Roles of bone marrow cells in skeletal metastases: No longer bystanders

Cancer Microenvironment

Volumn 4, Issue 3, 2011, Pages 237-246

  Park, Serk In ^a   Soki, Fabiana N ^a   Mccauley, Laurie K ^a  

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

Author keywords

Bone marrow; Hematopoietic stem cells; Macrophages; Megakaryocytes; Metastasis; Myeloid derived suppressor cells

Indexed keywords

CD11B ANTIGEN; CELL MARKER; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR4; GELATINASE B; GR1 PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; PARATHYROID HORMONE; PARATHYROID HORMONE RELATED PROTEIN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANATOMY; ANGIOGENESIS; APOPTOSIS; BONE MARROW; BONE MARROW CELL; BONE METASTASIS; CELL DIFFERENTIATION; CELL HOMING; CELL PROLIFERATION; HEMATOPOIETIC STEM CELL; HUMAN; MACROPHAGE; MEGAKARYOCYTE; MEGAKARYOPOIESIS; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; OSTEAL TISSUE MACROPHAGE; OSTEOBLAST; OSTEOBLASTOGENESIS; OSTEOCLAST; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; REVIEW; STEM CELL NICHE; THROMBOCYTE AGGREGATION; TUMOR ANGIOGENESIS; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR GROWTH;

EID: 84856426449     PISSN: 18752292     EISSN: 18752284     Source Type: Journal    
DOI: 10.1007/s12307-011-0081-8     Document Type: Review

References (100)

