The receptor tyrosine kinase Axl is an essential regulator of prostate cancer proliferation and tumor growth and represents a new therapeutic target

Oncogene

Volumn 32, Issue 6, 2013, Pages 689-698

  Paccez, J D ^a,b   Vasques, G J ^a   Correa, R G ^c   Vasconcellos, J F ^d   Duncan, K ^a   Gu, X ^d   Bhasin, M ^d   Libermann, T A ^d   Zerbini, L F ^a,b  

^a International Center for Genetic Engineering and Biotechnology   (South Africa)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c BURNHAM INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Axl; IL 6; NF B; proliferation; prostate cancer; tyrosine kinase receptor

Indexed keywords

6 AMINO 4 (4 PHENOXYPHENYLETHYLAMINO)QUINAZOLINE; I KAPPA B ALPHA; I KAPPA B KINASE ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; ISOHELENIN; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; RECEPTOR TYROSINE KINASE AX1; SC 514; SMALL INTERFERING RNA; SOMATOMEDIN C; STAT3 PROTEIN; UNCLASSIFIED DRUG; WEDELOLACTONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DRUG TARGETING; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN STABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MOLECULAR TARGETED THERAPY; NEOPLASM METASTASIS; NF-KAPPA B; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84873736003     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.89     Document Type: Article

References (50)

