Homing of cancer cells to the bone

Cancer Microenvironment

Volumn 4, Issue 3, 2011, Pages 221-235

  Mishra, Anjali ^a   Shiozawa, Yusuke ^a   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)

Author keywords

Bone microenvironment; Chemotaxis; Cytokines; Homing; HSC niche; Matrix degradation; Skeletal metastasis; Tumor bone cross talk

Indexed keywords

2 (5 CHLORO 2 FLUOROPHENYL) 4 (4 PYRIDINYLAMINO)PTERIDINE; AMD 1300; ANTINEOPLASTIC AGENT; AXL PROTEIN; BISPHOSPHONIC ACID DERIVATIVE; CADHERIN; CADHERIN 11; CATHEPSIN; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR7; CXCL16 CHEMOKINE; DENOSUMAB; DIPEPTIDYL PEPTIDASE IV; GROWTH ARREST SPECIFIC PROTEIN 6; HERMES ANTIGEN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LIPOCORTIN 2; MATRIX METALLOPROTEINASE; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPONTIN; OSTEOPROTEGERIN; PROSTATE SPECIFIC ANTIGEN; STROMAL CELL DERIVED FACTOR 1; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR RUNX2; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG; UNINDEXED DRUG; UROKINASE; VERY LATE ACTIVATION ANTIGEN 4; ZOLEDRONIC ACID;

ACIDOSIS; ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; BONE METASTASIS; BREAST CANCER; CANCER ASSOCIATED FIBROBLAST; CANCER CELL; CANCER STEM CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL HOMING; CELL MIGRATION; CELL PROLIFERATION; CHEMOTAXIS; CIRCULATING TUMOR CELL; DISSEMINATED TUMOR CELL; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FIBROBLAST; HEMATOPOIETIC STEM CELL; HUMAN; HYPOXIA; MELANOMA; NONHUMAN; ONCOLOGICAL PARAMETERS; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; PRIMARY TUMOR; PRIORITY JOURNAL; PROMYELOCYTIC LEUKEMIA; PROSTATE CANCER; PROTEIN EXPRESSION; PROTEIN FAMILY; REVIEW; STEM CELL NICHE; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR STROMA;

EID: 84856497985     PISSN: 18752292     EISSN: 18752284     Source Type: Journal    
DOI: 10.1007/s12307-011-0083-6     Document Type: Review

References (194)

1. Coleman RE (2006) Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res 12(20 Pt 2):6243s- 6249s (Pubitemid 44703797)
2. Mundy GR (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Cancer 2(8):584-593 (Pubitemid 37328925)
3. Jemal A et al (2007) Cancer statistics, 2007. CA Cancer J Clin 57(1):43-66 (Pubitemid 46148091)
4. Mantyh PW et al (2002) Molecular mechanisms of cancer pain. Nat Rev Cancer 2(3):201-209 (Pubitemid 37328789)
5. Coleman RE (1997) Skeletal complications of malignancy. Cancer 80(8 Suppl):1588-1594 (Pubitemid 27444031)
6. Townson JL, Chambers AF (2006) Dormancy of solitary metastatic cells. Cell Cycle 5(16):1744-1750 (Pubitemid 44435316)
7. Morgan TM 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 (2):677-683
8. Braun S et al (2005) A pooled analysis of bone marrow micrometastasis in breast cancer. N Engl J Med 353(8):793-802 (Pubitemid 41215488)
9. Cristofanilli M et al (2004) Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N Engl J Med 351(8):781-791 (Pubitemid 39095313)
10. Pierga JY et al (2008) Circulating tumor cell detection predicts early metastatic relapse after neoadjuvant chemotherapy in large operable and locally advanced breast cancer in a phase II randomized trial. Clin Cancer Res 14(21):7004-7010
11. Roudier M (2003) Phenotypic heterogeneity of end-stage prostate carcinoma metastatic to bone. Hum Pathol 34(7):646-653 (Pubitemid 36875509)
12. Liu W et al (2009) Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat Med 15(5):559-565
13. Roodman GD (2004) Mechanisms of bone metastasis. N Engl J Med 350(16):1655-1664
14. Guise TA et al (2006) Basic Mechanisms Responsible for Osteolytic and Osteoblastic Bone Metastases. Clin Cancer Res 12(20):6213s-6216s (Pubitemid 44703792)
15. Kalluri R, Weinberg RA (2009) The basics of epithelialmesenchymal transition. J Clin Invest 119(6):1420-1428
16. Vicovac L, Aplin JD (1996) Epithelial-mesenchymal transition during trophoblast differentiation. Acta Anat (Basel) 156(3):202-216 (Pubitemid 27072576)
17. Zeisberg EM et al (2007) Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 13(8):952-961 (Pubitemid 47222040)