1. Fidler IJ (2003) The pathogenesis of cancer metastasis: the 'seed and soil' hypothesis revisited. Nat Rev Canc 3(6):453-458 (Pubitemid 37328849)
2. Talmadge JE, Fidler IJ (2010) AACR centennial series: the biology of cancer metastasis: historical perspective. Canc Res 70 (14):5649-5669. doi:10.1158/0008-5472.CAN-10-1040
3. Fidler IJ (2002) Critical determinants of metastasis. Semin Canc Biol 12(2):89-96. doi:10.1006/scbi.2001.0416 (Pubitemid 34680737)
4. Paget S (1989) The distribution of secondary growths in cancer of the breast. 1889. Canc Metastasis Rev 8(2):98-101
5. Ewing J (1928) Neoplastic diseases; a treatise on tumors. 3d ed rev. and enl., with 546 illustrations. edn. W.B. Saunders, Philadelphia, London
6. Geldof AA (1997) Models for cancer skeletal metastasis: a reappraisal of Batson's plexus. Anticancer Res 17(3A):1535-1539 (Pubitemid 27257642)
7. Fidler IJ, Kripke ML (1977) Metastasis results from preexisting variant cells within a malignant tumor. Science 197(4306):893-895 (Pubitemid 8168759)
8. Hart IR, Fidler IJ (1980) Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Canc Res 40(7):2281-2287 (Pubitemid 10082239)
9. Tarin D, Price JE, Kettlewell MG, Souter RG, Vass AC, Crossley B (1984) Clinicopathological observations on metastasis in man studied in patients treated with peritoneovenous shunts. Br Med J (Clin Res Ed) 288(6419):749-751 (Pubitemid 14117952)
10. Tarin D, Price JE, Kettlewell MG, Souter RG, Vass AC, Crossley B (1984) Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunts. Canc Res 44 (8):3584-3592 (Pubitemid 14098615)
11. Hess KR, Varadhachary GR, Taylor SH, Wei W, Raber MN, Lenzi R, Abbruzzese JL (2006) Metastatic patterns in adenocarcinoma. Cancer 106(7):1624-1633. doi:10.1002/cncr.21778
12. Bubendorf L, Schopfer A, Wagner U, Sauter G, Moch H, Willi N, Gasser TC, Mihatsch MJ (2000) Metastatic patterns of prostate cancer: an autopsy study of 1,589 patients. Hum Pathol 31(5):578-583 (Pubitemid 30323983)
13. Mundy GR (2002) Metastasis to bone: causes, consequences and therapeutic opportunities. Nat Rev Canc 2(8):584-593. doi:10.1038/nrc867 (Pubitemid 37328925)
14. Roodman GD (2004) Mechanisms of bone metastasis. New Engl J Med 350(16):1655-1664. doi:10.1056/NEJMra030831 (Pubitemid 38501167)
15. Rubin MA, Putzi M, Mucci N, Smith DC, Wojno K, Korenchuk S, Pienta KJ (2000) Rapid ("warm") autopsy study for procurement of metastatic prostate cancer. Clin Canc Res 6 (3):1038-1045 (Pubitemid 30159365)
16. Weilbaecher KN, Guise TA, McCauley LK (2011) Cancer to bone: a fatal attraction. Nat Rev Canc 11(6):411-425. doi:10.1038/nrc3055
17. Casimiro S, Guise TA, Chirgwin J (2009) The critical role of the bone microenvironment in cancer metastases. Mol Cell Endocrinol 310(1-2):71-81. doi:10.1016/j.mce.2009.07.004
18. Guise TA, Yin JJ, Taylor SD, Kumagai Y, Dallas M, Boyce BF, Yoneda T, Mundy GR (1996) Evidence for a causal role of parathyroid hormone-related protein in the pathogenesis of human breast cancer-mediated osteolysis. J Clin Investig 98 (7):1544-1549. doi:10.1172/JCI118947 (Pubitemid 26327863)
19. Yin JJ, Selander K, Chirgwin JM, Dallas M, Grubbs BG, Wieser R, Massague J, Mundy GR, Guise TA (1999) TGF-beta signaling blockade inhibits PTHrP secretion by breast cancer cells and bone metastases development. J Clin Investig 103(2):197-206. doi:10.1172/JCI3523 (Pubitemid 29053137)
20. Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ, McCauley LK (2009) A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. Canc Res 69(4):1685-1692. doi:10.1158/0008-5472.CAN-08-2164
21. Liao J, Li X, Koh AJ, Berry JE, Thudi N, Rosol TJ, Pienta KJ, McCauley LK (2008) Tumor expressed PTHrP facilitates prostate cancer-induced osteoblastic lesions. Int J Canc 123 (10):2267-2278. doi:10.1002/ijc.23602
22. Liao J, McCauley LK (2006) Skeletal metastasis: established and emerging roles of parathyroid hormone related protein (PTHrP). Canc Metastasis Rev 25(4):559-571. doi:10.1007/s10555-006-9033-z (Pubitemid 46074999)
