 2001;293: 306-11.
41. Lu Q, Gore M, Zhang Q, et al. Tyro-3 family receptors are essential regulators of mammalian spermatogenesis. Nature 1999;398:723-8.
42. 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;7:215-21.
43. Angelillo-Scherrer A, Burnier L, Lambrechts D, et al. Role of Gas6 in erythropoiesis and anemia in mice. J Clin Invest 2008;118: 583-96.
44. Dupont J, Aghajanian C, Sabbatini P, Spriggs DR. New agents for the treatment of ovarian cancer: the next generation. Int J Gynecol Cancer 2005;15 Suppl 3:252-7.
45. Lay JD, Hong CC, Huang JS, et al. Sulfasalazine suppresses drug resistance and invasiveness of lung adenocarcinoma cells expressing AXL. Cancer Res 2007;67:3878-87.
46. 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: 314-24.