1. Haas GP, Delongchamps N, Brawley OW, Wang CY, de la Roza G. The worldwide epidemiology of prostate cancer: perspectives from autopsy studies. Can J Urol 2008; 15: 3866-3871.
2. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C et al. Axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 1991; 11: 5016-5031.
3. Janssen JW, Schulz AS, Steenvoorden AC, Schmidberger M, Strehl S, Ambros PF et al. A novel putative tyrosine kinase receptor with oncogenic potential. Oncogene 1991; 6: 2113-2120.
4. Ye X, Li Y, Stawicki S, Couto S, Eastham-Anderson J, Kallop D et al. An anti-Axl monoclonal antibody attenuates xenograft tumor growth and enhances the effect of multiple anticancer therapies. Oncogene 2010; 29: 5254-5264.
5. Holland SJ, Pan A, Franci C, Hu Y, Chang B, Li W 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: 1544-1554.
6. Zhang YX, Knyazev PG, Cheburkin YV, Sharma K, Knyazev YP, Orfi L et al. AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res 2008; 68: 1905-1915.
7. Rankin EB, Fuh KC, Taylor TE, Krieg AJ, Musser M, Yuan J et al. AXL is an essential factor and therapeutic target for metastatic ovarian cancer. Cancer Res 2010; 70: 7570-7579.
8. Koorstra JB, Karikari CA, Feldmann G, Bisht S, Rojas PL, Offerhaus GJ 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: 618-626.
9. Gjerdrum C, Tiron C, Hoiby T, Stefansson I, Haugen H, Sandal T et al. Axl is an essential epithelial-to-mesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 2010; 107: 1124-1129.
10. Varnum BC, Young C, Elliott G, Garcia A, Bartley TD, Fridell YW et al. Axl receptor tyrosine kinase stimulated by the vitamin K-dependent protein encoded by growth-arrest-specific gene 6. Nature 1995; 373: 623-626.
11. Manfioletti G, Brancolini C, Avanzi G, Schneider C. The protein encoded by a growth arrest-specific gene (gas6) is a new member of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol Cell Biol 1993; 13: 4976-4985.
12. Healy AM, Schwartz JJ, Zhu X, Herrick BE, Varnum B, Farber HW. Gas 6 promotes Axl-mediated survival in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 2001; 280: L1273-L1281.
13. Lee WP, Wen Y, Varnum B, Hung MC. Akt is required for Axl-Gas6 signaling to protect cells from E1A-mediated apoptosis. Oncogene 2002; 21: 329-336.
14. Bellosta P, Costa M, Lin DA, Basilico C. The receptor tyrosine kinase ARK mediates cell aggregation by homophilic binding. Mol Cell Biol 1995; 15: 614-625.
15. Gallicchio M, Mitola S, Valdembri D, Fantozzi R, Varnum B, Avanzi GC et al. Inhibition of vascular endothelial growth factor receptor 2-mediated endothelial cell activation by Axl tyrosine kinase receptor. Blood 2005; 105: 1970-1976.
16. Goruppi S, Chiaruttini C, Ruaro ME, Varnum B, Schneider C. Gas6 induces growth, beta-catenin stabilization, and T-cell factor transcriptional activation in contactinhibited C57 mammary cells. Mol Cell Biol 2001; 21: 902-915.
17. Goruppi S, Ruaro E, Varnum B, Schneider C. Requirement of phosphatidylinositol 3-kinase-dependent pathway and Src for Gas6-Axl mitogenic and survival activities in NIH 3T3 fibroblasts. Mol Cell Biol 1997; 17: 4442-4453.
18. Vajkoczy P, Knyazev P, Kunkel A, Capelle HH, Behrndt S, von Tengg-Kobligk H 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 USA 2006; 103: 5799-5804.
19. Li Y, Ye X, Tan C, Hongo JA, Zha J, Liu J et al. Axl as a potential therapeutic target in cancer: role of Axl in tumor growth, metastasis and angiogenesis. Oncogene 2009; 28: 3442-3455.
20. Shieh YS, Lai CY, Kao YR, Shiah SG, Chu YW, Lee HS et al. Expression of axl in lung adenocarcinoma and correlation with tumor progression. Neoplasia 2005; 7: 1058-1064.
21. Wimmel A, Glitz D, Kraus A, Roeder J, Schuermann M. Axl receptor tyrosine kinase expression in human lung cancer cell lines correlates with cellular adhesion. Eur J Cancer 2001; 37: 2264-2274.
22. Harwood FG, Kasibhatla S, Petak I, Vernes R, Green DR, Houghton JA. Regulation of FasL by NF-kappaB and AP-1 in Fas-dependent thymineless death of human colon carcinoma cells. J Biol Chem 2000; 275: 10023-10029.
23. Mitsiades N, Mitsiades CS, Poulaki V, Chauhan D, Richardson PG, Hideshima T et al. Biologic sequelae of nuclear factor-kappaB blockade in multiple myeloma: therapeutic applications. Blood 2002; 99: 4079-4086.
24. Li ZW, Chu W, Hu Y, Delhase M, Deerinck T, Ellisman M et al. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med 1999; 189: 1839-1845.
25. Zerbini LF, Wang Y, Cho JY, Libermann TA. Constitutive activation of nuclear factor kappaB p50/p65 and Fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer. Cancer Res 2003; 63: 2206-2215.