18. Zeisberg M et al (2007) Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition. J Biol Chem 282(32):23337-23347 (Pubitemid 47311952)
19. Thiery JP (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2(6):442-454
20. Mani SA et al (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133(4):704-715 (Pubitemid 351636299)
21. Morel AP et al (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 3(8): e2888
22. Lapidot T et al (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367 (6464):645-648 (Pubitemid 24067706)
23. Al-Hajj M et al (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100(7):3983-3988 (Pubitemid 36418143)
24. Ginestier C et al (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1(5):555-567 (Pubitemid 350056407)
25. Singh SK et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63(18):5821-5828 (Pubitemid 37187480)
26. Ronnov-Jessen L, Petersen OW, Bissell MJ (1996) Cellular changes involved in conversion of normal to malignant breast: importance of the stromal reaction. Physiol Rev 76(1):69-125 (Pubitemid 26048279)
27. Bierie B, Moses HL (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6(7):506-520 (Pubitemid 43980540)
28. Kuperwasser C et al (2004) Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci USA 101(14):4966-4971 (Pubitemid 38469186)
29. Orimo A et al (2005) Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell 121 (3):335-348 (Pubitemid 40692295)
30. Stetler-Stevenson WG, Aznavoorian S, Liotta LA (1993) Tumor cell interactions with the extracellular matrix during invasion and metastasis. Annu Rev Cell Biol 9:541-573
31. Sternlicht MD et al (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98 (2):137-146 (Pubitemid 29344902)
32. Karnoub AE et al (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449(7162):557-563 (Pubitemid 47525152)
33. Goldstein RH et al (2010) Human bone marrow-derived MSCs can home to orthotopic breast cancer tumors and promote bone metastasis. Cancer Res 70(24):10044-10050
34. Subarsky P, Hill RP (2003) The hypoxic tumour microenvironment and metastatic progression. Clin Exp Metastasis 20(3):237-250 (Pubitemid 36513228)
35. John A, Tuszynski G (2001) The role of matrix metalloproteinases in tumor angiogenesis and tumor metastasis. Pathol Oncol Res 7(1):14-23 (Pubitemid 32591662)
36. Wilson TJ, Singh RK (2008) Proteases as modulators of tumorstromal interaction: primary tumors to bone metastases. Biochim Biophys Acta 1785(2):85-95
37. Bachmeier BE et al (2001) Matrix metalloproteinases (MMPs) in breast cancer cell lines of different tumorigenicity. Anticancer Res 21(6A):3821-3828 (Pubitemid 34229247)
38. Nakopoulou L et al (2003) MMP-2 protein in invasive breast cancer and the impact of MMP-2/TIMP-2 phenotype on overall survival. Breast Cancer Res Treat 77(2):145-155 (Pubitemid 36197615)
39. Eck SM et al (2009) Matrix metalloproteinase-1 promotes breast cancer angiogenesis and osteolysis in a novel in vivo model. Breast Cancer Res Treat 116(1):79-90
40. Klein A et al (2009) Identification of brain- and bone-specific breast cancer metastasis genes. Cancer Lett 276(2):212-220
41. Dong Z et al (2005) Matrix metalloproteinase activity and osteoclasts in experimental prostate cancer bone metastasis tissue. Am J Pathol 166(4):1173-1186 (Pubitemid 40524441)
42. Nabha SMet al (2008) Bone marrow stromal cells enhance prostate cancer cell invasion through type I collagen in an MMP-12 dependent manner. Int J Cancer 122(11):2482-2490 (Pubitemid 351590480)
43. Janowska-Wieczorek A et al (2000) Differential MMP and TIMP production by human marrow and peripheral blood CD34(+) cells in response to chemokines. Exp Hematol 28(11):1274-1285
44. Sloane BF (1990) Cathepsin B and cystatins: evidence for a role in cancer progression. Semin Cancer Biol 1(2):137-152
45. Sinha AA et al (2001) Ratio of cathepsin B to stefin A identifies heterogeneity within Gleason histologic scores for human prostate cancer. Prostate 48(4):274-284 (Pubitemid 32816553)
46. Brubaker KD et al (2003) Cathepsin K mRNA and protein expression in prostate cancer progression. J Bone Miner Res 18 (2):222-230 (Pubitemid 36125914)
