GAS6 Receptor Status Is Associated with Dormancy and Bone Metastatic Tumor Formation

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Taichman, Russell S ^a   Patel, Lalit R ^b   Bedenis, Rachel ^b   Wang, Jingcheng ^a   Weidner, Savannah ^b   Schumann, Taibriana ^b   Yumoto, Kenji ^a   Berry, Janice E ^a   Shiozawa, Yusuke ^a   Pienta, Kenneth J ^b,c  

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

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AXL PROTEIN; GROWTH ARREST SPECIFIC PROTEIN 6; MER PROTEIN; TYRO3 PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE METASTASIS; CANCER CELL; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROSTATE CANCER; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

ANIMALS; BONE NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; GENE EXPRESSION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MODELS, BIOLOGICAL; NEOPLASMS, EXPERIMENTAL; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 84876545834     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0061873     Document Type: Article

References (55)

1. Vessella RL, Pantel K, Mohla S, (2007) Tumor cell dormancy: an NCI workshop report. Cancer Biol Ther 6: 1496-1504.
2. Yamazaki S, Iwama A, Takayanagi S, Morita Y, Eto K, et al. (2006) Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J 25: 3515-3523.
3. Wilson A, Oser GM, Jaworski M, Blanco-Bose WE, Laurenti E, et al. (2007) Dormant and self-renewing hematopoietic stem cells and their niches. Ann N Y Acad Sci 1106: 64-75.
4. Viale A, Pelicci PG, (2009) Awaking stem cells from dormancy: growing old and fighting cancer. EMBO Mol Med 1: 88-91.
5. Chitteti BR, Liu Y, Srour EF, (2011) Genomic and proteomic analysis of the impact of mitotic quiescence on the engraftment of human CD34+ cells. PLoS One 6: e17498.
6. Taichman RS, (2005) Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem cell niche. Blood 105(7) 2631-9: 2631-2639.
7. Dormady SP, Zhang XM, Basch RS, (2000) Hematopoietic progenitor cells grow on 3T3 fibroblast monolyers that overexpress growth arrest-specific gene-6 (GAS6). Proceedings of the National Academy of Sciences of the United States of America 97: 12260-12265.
8. Shiozawa Y, Pedersen EA, Patel LR, Ziegler AM, Havens AM, et al. (2010) GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia 12: 116-127.
9. Jung Y, Wang J, Song J, Shiozawa Y, Wang J, et al. (2007) Annexin II expressed by osteoblasts & endothelial cells regulates stem cell adhesion, homing & engraftment following transplantation. Blood 110: 82-90.
10. Bellido-Martin L, de Frutos PG, (2008) Vitamin K-dependent actions of Gas6. Vitam Horm 78: 185-209.
11. Neubauer A, Fiebeler A, Graham DK, Obryan JP, Schmidt CA, et al. (1994) Expression of Axl, A Transforming Receptor Tyrosine Kinase, in Normal and Malignant Hematopoiesis. Blood 84: 1931-1941.
12. Shain SA, (2004) Exogenous fibroblast growth factors maintain viability, promote proliferation, and suppress GADD45alpha and GAS6 transcript content of prostate cancer cells genetically modified to lack endogenous FGF-2. Molecular Cancer Research: MCR 2(11): 653-61.
13. Holland SJ, Powell MJ, Franci C, Chan EW, Friera AM, et al. (2005) Multiple roles for the receptor tyrosine kinase Axl in tumor formation. Cancer Res 65: 9294-9303.
14. Crosier PS, Freeman SA, Orlic D, Bodine DM, Crosier KE, (1996) The Dtk receptor tyrosine kinase, which binds protein S, is expressed during hematopoiesis. Exp Hematol 24: 318-323.