26. Grall F, Gu X, Tan L, Cho JY, Inan MS, Pettit AR et al. Responses to the proinflammatory cytokines interleukin-1 and tumor necrosis factor alpha in cells derived from rheumatoid synovium and other joint tissues involve nuclear factor kappaB-mediated induction of the Ets transcription factor ESE-1. Arthritis Rheum 2003; 48: 1249-1260.
27. Walz A, Schmutz P, Mueller C, Schnyder-Candrian S. Regulation and function of the CXC chemokine ENA-78 in monocytes and its role in disease. J Leukoc Biol 1997; 62: 604-611.
28. Koch AE. Chemokines and their receptors in rheumatoid arthritis: future targets? Arthritis Rheum 2005; 52: 710-721.
29. Zerbini LF, Wang Y, Czibere A, Correa RG, Cho JY, Ijiri K et al. NF-kappa B-mediated repression of growth arrest-and DNA-damage-inducible proteins 45alpha and gamma is essential for cancer cell survival. Proc Natl Acad Sci USA 2004; 101: 13618-13623.
30. Tsai KC, Teng LW, Shao YM, Chen YC, Lee YC, Li M et al. The first pharmacophore model for potent NF-kappaB inhibitors. Bioorg Med Chem Lett 2009; 19: 5665-5669.
31. Tobe M, Isobe Y, Tomizawa H, Nagasaki T, Takahashi H, Fukazawa T et al. Discovery of quinazolines as a novel structural class of potent inhibitors of NFkappa B activation. Bioorg Med Chem 2003; 11: 383-391.
32. Kobori M, Yang Z, Gong D, Heissmeyer V, Zhu H, Jung YK et al. Wedelolactone suppresses LPS-induced caspase-11 expression by directly inhibiting the IKK complex. Cell Death Differ 2004; 11: 123-130.
33. Sarker D, Reid AH, Yap TA, de Bono JS. Targeting the PI3K/AKT pathway for the treatment of prostate cancer. Clin Cancer Res 2009; 15: 4799-4805.
34. Romashkova JA, Makarov SS. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature 1999; 401: 86-90.
35. Zheng WH, Kar S, Quirion R. Insulin-like growth factor-1-induced phosphorylation of transcription factor FKHRL1 is mediated by phosphatidylinositol 3-kinase/Akt kinase and role of this pathway in insulin-like growth factor-1-induced survival of cultured hippocampal neurons. Mol Pharmacol 2002; 62: 225-233.
36. Okamoto M, Lee C, Oyasu R. Interleukin-6 as a paracrine and autocrine growth factor in human prostatic carcinoma cells in vitro. Cancer Res 1997; 57: 141-146.
37. Hutterer M, Knyazev P, Abate A, Reschke M, Maier H, Stefanova N et al. Axl and growth arrest-specific gene 6 are frequently overexpressed in human gliomas and predict poor prognosis in patients with glioblastoma multiforme. Clin Cancer Res 2008; 14: 130-138.
38. 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: 36-44.
39. Shiozawa Y, Pedersen EA, Patel LR, Ziegler AM, Havens AM, Jung Y et al. GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia 2010; 12: 116-127.
40. Jacob AN, Kalapurakal J, Davidson WR, Kandpal G, Dunson N, Prashar Y et al. A receptor tyrosine kinase, UFO/Axl, and other genes isolated by a modified differential display PCR are overexpressed in metastatic prostatic carcinoma cell line DU145. Cancer Detect Prev 1999; 23: 325-332.
41. Lay JD, Hong CC, Huang JS, Yang YY, Pao CY, Liu CH et al. Sulfasalazine suppresses drug resistance and invasiveness of lung adenocarcinoma cells expressing AXL. Cancer Res 2007; 67: 3878-3887.
42. Demarchi F, Verardo R, Varnum B, Brancolini C, Schneider C. Gas6 antiapoptotic signaling requires NF-kappa B activation. J Biol Chem 2001; 276: 31738-31744.
43. Hasanbasic I, Cuerquis J, Varnum B, Blostein MD. Intracellular signaling pathways involved in Gas6-Axl-mediated survival of endothelial cells. Am J Physiol Heart Circ Physiol 2004; 287: H1207-H1213.
44. Seaton A, Scullin P, Maxwell PJ, Wilson C, Pettigrew J, Gallagher R et al. Interleukin-8 signaling promotes androgen-independent proliferation of prostate cancer cells via induction of androgen receptor expression and activation. Carcinogenesis 2008; 29: 1148-1156.
45. Begley LA, Kasina S, Mehra R, Adsule S, Admon AJ, Lonigro RJ et al. CXCL5 promotes prostate cancer progression. Neoplasia 2008; 10: 244-254.
46. Voronov E, Shouval DS, Krelin Y, Cagnano E, Benharroch D, Iwakura Y et al. IL-1 is required for tumor invasiveness and angiogenesis. Proc Natl Acad Sci USA 2003; 100: 2645-2650.
47. De Smaele E, Zazzeroni F, Papa S, Nguyen DU, Jin R, Jones J et al. Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling. Nature 2001; 414: 308-313.
48. Sawabu T, Seno H, Kawashima T, Fukuda A, Uenoyama Y, Kawada M et al. Growth arrest-specific gene 6 and Axl signaling enhances gastric cancer cell survival via Akt pathway. Mol Carcinog 2007; 46: 155-164.
49. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway. J Cell Sci 2004; 117 (Part 8): 1281-1283.
50. Zerbini LF, Czibere A, Wang Y, Correa RG, Otu H, Joseph M et al. A novel pathway involving melanoma differentiation associated gene-7/interleukin-24 mediates nonsteroidal anti-inflammatory drug-induced apoptosis and growth arrest of cancer cells. Cancer Res 2006; 66: 11922-11931.