47. Testa JE, Quigley JP (1990) The role of urokinase-type plasminogen activator in aggressive tumor cell behavior. Cancer Metastasis Rev 9(4):353-367
48. Achbarou A et al (1994) Urokinase overproduction results in increased skeletal metastasis by prostate cancer cells in vivo. Cancer Res 54(9):2372-2377 (Pubitemid 24138727)
49. Rabbani SA et al (1990) An amino-terminal fragment of urokinase isolated from a prostate cancer cell line (PC-3) is mitogenic for osteoblast-such as cells. Biochem Biophys Res Commun 173(3):1058-1064
50. Christopherson KW 2nd, Hangoc G, Broxmeyer HE (2002) Cell surface peptidase CD26/dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 alpha-mediated chemotaxis of human cord blood CD34+ progenitor cells. J Immunol 169(12):7000-7008 (Pubitemid 36899288)
51. Sun YX et al (2008) CD26/dipeptidyl peptidase IV regulates prostate cancer metastasis by degrading SDF-1/CXCL12. Clin Exp Metastasis 25(7):765-776
52. Christopherson KW 2nd et al (2004) Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 305 (5686):1000-1003 (Pubitemid 39071774)
53. Cramer SD, Chen Z, Peehl DM (1996) Prostate specific antigen cleaves parathyroid hormone-related protein in the PTH-such as domain: inactivation of PTHrP-stimulated cAMP accumulation in mouse osteoblasts. J Urol 156(2 Pt 1):526-531 (Pubitemid 126445373)
54. Dallas SL et al (1995) Dual role for the latent transforming growth factor-beta binding protein in storage of latent TGF-beta in the extracellular matrix and as a structural matrix protein. J Cell Biol 131(2):539-549
55. Iwamura M et al (1996) Alteration of the hormonal bioactivity of parathyroid hormone-related protein (PTHrP) as a result of limited proteolysis by prostate-specific antigen. Urology 48 (2):317-325 (Pubitemid 26279633)
56. Killian CS et al (1993) Mitogenic response of osteoblast cells to prostate-specific antigen suggests an activation of latent TGFbeta and a proteolytic modulation of cell adhesion receptors. Biochem Biophys Res Commun 192(2):940-947 (Pubitemid 23227414)
57. Nadiminty N et al (2006) Prostate-specific antigen modulates genes involved in bone remodeling and induces osteoblast differentiation of human osteosarcoma cell line SaOS-2. Clin Cancer Res 12(5):1420-1430
58. Nagasawa T, Tachibana K, Kishimoto T (1998) A novel CXC chemokine PBSF/SDF-1 and its receptor CXCR4: their functions in development, hematopoiesis and HIV infection. Semin Immunol 10(3):179-185 (Pubitemid 28347034)
59. Ponomaryov T et al (2000) Induction of the chemokine stromalderived factor-1 following DNA damage improves human stem cell function. J Clin Invest 106(11):1331-1339
60. Loetscher M et al (1994) Cloning of a human seventransmembrane domain receptor, LESTR, that is highly expressed in leukocytes. J Biol Chem 269(1):232-237 (Pubitemid 24026649)
61. Peled A et al (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283(5403):845-848
62. Kollet O et al (2001) Rapid and efficient homing of human CD34(+)CD38(?/low)CXCR4(+) stem and progenitor cells to the bone marrow and spleen of NOD/SCID and NOD/SCID/B2m(null) mice. Blood 97(10):3283-3291
63. Peled A et al (1999) The chemokine SDF-1 stimulates integrinmediated arrest of CD34(+) cells on vascular endothelium under shear flow. J Clin Invest 104(9):1199-1211 (Pubitemid 29536291)
64. Peled A et al (2000) The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/ stromal migration and engraftment of NOD/SCID mice. Blood 95(11):3289-3296 (Pubitemid 30428455)
65. Wysoczynski M et al (2005) Incorporation of CXCR4 into membrane lipid rafts primes homing-related responses of hematopoietic stem/progenitor cells to an SDF-1 gradient. Blood 105(1):40-48 (Pubitemid 40053061)
66. Taichman RS et al (2002) Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Cancer Res 62(6):1832-1837 (Pubitemid 34408510)
67. Sun YX et al (2005) Skeletal localization and neutralization of the SDF-1(CXCL12)/CXCR4 axis blocks prostate cancer metastasis and growth in osseous sites in vivo. J Bone Miner Res 20 (2):318-329
68. Sun YX et al (2003) Expression of CXCR4 and CXCL12 (SDF- 1) in human prostate cancers (PCa) in vivo. J Cell Biochem 89 (3):462-473