15. Darby C, Giannola DM, Couzens MS, Emerson SG, (2000) ETK2 receptor tyrosine kinase promotes survival of factor-dependent FDC-P1 progenitor cells. Exp Hematol 28: 716-725.
16. Li X, Gounari F, Protopopov A, Khazaie K, von Boehmer H, (2008) Oncogenesis of T-ALL and nonmalignant consequences of overexpressing intracellular NOTCH1. J Exp Med 205: 2851-2861.
17. Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, et al. (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 121: 1298-1312.
18. Havens AM, Pedersen EA, Shiozawa Y, Ying C, Jung Y, et al. (2008) An in vivo mouse model for human prostate cancer metastasis. Neoplasia 10: 371-380.
19. Cooper CR, McLean L, Mucci NR, Poncza P, Pienta KJ, (2000) Prostate cancer cell adhesion to quiescent endothelial cells is not mediated by beta-1 integrin subunit. Anticancer Res 20: 4159-4162.
20. Rehemtulla A, Stegman LD, Cardozo SJ, Gupta S, Hall DE, et al. (2000) Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia (New York) 2: 491-495.
21. Guise TA, Chirgwin JM (2003) Transforming growth factor-beta in osteolytic breast cancer bone metastases. Clin Orth Rel Res S32-S38.
22. Thalmann GN, Anezinis PE, Chang SM, Zhau HE, Kim EE, et al. (1994) Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer [published erratum appears in Cancer Res 1994 Jul 15;54(14):3953]. Cancer Res 54: 2577-2581.
23. Wu TT, Sikes RA, Cui Q, Thalmann GN, Kao C, et al. (1998) Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines. International Journal of Cancer 77: 887-894.
24. Korenchuk S, Lehr JE, McLean L, Lee YG, Whitney S, et al. (2001) VCaP, a cell-based model system of human prostate cancer. In Vivo 15: 163-168.
25. Athanassiadou P, Grapsa D, (2006) Recent advances in the detection of bone marrow micrometastases: A promising area for research or just another false hope? A review of the literature. Cancer Metastasis Rev 25: 507-519.
26. Morgan TM, Lange PH, Porter MP, Lin DW, Ellis WJ, et al. (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.
27. Park SI, Kim SJ, McCauley LK, Gallick GE (2010) Pre-clinical mouse models of human prostate cancer and their utility in drug discovery. Curr Protoc Pharmacol Chapter 14: Unit.
28. Taichman RS, Loberg RD, Mehra R, Pienta KJ, (2007) The evolving biology and treatment of prostate cancer. J Clin Invest 117: 2351-2361.
29. Pienta KJ, McGregor N, Axelrod R, Axelrod DE, (2008) Ecological therapy for cancer: defining tumors using an ecosystem paradigm suggests new opportunities for novel cancer treatments. Transl Oncol 1: 158-164.
30. Wikman H, Vessella R, Pantel K, (2008) Cancer micrometastasis and tumour dormancy. APMIS 116: 754-770.
31. Yu C, Shiozawa Y, Taichman RS, McCauley LK, (2012) Prostate cancer and parasitism of the bone hematopoietic stem cell niche. Crit Rev Eukaryot Gene Expr 22: 131-148.
32. Keller ET, Zhang J, Cooper CR, Smith PC, McCauley LK, et al. (2001) Prostate carcinoma skeletal metastases: cross-talk between tumor andbone. Cancer Metastasis Reviews 20: 333-349.
33. Jung Y, Shiozawa Y, Wang J, McGregor N, Dai J, et al. (2012) Prevalence of prostate cancer metastases after intravenous inoculation provides clues into the molecular basis of dormancy in the bone marrow microenvironment. Neoplasia 14: 429-439.
34. American Cancer Society (2003) American Cancer Society; Cancer Facts & Figures. 2003: 1-52.
35. Loberg RD, Fridman Y, Pienta BA, Keller ET, McCauley LK, et al. (2004) Detection and isolation of circulating tumor cells in urologic cancers: A review. Neoplasia 6: 302-309.
36. Mishra A, Wang J, Shiozawa Y, McGee S, Kim J, et al. (2012) Hypoxia Stabilizes GAS6/Axl Signaling in Metastatic Prostate Cancer. Mol Cancer Res 10(6): 703-712.