23. Bergfeld SA, DeClerck YA (2010) Bone marrow-derived mesenchymal stem cells and the tumor microenvironment. Canc Metastasis Rev 29(2):249-261. doi:10.1007/s10555-010-9222-7
24. Ara T, Declerck YA (2010) Interleukin-6 in bone metastasis and cancer progression. Eur J Canc 46(7):1223-1231. doi:10.1016/j.ejca.2010.02.026
25. Paul WE (1999) Fundamental immunology, 4th edn. Lippincott- Raven, Philadelphia
26. Schermer S (1967) The blood morphology of laboratory animals, 3rd edn. Davis, Philadelphia
27. Travlos GS (2006) Normal structure, function, and histology of the bone marrow. Toxicol Pathol 34(5):548-565. doi:10.1080/01926230600939856 (Pubitemid 44652217)
28. Shirota T, Tavassoli M (1991) Cyclophosphamide-induced alterations of bone marrow endothelium: implications in homing of marrow cells after transplantation. Exp Hematol 19(5):369-373
29. Shirota T, Tavassoli M (1992) Alterations of bone marrow sinus endothelium induced by ionizing irradiation: implications in the homing of intravenously transplanted marrow cells. Blood Cell 18(2):197-214
30. Weiss L, Geduldig U (1991) Barrier cells: stromal regulation of hematopoiesis and blood cell release in normal and stressed murine bone marrow. Blood 78(4):975-990
31. Tavassoli M, Hardy CL (1990) Molecular basis of homing of intravenously transplanted stem cells to the marrow. Blood 76 (6):1059-1070 (Pubitemid 20318147)
32. Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH (1998) Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 188(3):465-474 (Pubitemid 28369136)
33. Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD (1998) Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci U S A 95(24):14423-14428 (Pubitemid 28549383)
34. Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, Nagler A, Ben-Hur H, Many A, Shultz L, Lider O, Alon R, Zipori D, Lapidot T (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283(5403):845-848
35. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T,Murphy E, YuanW,Wagner SN, Barrera JL,Mohar A, Verastegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410(6824):50-56. doi:10.1038/35065016 (Pubitemid 32225831)
36. Taichman RS, Cooper C, Keller ET, Pienta KJ, Taichman NS, McCauley LK (2002) Use of the stromal cell-derived factor-1/CXCR4 pathway in prostate cancer metastasis to bone. Canc Res 62(6):1832-1837 (Pubitemid 34408510)
37. Sun X, Cheng G, Hao M, Zheng J, Zhou X, Zhang J, Taichman RS, Pienta KJ, Wang J (2010) CXCL12/CXCR4/CXCR7 chemokine axis and cancer progression. Canc Metastasis Rev 29(4):709-722. doi:10.1007/s10555-010-9256-x
38. Jung Y, Wang J, Song J, Shiozawa Y, Havens A, Wang Z, Sun YX, Emerson SG, Krebsbach PH, Taichman RS (2007) Annexin II expressed by osteoblasts and endothelial cells regulates stem cell adhesion, homing, and engraftment following transplantation. Blood 110(1):82-90. doi:10.1182/blood-2006-05-021352 (Pubitemid 47026822)
39. Shiozawa Y, Havens AM, Jung Y, Ziegler AM, Pedersen EA, Wang J, Lu G, Roodman GD, Loberg RD, Pienta KJ, Taichman RS (2008) Annexin II/annexin II receptor axis regulates adhesion, migration, homing, and growth of prostate cancer. J Cell Biochem 105(2):370-380. doi:10.1002/jcb.21835
40. Shiozawa Y, Pedersen EA, Havens AM, Jung Y, Mishra A, Joseph J, Kim JK, Patel LR, Ying C, Ziegler AM, Pienta MJ, Song J,Wang J, Loberg RD, Krebsbach PH, Pienta KJ, Taichman RS (2011) Human prostate cancer metastases target the hematopoietic stem cell niche to establish footholds in mouse bone marrow. J Clin Investig. doi:10.1172/JCI43414
41. Okamoto R, Ueno M, Yamada Y, Takahashi N, Sano H, Suda T, Takakura N (2005) Hematopoietic cells regulate the angiogenic switch during tumorigenesis. Blood 105(7):2757-2763. doi:10.1182/blood-2004-08-3317 (Pubitemid 40446266)
42. Schneider A, Kalikin LM, Mattos AC, Keller ET, Allen MJ, Pienta KJ, McCauley LK (2005) Bone turnover mediates preferential localization of prostate cancer in the skeleton. Endocrinology 146(4):1727-1736. doi:10.1210/en.2004-1211 (Pubitemid 40396881)
43. Lichtman MA, Chamberlain JK, Simon W, Santillo PA (1978) Parasinusoidal location of megakaryocytes in marrow: a determinant of platelet release. Am J Hematol 4(4):303-312 (Pubitemid 9066765)