69. Arya M et al (2004) The importance of the CXCL12-CXCR4 chemokine ligand-receptor interaction in prostate cancer metastasis. J Exp Ther Oncol 4(4):291-303 (Pubitemid 40189442)
70. Wang J et al (2008) The role of CXCR7/RDC1 as a chemokine receptor for CXCL12/SDF-1 in prostate cancer. J Biol Chem 283 (7):4283-4294
71. Muller A et al (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50-56 (Pubitemid 32225831)
72. Sloan EK, Anderson RL (2002) Genes involved in breast cancer metastasis to bone. Cell Mol Life Sci 59(9):1491-1502 (Pubitemid 35239305)
73. Kang Y et al (2003) A multigenic program mediating breast cancer metastasis to bone. Cancer Cell 3(6):537-549 (Pubitemid 36808649)
74. Luker KE, Luker GD (2006) Functions of CXCL12 and CXCR4 in breast cancer. Cancer Lett 238(1):30-41 (Pubitemid 44183757)
75. Shim H et al (2006) Lower expression of CXCR4 in lymph node metastases than in primary breast cancers: potential regulation by ligand-dependent degradation and HIF-1alpha. Biochem Biophys Res Commun 346(1):252-258 (Pubitemid 43865990)
76. Salvucci O et al (2006) The role of CXCR4 receptor expression in breast cancer: a large tissue microarray study. Breast Cancer Res Treat 97(3):275-283 (Pubitemid 43945757)
77. Bradstock KF et al (2000) Effects of the chemokine stromal cellderived factor-1 on the migration and localization of precursor-B acute lymphoblastic leukemia cells within bone marrow stromal layers. Leukemia 14(5):882-888 (Pubitemid 30235067)
78. Bendall LJ et al (2005) Defective p38 mitogen-activated protein kinase signaling impairs chemotaxic but not proliferative responses to stromal-derived factor-1alpha in acute lymphoblastic leukemia. Cancer Res 65(8):3290-3298 (Pubitemid 40524613)
79. Spiegel A et al (2004) Unique SDF-1-induced activation of human precursor-B ALL cells as a result of altered CXCR4 expression and signaling. Blood 103(8):2900-2907 (Pubitemid 38451658)
80. Mohle R et al (1998) The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 91(12):4523-4530 (Pubitemid 28270300)
81. Voermans C et al (2002) Migratory behavior of leukemic cells from acute myeloid leukemia patients. Leukemia 16(4):650-657 (Pubitemid 34449747)
82. Burger JA et al (2003) CXCR4 chemokine receptors (CD184) and alpha4beta1 integrins mediate spontaneous migration of human CD34+ progenitors and acute myeloid leukaemia cells beneath marrow stromal cells (pseudoemperipolesis). Br J Haematol 122(4):579-589 (Pubitemid 37006402)
83. Tavor S et al (2004) CXCR4 regulates migration and development of human acute myelogenous leukemia stem cells in transplanted NOD/SCID mice. Cancer Res 64 (8):2817-2824 (Pubitemid 38500620)
84. Monaco G et al (2004) Engraftment of acute myeloid leukemia in NOD/SCID mice is independent of CXCR4 and predicts poor patient survival. Stem Cells 22(2):188-201 (Pubitemid 38282634)
85. Burger JA, Burger M, Kipps TJ (1999) Chronic lymphocytic leukemia B cells express functional CXCR4 chemokine receptors that mediate spontaneous migration beneath bone marrow stromal cells. Blood 94(11):3658-3667
86. Burger M et al (2005) Small peptide inhibitors of the CXCR4 chemokine receptor (CD184) antagonize the activation, migration, and antiapoptotic responses of CXCL12 in chronic lymphocytic leukemia B cells. Blood 106(5):1824-1830 (Pubitemid 41208600)
87. Lu Y et al (2008) CXCL16 functions as a novel chemotactic factor for prostate cancer cells in vitro. Mol Cancer Res 6 (4):546-554 (Pubitemid 351521836)
88. Takahashi S et al (1994) Cloning and identification of annexin II as an autocrine/paracrine factor that increases osteoclast formation and bone resorption. J Biol Chem 269(46):28696-28701 (Pubitemid 24366705)
89. Jung Y et al (2007) Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 110(1):82-90 (Pubitemid 47026822)
90. Cole SP et al (1992) Elevated expression of annexin II (lipocortin II, p36) in a multidrug resistant small cell lung cancer cell line. Br J Cancer 65(4):498-502
91. Emoto K et al (2001) Annexin II overexpression correlates with stromal tenascin-C overexpression: a prognostic marker in colorectal carcinoma. Cancer 92(6):1419-1426 (Pubitemid 32947825)