37. Yin T, Li L, (2006) The stem cell niches in bone. Journal of Clinical Investigation 116(5): 1195-2010.
38. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, et al. (2004) Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med 10: 858-864.
39. Sainaghi PP, Castello L, Bergamasco L, Galletti M, Bellosta P, et al. (2004) Gas6 induces proliferation in prostate carcinoma cell lines expressing the Axl receptor. Journal of Cellular Physiology 36-44.
40. Paccez JD, Vasques GJ, Correa RG, Vasconcellos JF, Duncan K, et al. (2012) The receptor tyrosine kinase Axl is an essential regulator of prostate cancer proliferation and tumor growth and represents a new therapeutic target. Oncogene 689-698.
41. Hutterer M, Knyazev P, Abate A, Reschke M, Maier H, et al. (2008) 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 14: 130-138.
42. Linger RM, Keating AK, Earp HS, Graham DK, (2010) Taking aim at Mer and Axl receptor tyrosine kinases as novel therapeutic targets in solid tumors. Expert Opin Ther Targets 14: 1073-1090.
43. Koorstra JB, Karikari CA, Feldmann G, Bisht S, Rojas PL, et al. (2009) The Axl receptor tyrosine kinase confers an adverse prognostic influence in pancreatic cancer and represents a new therapeutic target. Cancer Biol Ther 8: 618-626.
44. Song X, Wang H, Logsdon CD, Rashid A, Fleming JB, et al. (2011) Overexpression of receptor tyrosine kinase Axl promotes tumor cell invasion and survival in pancreatic ductal adenocarcinoma. Cancer 117: 734-743.
45. Mollard A, Warner SL, Call LT, Wade ML, Bearss JJ, et al. (2011) Design, Synthesis and Biological Evaluation of a Series of Novel Axl Kinase Inhibitors. ACS Med Chem Lett 2: 907-912.
46. van Ginkel PR, Gee RL, Shearer RL, Subramanian L, Walker TM, et al. (2004) Expression of the receptor tyrosine kinase Axl promotes ocular melanoma cell survival. Cancer Res 64: 128-134.
47. Costa M, Bellosta P, Basilico C, (1996) Cleavage and release of a soluble form of the receptor tyrosine kinase ARK in vitro and in vivo. J Cell Physiol 168: 737-744.
48. Weinger JG, Omari KM, Marsden K, Raine CS, Shafit-Zagardo B, (2009) Up-regulation of soluble Axl and Mer receptor tyrosine kinases negatively correlates with Gas6 in established multiple sclerosis lesions. Am J Pathol 175: 283-293.
49. Ekman C, Stenhoff J, Dahlback B, (2010) Gas6 is complexed to the soluble tyrosine kinase receptor Axl in human blood. J Thromb Haemost 8: 838-844.
50. Ekman C, Gottsater A, Lindblad B, Dahlback B, (2010) Plasma concentrations of Gas6 and soluble Axl correlate with disease and predict mortality in patients with critical limb ischemia. Clin Biochem 43: 873-876.
51. Rankin EB, Fuh KC, Taylor TE, Krieg AJ, Musser M, et al. (2010) AXL is an essential factor and therapeutic target for metastatic ovarian cancer3. Cancer Res 70: 7570-7579.
52. Ekman C, Jonsen A, Sturfelt G, Bengtsson AA, Dahlback B, (2011) Plasma concentrations of Gas6 and sAxl correlate with disease activity in systemic lupus erythematosus. Rheumatology (Oxford) 50: 1064-1069.
53. Caberoy NB, Zhou Y, Li W, (2010) Tubby and tubby-like protein 1 are new MerTK ligands for phagocytosis. EMBO J 29: 3898-3910.
54. Caberoy NB, Alvarado G, Bigcas JL, Li W, (2012) Galectin-3 is a new MerTK-specific eat-me signal. J Cell Physiol 227: 401-407.
55. Suh CH, Hilliard B, Li S, Merrill JT, Cohen PL, (2010) TAM receptor ligands in lupus: protein S but not Gas6 levels reflect disease activity in systemic lupus erythematosus. Arthritis Res Ther 12: R146.