44. Li X, Koh AJ, Wang Z, Soki FN, Park SI, Pienta KJ, McCauley LK (2011) Inhibitory effects of megakaryocytic cells in prostate cancer skeletal metastasis. J Bone Miner Res 26(1):125-134. doi:10.1002/jbmr.204
45. Kacena MA, Gundberg CM, Horowitz MC (2006) A reciprocal regulatory interaction between megakaryocytes, bone cells, and hematopoietic stem cells. Bone 39(5):978-984. doi:10.1016/j. bone.2006.05.019 (Pubitemid 44528390)
46. Kacena MA, Nelson T, Clough ME, Lee SK, Lorenzo JA, Gundberg CM, Horowitz MC (2006) Megakaryocyte-mediated inhibition of osteoclast development. Bone 39(5):991-999. doi:10.1016/j.bone.2006.05.004 (Pubitemid 44528382)
47. Kacena MA, Shivdasani RA,Wilson K, Xi Y, Troiano N, Nazarian A, GundbergCM, BouxseinML, Lorenzo JA, HorowitzMC(2004) Megakaryocyte-osteoblast interaction revealed in mice deficient in transcription factors GATA-1 and NF-E2. J Bone Miner Res 19 (4):652-660. doi:10.1359/JBMR.0301254 (Pubitemid 41071226)
48. Bord S, Frith E, Ireland DC, Scott MA, Craig JI, Compston JE (2005) Megakaryocytes modulate osteoblast synthesis of typel collagen, osteoprotegerin, and RANKL. Bone 36(5):812-819.doi:10.1016/j.bone.2004.12.006 (Pubitemid 40616016)
49. Calvi LM, Adams GB, Weibrecht KW, Weber JM, Olson DP, Knight MC, Martin RP, Schipani E, Divieti P, Bringhurst FR, Milner LA, Kronenberg HM, Scadden DT (2003) Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 425 (6960):841-846. doi:10.1038/nature02040 (Pubitemid 37351468)
50. Udagawa N, Takahashi N, Jimi E,Matsuzaki K, Tsurukai T, Itoh K, Nakagawa N, Yasuda H, Goto M, Tsuda E, Higashio K, Gillespie MT, Martin TJ, Suda T (1999) Osteoblasts/stromal cells stimulate osteoclast activation through expression of osteoclast differentiation factor/RANKL but not macrophage colony-stimulating factor: receptor activator of NF-kappa B ligand. Bone 25(5):517-523 (Pubitemid 29469457)
51. Ahmed N, Khokher MA, Hassan HT (1999) Cytokine-induced expansion of human CD34+ stem/progenitor and CD34 + CD41 + early megakaryocytic marrow cells cultured on normal osteoblasts. Stem Cell 17(2):92-99. doi:10.1002/stem.170092 (Pubitemid 29149398)
52. Roato I, D'Amelio P, Gorassini E, Grimaldi A, Bonello L, Fiori C, Delsedime L, Tizzani A, De Libero A, Isaia G, Ferracini R (2008) Osteoclasts are active in bone forming metastases of prostate cancer patients. PLoS One 3(11):e3627. doi:10.1371/journal.pone.0003627
53. Carmeliet P, Jain RK (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473(7347):298-307. doi:10.1038/nature10144
54. Nieswandt B, Hafner M, Echtenacher B, Mannel DN (1999) Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Canc Res 59(6):1295-1300 (Pubitemid 29136261)
55. Boucharaba A, Serre CM, Gres S, Saulnier-Blache JS, Bordet JC, Guglielmi J, Clezardin P, Peyruchaud O (2004) Plateletderived lysophosphatidic acid supports the progression of osteolytic bone metastases in breast cancer. J Clin Investig 114 (12):1714-1725. doi:10.1172/JCI22123 (Pubitemid 40385527)
56. Gupta GP, Massague J (2004) Platelets and metastasis revisited: a novel fatty link. J Clin Investig 114(12):1691-1693. doi:10.1172/JCI23823 (Pubitemid 40385522)
57. Mizutani K, Sud S, McGregor NA, Martinovski G, Rice BT, Craig MJ, Varsos ZS, Roca H, Pienta KJ (2009) The chemokine CCL2 increases prostate tumor growth and bone metastasis through macrophage and osteoclast recruitment. Neoplasia 11 (11):1235-1242
58. Loberg RD, Ying C, Craig M, Yan L, Snyder LA, Pienta KJ (2007) CCL2 as an important mediator of prostate cancer growth in vivo through the regulation of macrophage infiltration. Neoplasia 9 (7):556-562 (Pubitemid 47121829)
59. Halin S, Rudolfsson SH, Van Rooijen N, Bergh A (2009) Extratumoral macrophages promote tumor and vascular growth in an orthotopic rat prostate tumor model. Neoplasia 11(2):177-186
60. Solinas G, Germano G, Mantovani A, Allavena P (2009) Tumor-associated macrophages (TAM) as major players of the cancer-related inflammation. J Leukoc Biol 86(5):1065-1073. doi:10.1189/jlb.0609385
