GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche

Neoplasia

Volumn 12, Issue 2, 2010, Pages 116-127

  Shiozawa, Yusuke ^a   Pedersen, Elisabeth A ^a   Patel, Lalit R ^b   Ziegler, Anne M ^a   Havens, Aaron M ^a,c   Jung, Younghun ^a   Wang, Jingcheng ^a   Zalucha, Stephanie ^a   Loberg, Robert D ^b   Pienta, Kenneth J ^b   Taichman, Russell S ^a  

^a UNIVERSITY OF MICHIGAN SCHOOL OF DENTISTRY   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL RECEPTOR AXL; CELL RECEPTOR MER; CELL RECEPTOR SKY; GROWTH ARREST SPECIFIC PROTEIN 6; LIPOCORTIN 2; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BONE MARROW; CANCER INVASION; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DORMANCY; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

EID: 76749109371     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.91384     Document Type: Article

References (56)

1. Coleman RE (2006). Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 12, 6243s-6249s.
2. Taichman RS (2005). Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105, 2631-2639.
3. Taichman RS and Emerson SG (1994). Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 179, 1677-1682.
4. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, and Suda T (2004). Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118, 149-161.
5. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, et al. (2003). Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425, 841-846.
6. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, et al. (2003). Identification of the haematopoietic stem cell niche and control of the niche size. Nature 425, 836-841.
7. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, and Morrison SJ (2005). SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121, 1109-1121.
8. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, and McCauley LK (2002). Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 62, 1832-1837.
9. Shiozawa Y, Havens AM, Jung Y, Ziegler AM, Pedersen EA, Wang J, Lu G, Roodman GD, Loberg RD, Pienta KJ, et al. (2008). Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem 105, 370-380.
10. Pantel K, Alix-Panabieres C, and Riethdorf S (2009). Cancer micrometastases. Nat Rev Clin Oncol 6, 339-351.
11. Morgan TM, Lange PH, Porter MP, Lin DW, Ellis WJ, Gallaher IS, and Vessella RL (2009). Disseminated tumor cells in prostate cancer patients after radical prostatectomy and without evidence of disease predicts biochemical recurrence. Clin Cancer Res 15, 677-683.
12. Nash KT, Phadke PA, Navenot JM, Hurst DR, Accavitti-Loper MA, Sztul E, Vaidya KS, Frost AR, Kappes JC, Peiper SC, et al. (2007). Requirement of KISS1 secretion for multiple organ metastasis suppression and maintenance of tumor dormancy. J Natl Cancer Inst 99, 309-321.
13. Miura Y, Gao Z, Miura M, Seo BM, Sonoyama W, Chen W, Gronthos S, Zhang L, and Shi S (2006). Mesenchymal stem cell-organized bone marrow elements: an alternative hematopoietic progenitor resource. Stem Cells 24, 2428-2436.
14. Raynal P and Pollard HB (1994). Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins. Biochim Biophys Acta 1197, 63-93.
15. Jung Y, Wang J, Song J, Shiozawa Y, Havens A, Wang Z, Sun YX, Emerson SG, Krebsbach PH, and Taichman RS (2007). Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 110, 82-90.
16. Hafizi S and Dahlback B (2006). Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 17, 295-304.
17. Neubauer A, Fiebeler A, Graham DK, O'Bryan JP, Schmidt CA, Barckow P, Serke S, Siegert W, Snodgrass HR, Huhn D, et al. (1994). Expression of axl, a transforming receptor tyrosine kinase, in normal and malignant hematopoiesis. Blood 84, 1931-1941.
18. Crosier PS, Hall LR, Vitas MR, Lewis PM, and Crosier KE (1995). Identification of a novel receptor tyrosine kinase expressed in acute myeloid leukemic blasts. Leuk Lymphoma 18, 443-449.