92. Roseman BJ et al (1994) Annexin II marks astrocytic brain tumors of high histologic grade. Oncol Res 6(12):561-567
93. Vishwanatha JK et al (1993) Enhanced expression of annexin II in human pancreatic carcinoma cells and primary pancreatic cancers. Carcinogenesis 14(12):2575-2579 (Pubitemid 24016599)
94. Shiozawa Y et al (2008) Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem 105(2):370-380
95. Shiozawa Y, Pedersen EA, Taichman RS (2010) 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 38(2):132-140
96. Gjerdrum C et al (2010) Axl is an essential epithelial-tomesenchymal transition-induced regulator of breast cancer metastasis and patient survival. Proc Natl Acad Sci USA 107 (3):1124-1129
97. Koorstra JB 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(7):618-626
98. Rankin EB et al (2010) AXL is an essential factor and therapeutic target for metastatic ovarian cancer. Cancer Res 70 (19):7570-7579
99. Hector A et al (2010) The Axl receptor tyrosine kinase is an adverse prognostic factor and a therapeutic target in esophageal adenocarcinoma. Cancer Biol Ther 10(10):1009-1018
100. Gustafsson A et al (2009) Gas6 and the receptor tyrosine kinase Axl in clear cell renal cell carcinoma. PLoS One 4(10):e7575
101. Shiozawa Y et al (2010) GAS6/AXL axis regulates prostate cancer invasion, proliferation, and survival in the bone marrow niche. Neoplasia 12(2):116-127
102. Hill A et al (2006) The emerging role of CD44 in regulating skeletal micrometastasis. Cancer Lett 237(1):1-9
103. Avigdor A et al (2004) CD44 and hyaluronic acid cooperate with SDF-1 in the trafficking of human CD34+ stem/progenitor cells to bone marrow. Blood 103(8):2981-2989 (Pubitemid 38451670)
104. Nilsson SK et al (2005) Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 106(4):1232-1239 (Pubitemid 41129584)
105. Fedarko NS et al (2001) Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clin Cancer Res 7(12):4060-4066 (Pubitemid 34044628)
106. Rudland PS et al (2002) Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res 62(12):3417-3427 (Pubitemid 34651388)
107. Thalmann GN et al (1999) Osteopontin: possible role in prostate cancer progression. Clin Cancer Res 5(8):2271-2277 (Pubitemid 29399287)
108. Tuck AB et al (1997) Osteopontin and p53 expression are associated with tumor progression in a case of synchronous, bilateral, invasive mammary carcinomas. Arch Pathol Lab Med 121(6):578-584 (Pubitemid 27259939)
109. Tuck AB et al (1999) Osteopontin induces increased invasiveness and plasminogen activator expression of human mammary epithelial cells. Oncogene 18(29):4237-4246 (Pubitemid 29377854)
110. Wai PY, Kuo PC (2004) The role of Osteopontin in tumor metastasis. J Surg Res 121(2):228-241 (Pubitemid 39387464)
111. Giancotti FG, Ruoslahti E (1999) Integrin signaling. Science 285 (5430):1028-1032
112. Furger KA et al (2003) Beta(3) integrin expression increases breast carcinoma cell responsiveness to the malignancyenhancing effects of osteopontin. Mol Cancer Res 1(11):810-819 (Pubitemid 37174452)
113. Sun YX et al (2007) Expression and activation of alpha v beta 3 integrins by SDF-1/CXC12 increases the aggressiveness of prostate cancer cells. Prostate 67(1):61-73
114. Sethi T et al (1999) Extracellular matrix proteins protect small cell lung cancer cells against apoptosis: a mechanism for small cell lung cancer growth and drug resistance in vivo. Nat Med 5 (6):662-668 (Pubitemid 29289430)
115. Hodkinson PS et al (2006) ECM overrides DNA damageinduced cell cycle arrest and apoptosis in small-cell lung cancer cells through beta1 integrin-dependent activation of PI3-kinase. Cell Death Differ 13(10):1776-1788 (Pubitemid 44390864)
116. Aoudjit F, Vuori K (2001) Integrin signaling inhibits paclitaxelinduced apoptosis in breast cancer cells. Oncogene 20(36):4995-5004 (Pubitemid 32769789)
117. Matsunaga T et al (2003) Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med 9 (9):1158-1165 (Pubitemid 37173700)
118. Verfaillie CM (1998) Adhesion receptors as regulators of the hematopoietic process. Blood 92(8):2609-2612 (Pubitemid 28469071)