61. Hiraoka K, Zenmyo M, Watari K, Iguchi H, Fotovati A, Kimura YN, Hosoi F, Shoda T, Nagata K, Osada H, Ono M, Kuwano M (2008) Inhibition of bone and muscle metastases of lung cancer cells by a decrease in the number of monocytes/macrophages. Canc Sci 99(8):1595-1602. doi:10.1111/j.1349-7006.2008. 00880.x
62. Bingle L, Brown NJ, Lewis CE (2002) The role of tumourassociated macrophages in tumour progression: implications for new anticancer therapies. J Pathol 196(3):254-265. doi:10.1002/path.1027 (Pubitemid 34189413)
63. Sica A, Larghi P, Mancino A, Rubino L, Porta C, Totaro MG, Rimoldi M, Biswas SK, Allavena P, Mantovani A (2008) Macrophage polarization in tumour progression. Semin Canc Biol 18(5):349-355. doi:10.1016/j.semcancer.2008.03.004
64. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357(9255):539-545. doi:10.1016/S0140-6736(00)04046-0 (Pubitemid 32173595)
65. Loberg RD, Ying C, Craig M, Day LL, Sargent E, Neeley C, Wojno K, Snyder LA, Yan L, Pienta KJ (2007) Targeting CCL2 with systemic delivery of neutralizing antibodies induces prostate cancer tumor regression in vivo. Canc Res 67 (19):9417-9424. doi:10.1158/0008-5472.CAN-07-1286 (Pubitemid 47535932)
66. Roca H, Varsos Z, Pienta KJ (2008) CCL2 protects prostate cancer PC3 cells from autophagic death via phosphatidylinositol 3-kinase/AKT-dependent survivin up-regulation. J Biol Chem 283(36):25057-25073. doi:10.1074/jbc. M801073200
67. Roca H, Varsos ZS, Sud S, Craig MJ, Ying C, Pienta KJ (2009) CCL2 and interleukin-6 promote survival of human CD11b + peripheral blood mononuclear cells and induce M2-type macrophage polarization. J Biol Chem 284(49):34342-34354. doi:10.1074/jbc.M109.042671
68. Zhang J, Lu Y, Pienta KJ (2010) Multiple roles of chemokine (C-C motif) ligand 2 in promoting prostate cancer growth. J Natl Canc Inst 102(8):522-528. doi:10.1093/jnci/djq044
69. Lin EY, Li JF, Gnatovskiy L, Deng Y, Zhu L, Grzesik DA, Qian H, Xue XN, Pollard JW (2006) Macrophages regulate the angiogenic switch in a mouse model of breast cancer. Canc Res 66(23):11238-11246. doi:10.1158/0008-5472.CAN-06-1278 (Pubitemid 46009952)
70. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL (1996) Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Canc Res 56(20):4625-4629 (Pubitemid 26338061)
71. Hildenbrand R, Dilger I, Horlin A, Stutte HJ (1995) Urokinase and macrophages in tumour angiogenesis. Br J Canc 72(4):818-823
72. Miles DW, Happerfield LC, Naylor MS, Bobrow LG, Rubens RD, Balkwill FR (1994) Expression of tumour necrosis factor (TNF alpha) and its receptors in benign and malignant breast tissue. Int J Canc 56(6):777-782 (Pubitemid 24102739)
73. Jung YJ, Isaacs JS, Lee S, Trepel J, Neckers L (2003) IL- 1beta-mediated up-regulation of HIF-1alpha via an NFkappaB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J 17(14):2115-2117. doi:10.1096/fj.03-0329fje
74. MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15:323-350. doi:10.1146/annurev.immunol.15.1.323 (Pubitemid 27169284)
75. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Canc 4(1):71-78. doi:10.1038/nrc1256 (Pubitemid 38082155)
76. Qian BZ, Pollard JW (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141(1):39-51. doi:10.1016/j.cell.2010.03.014
77. Lewis CE, Pollard JW (2006) Distinct role of macrophages in different tumor microenvironments. Canc Res 66(2):605-612. doi:10.1158/0008-5472.CAN-05- 4005 (Pubitemid 43165918)
78. Alexander K, Chang M, Maylin E, Kohler T, Muller R, Wu A, Van Rooijen N, Sweet M, Hume D, Raggatt L, Pettit A (2011) Osteal macrophages promote in vivo intramembranous bone healing in a mouse tibial injury model. J Bone Miner Res 26 (7):1517-1532. doi:10.1002/jbmr.354
79. Chang MK, Raggatt LJ, Alexander KA, Kuliwaba JS, Fazzalari NL, Schroder K, Maylin ER, Ripoll VM, Hume DA, Pettit AR (2008) Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol 181(2):1232-1244
80. Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. New Engl J Med 315(26):1650-1659. doi:10.1056/NEJM198612253152606 (Pubitemid 17052899)
81. Zumsteg A, Christofori G (2009) Corrupt policemen: inflammatory cells promote tumor angiogenesis. Curr Opin Oncol 21(1):60-70. doi:10.1097/CCO. 0b013e32831bed7e