19. Avanzi GC, Gallicchio M, Cavalloni G, Gammaitoni L, Leone F, Rosina A, Boldorini R, Monga G, Pegoraro L, Varnum B, et al. (1997). GAS6, the ligand of Axl and Rse receptors, is expressed in hematopoietic tissue but lacks mitogenic activity. Exp Hematol 25, 1219-1226.
20. Satomura K, Derubeis AR, Fedarko NS, Ibaraki-O'Connor K, Kuznetsov SA, Rowe DW, Young MF, and Gehron Robey P (1998). Receptor tyrosine kinase expression in human bone marrow stromal cells. J Cell Physiol 177, 426-438.
21. Dormady SP, Zhang XM, and Basch RS (2000). Hematopoietic progenitor cells grow on 3T3 fibroblast monolayers that overexpress growth arrest-specific gene-6 (GAS6). Proc Natl Acad Sci USA 97, 12260-12265.
22. Jiang HY, Lee KH, Schneider C, O WS, Tang PL, and Chow PH (2001). The growth arrest specific gene (gas6) protein is expressed in abnormal embryos sired by male golden hamsters with accessory sex glands removed. Anat Embryol (Berl) 203, 343-355.
23. Wu TT, Sikes RA, Cui Q, Thalmann GN, Kao C, Murphy CF, Yang H, Zhau HE, Balian G, and Chung LW (1998). Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigenproducing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines. Int J Cancer 77, 887-894.
24. 3 integrins by SDF-1/CXC12 increases the aggressiveness of prostate cancer cells. Prostate 67, 61-73.
25. Wang J, Shiozawa Y, Wang Y, Jung Y, Pienta KJ, Mehra R, Loberg R, and Taichman RS (2008). The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 283, 4283-4294.
26. 1 phase of the cell cycle. Blood 90, 4384-4393.
27. Fridell YW, Jin Y, Quilliam LA, Burchert A, McCloskey P, Spizz G, Varnum B, Der C, and Liu ET (1996). Differential activation of the Ras/ extracellular-signal-regulated protein kinase pathway is responsible for the biological consequences induced by the Axl receptor tyrosine kinase. Mol Cell Biol 16, 135-145.
28. Chetcuti A, Margan SH, Russell P, Mann S, Millar DS, Clark SJ, Rogers J, Handelsman DJ, and Dong Q (2001). Loss of annexin II heavy and light chains in prostate cancer and its precursors. Cancer Res 61, 6331-6334.
29. Banerjee AG, Liu J, Yuan Y, Gopalakrishnan VK, Johansson SL, Dinda AK, Gupta NP, Trevino L, and Vishwanatha JK (2003). Expression of biomarkers modulating prostate cancer angiogenesis: differential expression of annexin II in prostate carcinomas from India and USA. Mol Cancer 2, 34.
30. Kirshner J, Chen CJ, Liu P, Huang J, and Shively JE (2003). CEACAM1-4S, a cell-cell adhesion molecule, mediates apoptosis and reverts mammary carcinoma cells to a normal morphogenic phenotype in a 3D culture. Proc Natl Acad Sci USA 100, 521-526.
31. Liu JW, Shen JJ, Tanzillo-Swarts A, Bhatia B, Maldonado CM, Person MD, Lau SS, and Tang DG (2003). Annexin II expression is reduced or lost in prostate cancer cells and its re-expression inhibits prostate cancer cell migration. Oncogene 22, 1475-1485.
32. Smitherman AB, Mohler JL, Maygarden SJ, and Ornstein DK (2004). Expression of annexin I, II and VII proteins in androgen stimulated and recurrent prostate cancer. J Urol 171, 916-920.
33. Semov A, Moreno MJ, Onichtchenko A, Abulrob A, Ball M, Ekiel I, Pietrzynski G, Stanimirovic D, and Alakhov V (2005). Metastasis-associated protein S100A4 induces angiogenesis through interaction with annexin II and accelerated plasmin formation. J Biol Chem 280, 20833-20841.
34. Koh AJ, Demiralp B, Neiva KG, Hooten J, Nohutcu RM, Shim H, Datta NS, Taichman RS, and McCauley LK (2005). Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology 146, 4584-4596.
35. Pettway GJ and McCauley LK (2008). Ossicle and vossicle implant model systems. Methods Mol Biol 455, 101-110.
36. Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, Atchison RE, McLaughlin J, Swift SE, Pali ES, Yam G, et al. (2005). Multiple roles for the receptor tyrosine kinase axl in tumor formation. Cancer Res 65, 9294-9303.