119. Taichman RS (2005) Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105(7):2631-2639 (Pubitemid 40446251)
120. Chu K et al (2008) Cadherin-11 promotes the metastasis of prostate cancer cells to bone. Mol Cancer Res 6(8):1259-1267
121. Huang CF et al (2010) Cadherin-11 increases migration and invasion of prostate cancer cells and enhances their interaction with osteoblasts. Cancer Res 70(11):4580-4589
122. Tamura D et al (2008) Cadherin-11-mediated interactions with bone marrow stromal/osteoblastic cells support selective colonization of breast cancer cells in bone. Int J Oncol 33(1):17-24
123. Wein F et al (2010) N-cadherin is expressed on human hematopoietic progenitor cells and mediates interaction with human mesenchymal stromal cells. Stem Cell Res 4(2):129-139
124. Kiel MJ et al (2009) Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell 4 (2):170-179
125. Fidler IJ, Kim S-J, Langley RR (2007) The role of the organ microenvironment in the biology and therapy of cancer metastasis. J Cell Biochem 101(4):927-936 (Pubitemid 47040873)
126. Yoneda T, Hiraga T (2005) Crosstalk between cancer cells and bone microenvironment in bone metastasis. Biochem Biophys Res Commun 328(3):679-687 (Pubitemid 40208305)
127. Lacey DL et al (1998) Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell 93 (2):165-176 (Pubitemid 28180851)
128. Boyle WJ, Simonet WS, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423(6937):337-342 (Pubitemid 40852708)
129. Simonet WS et al (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89 (2):309-319 (Pubitemid 27199902)
130. Grimaud E et al (2003) Receptor activator of nuclear factor kappaB ligand (RANKL)/osteoprotegerin (OPG) ratio is increased in severe osteolysis. Am J Pathol 163(5):2021-2031 (Pubitemid 37310032)
131. Brown JM et al (2001) Osteoprotegerin and rank ligand expression in prostate cancer. Urology 57(4):611-616
132. Lynch CC et al (2005) MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell 7 (5):485-496 (Pubitemid 40719131)
133. Sordillo EM, Pearse RN (2003) RANK-Fc: a therapeutic antagonist for RANK-L in myeloma. Cancer 97(3 Suppl):802-812 (Pubitemid 36125816)
134. Jones DH et al (2006) Regulation of cancer cell migration and bone metastasis by RANKL. Nature 440(7084):692-696
135. Miller J et al (2002) The core-binding factor beta subunit is required for bone formation and hematopoietic maturation. Nat Genet 32(4):645-649 (Pubitemid 35435178)
136. Komori T et al (1997) Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89(5):755-764 (Pubitemid 27516178)
137. Barnes GL et al (2003) Osteoblast-related transcription factors Runx2 (Cbfa1/AML3) and MSX2 mediate the expression of bone sialoprotein in human metastatic breast cancer cells. Cancer Res 63(10):2631-2637 (Pubitemid 36605206)
138. Enomoto H et al (2003) Induction of osteoclast differentiation by Runx2 through receptor activator of nuclear factor-kappa B ligand (RANKL) and osteoprotegerin regulation and partial rescue of osteoclastogenesis in Runx2-/- mice by RANKL transgene. J Biol Chem 278(26):23971-23977 (Pubitemid 36830226)
139. Pratap J et al (2005) The Runx2 osteogenic transcription factor regulates matrix metalloproteinase 9 in bone metastatic cancer cells and controls cell invasion. Mol Cell Biol 25(19):8581-8591 (Pubitemid 41369178)
140. Pratap J et al (2006) Regulatory roles of Runx2 in metastatic tumor and cancer cell interactions with bone. Cancer Metastasis Rev 25(4):589-600 (Pubitemid 46071865)
141. Akech J et al (2010) Runx2 association with progression of prostate cancer in patients: mechanisms mediating bone osteolysis and osteoblastic metastatic lesions. Oncogene 29(6):811-821
142. Baniwal SK et al (2010) Runx2 transcriptome of prostate cancer cells: insights into invasiveness and bone metastasis. Mol Cancer 9:258
143. Elliott RL, Blobe GC (2005) Role of transforming growth factor Beta in human cancer. J Clin Oncol 23(9):2078-2093 (Pubitemid 46211385)
144. Mohammad KS et al (2009) Pharmacologic inhibition of the TGF-beta type I receptor kinase has anabolic and anti-catabolic effects on bone. PLoS One 4(4):e5275