82. Murdoch C, Muthana M, Coffelt SB, Lewis CE (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Canc 8(8):618-631. doi:10.1038/nrc2444
83. Coffelt SB, Lewis CE, Naldini L, Brown JM, Ferrara N, De Palma M (2010) Elusive identities and overlapping phenotypes of proangiogenic myeloid cells in tumors. Am J Pathol 176 (4):1564-1576. doi:10.2353/ajpath.2010.090786
84. Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber DL, Schneck J, Gabrilovich DI (2007) Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med 13(7):828-835. doi:10.1038/nm1609 (Pubitemid 47038194)
85. Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9 (3):162-174. doi:10.1038/nri2506
86. Nagaraj S, Gabrilovich DI (2008) Tumor escape mechanism governed by myeloid-derived suppressor cells. Canc Res 68 (8):2561-2563. doi:10.1158/0008-5472.CAN-07-6229 (Pubitemid 351556251)
87. Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP, Lin PC (2004) Expansion of myeloid immune suppressor Gr + CD11b + cells in tumorbearing host directly promotes tumor angiogenesis. Canc Cell 6 (4):409-421. doi:10.1016/j.ccr.2004.08.031 (Pubitemid 39361441)
88. Yang L, EdwardsCM,MundyGR (2010)Gr-1 + CD11b +myeloidderived suppressor cells (MDSCs): formidable partners in tumor metastasis. J Bone Miner Res 25(8):1701-1706. doi:10.1002/jbmr.154
89. Kim SJ, Kim JS, Papadopoulos J, Wook Kim S, Maya M, Zhang F, He J, Fan D, Langley R, Fidler IJ (2009) Circulating monocytes expressing CD31: implications for acute and chronic angiogenesis. Am J Pathol 174(5):1972-1980. doi:10.2353/ajpath.2009.080819
90. Shojaei F, Zhong C, Wu X, Yu L, Ferrara N (2008) Role of myeloid cells in tumor angiogenesis and growth. Trends Cell Biol 18(8):372-378. doi:10.1016/j.tcb.2008.06.003
91. Ahn GO, Brown JM (2008) Matrix metalloproteinase-9 is required for tumor vasculogenesis but not for angiogenesis: role of bone marrow-derived myelomonocytic cells. Canc Cell 13 (3):193-205. doi:10.1016/j.ccr.2007.11.032 (Pubitemid 351318369)
92. Taichman NS, Young S, Cruchley AT, Taylor P, Paleolog E (1997) Human neutrophils secrete vascular endothelial growth factor. J Leukoc Biol 62(3):397-400 (Pubitemid 27431612)
93. Yang L, Huang J, Ren X, Gorska AE, Chytil A, Aakre M, Carbone DP, Matrisian LM, Richmond A, Lin PC, Moses HL (2008) Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1 + CD11b + myeloid cells that promote metastasis. Canc Cell 13(1):23-35. doi:10.1016/j.ccr.2007.12.004 (Pubitemid 350309741)
94. ASBMR 29th Annual Meeting (2007) J Bone Miner Res 22(S1): s2-s51. doi:10.1002/jbmr.5650221402
95. Zhuang J, Yang L, Lwin ST, Edwards CM, Edwards JR, Mundy GR (2008) Osteoclasts in myeloma are derived from Gr-1 + CD11b + myeloid immune suppressor cells of the bone marrow niche in vivo. ASH Annu Meet Abstr 112(11):736
96. Melani C, Sangaletti S, Barazzetta FM, Werb Z, Colombo MP (2007) Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloidderived suppressor cell expansion and macrophage infiltration in tumor stroma. Canc Res 67(23):11438-11446. doi:10.1158/0008- 5472.CAN-07-1882 (Pubitemid 350248572)
97. Shiozawa Y, Jung Y, Ziegler AM, Pedersen EA, Wang J, Wang Z, Song J, Lee CH, Sud S, Pienta KJ, Krebsbach PH, Taichman RS (2010) Erythropoietin couples hematopoiesis with bone formation. PLoS One 5(5):e10853. doi:10.1371/journal. pone.0010853
98. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ (2009) Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature 460(7252):259-263. doi:10.1038/nature08099
99. Kaplan RN, Psaila B, Lyden D (2006) Bone marrow cells in the 'pre-metastatic niche': within bone and beyond. Canc Metastasis Rev 25(4):521-529. doi:10.1007/s10555-006-9036-9 (Pubitemid 46071861)
100. Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, MacDonald DD, Jin DK, Shido K, Kerns SA, Zhu Z, Hicklin D, Wu Y, Port JL, Altorki N, Port ER, Ruggero D, Shmelkov SV, Jensen KK, Rafii S, Lyden D (2005) VEGFR1- positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 438(7069):820-827. doi:10.1038/nature04186 (Pubitemid 41753060)