37. Budagian V, Bulanova E, Orinska Z, Duitman E, Brandt K, Ludwig A, Hartmann D, Lemke G, Saftig P, and Bulfone-Paus S (2005). Soluble Axl is generated by ADAM10-dependent cleavage and associates with Gas6 in mouse serum. Mol Cell Biol 25, 9324-9339.
38. van Ginkel PR, Gee RL, Shearer RL, Subramanian L, Walker TM, Albert DM, Meisner LF, Varnum BC, and Polans AS (2004). Expression of the receptor tyrosine kinase Axl promotes ocular melanoma cell survival. Cancer Res 64, 128-134.
39. Son BK, Kozaki K, Iijima K, Eto M, Nakano T, Akishita M, and Ouchi Y (2007). Gas6/Axl-PI3K/Akt pathway plays a central role in the effect of statins on inorganic phosphate-induced calcification of vascular smooth muscle cells. Eur J Pharmacol 556, 1-8.
40. Sainaghi PP, Castello L, Bergamasco L, Galletti M, Bellosta P, and Avanzi GC (2005). Gas6 induces proliferation in prostate carcinoma cell lines expressing the Axl receptor. J Cell Physiol 204, 36-44.
41. Wu YM, Robinson DR, and Kung HJ (2004). Signal pathways in up-regulation of chemokines by tyrosine kinase MER/NYK in prostate cancer cells. Cancer Res 64, 7311-7320.
42. O'Bryan JP, Frye RA, Cogswell PC, Neubauer A, Kitch B, Prokop C, Espinosa R III, Le Beau MM, Earp HS, and Liu ET (1991). axl, a transforming gene isolated from primary human myeloid leukemia cells, encodes a novel receptor tyrosine kinase. Mol Cell Biol 11, 5016-5031.
43. Rochlitz C, Lohri A, Bacchi M, Schmidt M, Nagel S, Fopp M, Fey MF, Herrmann R, and Neubauer A (1999). 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 13, 1352-1358.
44. Wimmel A, Glitz D, Kraus A, Roeder J, and Schuermann M (2001). Axl receptor tyrosine kinase expression in human lung cancer cell lines correlates with cellular adhesion. Eur J Cancer 37, 2264-2274.
45. Shieh YS, Lai CY, Kao YR, Shiah SG, Chu YW, Lee HS, and Wu CW (2005). Expression of axl in lung adenocarcinoma and correlation with tumor progression. Neoplasia 7, 1058-1064.
46. Chung BI, Malkowicz SB, Nguyen TB, Libertino JA, and McGarvey TW (2003). Expression of the proto-oncogene Axl in renal cell carcinoma. DNA Cell Biol 22, 533-540.
47. Meric F, Lee WP, Sahin A, Zhang H, Kung HJ, and Hung MC (2002). Expression profile of tyrosine kinases in breast cancer. Clin Cancer Res 8, 361-367.
48. Wu CW, Li AF, Chi CW, Lai CH, Huang CL, Lo SS, Lui WY, and Lin WC (2002). Clinical significance of AXL kinase family in gastric cancer. Anticancer Res 22, 1071-1078.
49. Zhang YX, Knyazev PG, Cheburkin YV, Sharma K,Knyazev YP,Orfi L, Szabadkai I, Daub H, Keri G, and Ullrich A (2008). AXL is a potential target for therapeutic intervention in breast cancer progression. Cancer Res 68, 1905-1915.
50. Manfioletti G, Brancolini C, Avanzi G, and Schneider C (1993). 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 13, 4976-4985.
51. Robinson D, He F, Pretlow T, and Kung HJ (1996). A tyrosine kinase profile of prostate carcinoma. Proc Natl Acad Sci USA 93, 5958-5962.
52. Jacob AN, Kalapurakal J, Davidson WR, Kandpal G, Dunson N, Prashar Y, and Kandpal RP (1999). 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 23, 325-332.
53. Shiozawa Y, Havens AM, Pienta KJ, and Taichman RS (2008). The bone marrow niche: habitat to hematopoietic and mesenchymal stem cells, and unwitting host to molecular parasites. Leukemia 22, 941-950.
54. Shiozawa Y, Pedersen EA, and Taichman RS (in press). GAS6/Mer axis regulates the homing and survival of the E2A/PBX1-positive B-cell precursor acute lymphoblastic leukemia in the bone marrow niche. Exp Hematol.
55. Jung Y, Wang J, Schneider A, Sun YX, Koh-Paige AJ, Osman NI, McCauley LK, and Taichman RS (2006). Regulation of SDF-1 (CXCL12) production by osteoblasts; a possible mechanism for stem cell homing. Bone 38, 497-508.
56. Schofield R (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4, 7-25.