145. Derynck R, Zhang YE (2003) Smad-dependent and Smadindependent pathways in TGF-beta family signalling. Nature 425(6958):577-584 (Pubitemid 37280136)
146. Massague J (2000) How cells read TGF-beta signals. Nat Rev Mol Cell Biol 1(3):169-178
147. Dallas SL et al (2002) Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J Biol Chem 277(24):21352-21360 (Pubitemid 34952275)
148. Kakonen SM et al (2002) Transforming growth factor-beta stimulates parathyroid hormone-related protein and osteolytic metastases via Smad and mitogen-activated protein kinase signaling pathways. J Biol Chem 277(27):24571-24578
149. Kitazawa S, Kitazawa R (2002) RANK ligand is a prerequisite for cancer-associated osteolytic lesions. J Pathol 198(2):228-236 (Pubitemid 35243881)
150. Kondo H, Guo J, Bringhurst FR (2002) Cyclic adenosine monophosphate/protein kinase A mediates parathyroid hormone/parathyroid hormone-related protein receptor regulation of osteoclastogenesis and expression of RANKL and osteoprotegerin mRNAs by marrow stromal cells. J Bone Miner Res 17(9):1667-1679
151. Gallwitz WE, Guise TA, Mundy GR (2002) Guanosine nucleotides inhibit different syndromes of PTHrP excess caused by human cancers in vivo. J Clin Invest 110(10):1559-1572 (Pubitemid 35396925)
152. Javelaud D et al (2007) Stable overexpression of Smad7 in human melanoma cells impairs bone metastasis. Cancer Res 67 (5):2317-2324 (Pubitemid 46424252)
153. Alexaki VI et al (2010) GLI2-mediated melanoma invasion and metastasis. J Natl Cancer Inst 102(15):1148-1159
154. Gazzerro E, Canalis E (2006) Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 7(1-2):51-65 (Pubitemid 46044349)
155. Katsuno Y et al (2008) Bone morphogenetic protein signaling enhances invasion and bone metastasis of breast cancer cells through Smad pathway. Oncogene 27(49):6322-6333
156. Lai TH et al (2008) Osteoblasts-derived BMP-2 enhances the motility of prostate cancer cells via activation of integrins. Prostate 68(12):1341-1353
157. Virk MS et al (2009) Influence of simultaneous targeting of the bone morphogenetic protein pathway and RANK/RANKL axis in osteolytic prostate cancer lesion in bone. Bone 44(1):160-167
158. Hauschka PV et al (1986) Growth factors in bone matrix. Isolation of multiple types by affinity chromatography on heparin-Sepharose. J Biol Chem 261(27):12665-12674 (Pubitemid 17204223)
159. GoyaMet al (2004)Growth inhibition of human prostate cancer cells in human adult bone implanted into nonobese diabetic/severe combined immunodeficient mice by a ligand-specific antibody to human insulin-such as growth factors. Cancer Res 64(17):6252-6258 (Pubitemid 39129428)
160. van Golen CM et al (2006) Insulin-such as growth factor-I receptor expression regulates neuroblastoma metastasis to bone. Cancer Res 66(13):6570-6578 (Pubitemid 44085612)
161. Kingsley LA et al (2007) Molecular biology of bone metastasis. Mol Cancer Ther 6(10):2609-2617 (Pubitemid 350058141)
162. Zhong H et al (1999) Overexpression of hypoxia-inducible factor 1alpha in
163. Le QT, Denko NC, Giaccia AJ (2004) Hypoxic gene expression and metastasis. Cancer Metastasis Rev 23(3-4):293-310 (Pubitemid 38881813)
164. Garayoa M et al (2000) Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol Endocrinol 14(6):848-862 (Pubitemid 32260498)
165. McMahon S et al (2006) Transforming growth factor beta1 induces hypoxia-inducible factor-1 stabilization through selective inhibition of PHD2 expression. J Biol Chem 281(34):24171-24181 (Pubitemid 44274191)
166. Hiraga T et al (2007) Hypoxia and hypoxia-inducible factor-1 expression enhance osteolytic bone metastases of breast cancer. Cancer Res 67(9):4157-4163 (Pubitemid 46815061)
167. Brandao-Burch A et al (2005) Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization. Calcif Tissue Int 77(3):167-174 (Pubitemid 41569747)
168. Webb SD, Sherratt JA, Fish RG (1999) Alterations in proteolytic activity at low pH and its association with invasion: a theoretical model. Clin Exp Metastasis 17(5):397-407 (Pubitemid 30019997)
169. Shannon AM et al (2003) Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev 29 (4):297-307
170. Berger CE et al (2001) Scanning electrochemical microscopy at the surface of bone-resorbing osteoclasts: evidence for steadystate disposal and intracellular functional compartmentalization of calcium. J Bone Miner Res 16(11):2092-2102 (Pubitemid 32995401)
171. Chattopadhyay N (2006) Effects of calcium-sensing receptor on the secretion of parathyroid hormone-related peptide and its impact on humoral hypercalcemia of malignancy. Am J Physiol Endocrinol Metab 290(5):E761-E770
172. Sanders JL et al (2000) Extracellular calcium-sensing receptor expression and its potential role in regulating parathyroid hormone-related peptide secretion in human breast cancer cell lines. Endocrinology 141(12):4357-4364 (Pubitemid 32055109)
173. Sanders JL et al (2001) Ca(2+)-sensing receptor expression and PTHrP secretion in PC-3 human prostate cancer cells. Am J Physiol Endocrinol Metab 281(6):E1267-E1274 (Pubitemid 34001203)
174. Liao J et al (2006) Extracellular calcium as a candidate mediator of prostate cancer skeletal metastasis. Cancer Res 66(18):9065-9073 (Pubitemid 44521125)
175. Mihai R et al (2006) Expression of the calcium receptor in human breast cancer-a potential new marker predicting the risk of bone metastases. Eur J Surg Oncol 32(5):511-515
176. Wilson A, Trumpp A (2006) Bone-marrow haematopoietic-stem-cell niches. Nat Rev Immunol 6(2):93-106 (Pubitemid 43361585)
177. Yin T, Li L (2006) The stem cell niches in bone. J Clin Invest 116 (5):1195-1201
178. Shiozawa Y, et al (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Invest 121(4):1298-1312
179. Kaplan RN et al (2005) VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438 (7069):820-827 (Pubitemid 41753060)
180. Roelofs AJ et al (2006) Molecular mechanisms of action of bisphosphonates: current status. Clin Cancer Res 12(20 Pt 2):6222s-6230s (Pubitemid 44703794)
181. Fizazi K et al (2009) Randomized phase II trial of denosumab in patients with bone metastases from prostate cancer, breast cancer, or other neoplasms after intravenous bisphosphonates. J Clin Oncol 27(10):1564-1571
182. Mohammad KS et al (2011) TGF-beta-RI kinase inhibitor SD-208 reduces the development and progression of melanoma bone metastases. Cancer Res 71(1):175-184
183. Buijs JT et al (2007) BMP7, a putative regulator of epithelial homeostasis in the human prostate, is a potent inhibitor of prostate cancer bone metastasis in vivo. Am J Pathol 171 (3):1047-1057 (Pubitemid 47441001)
184. Coenegrachts L et al (2010) Anti-placental growth factor reduces bone metastasis by blocking tumor cell engraftment and osteoclast differentiation. Cancer Res 70(16):6537-6547
185. Carducci MA, Jimeno A (2006) Targeting bone metastasis in prostate cancer with endothelin receptor antagonists. Clin Cancer Res 12(20 Pt 2):6296s-6300s (Pubitemid 44703806)
186. Zhao Y et al (2007) Tumor alphavbeta3 integrin is a therapeutic target for breast cancer bone metastases. Cancer Res 67 (12):5821-5830 (Pubitemid 46985016)
187. Mori Y et al (2004) Anti-alpha4 integrin antibody suppresses the development of multiple myeloma and associated osteoclastic osteolysis. Blood 104(7):2149-2154 (Pubitemid 39297870)
188. Petit I et al (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3(7):687-694 (Pubitemid 34752479)
189. Lapidot T, Dar A, Kollet O (2005) How do stem cells find their way home? Blood 106(6):1901-1910 (Pubitemid 41291700)
190. Abkowitz JL et al (2003) Mobilization of hematopoietic stem cells during homeostasis and after cytokine exposure. Blood 102 (4):1249-1253 (Pubitemid 36988029)
191. Azab AK et al (2009) CXCR4 inhibitor AMD3100 disrupts the interaction of multiple myeloma cells with the bone marrow microenvironment and enhances their sensitivity to therapy. Blood 113(18):4341-4351
192. Nervi B et al (2009) Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood 113(24):6206-6214
193. Burger JA, Stewart DJ (2009) CXCR4 chemokine receptor antagonists: perspectives in SCLC. Expert Opin Investig Drugs 18 (4):481-490
194. Hastie C et al (2008) Interferon-gamma reduces cell surface expression of annexin 2 and suppresses the invasive capacity of prostate cancer cells. J Biol Chem 283(18):12595-12603