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Bone marrow microenvironment and tumor progression

Bibliographic reference Chantrain, Christophe ; Feron, Olivier ; Marbaix, Etienne ; DeClerck, Yves A. Bone marrow microenvironment and tumor progression. In: Cancer Microenvironment, Vol. 1, no. 1, p. 23-35 (2008)
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  1. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57–70
  2. Hurwitz H, Fehrenbacher L, Novotny W, Cartwright T, Hainsworth J, Heim W, Berlin J, Baron A, Griffing S, Holmgren E, Ferrara N, Fyfe G, Rogers B, Ross R, Kabbinavar F (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350:2335–2342
  3. Roodman GD (2004) Mechanisms of bone metastasis. N Engl J Med 350:1655–1664
  4. Guise TA, Kozlow WM, Heras-Herzig A, Padalecki SS, Yin JJ, Chirgwin JM (2005) Molecular mechanisms of breast cancer metastases to bone. Clin Breast Cancer 5(Suppl):S46–S53
  5. Mitsiades CS, McMillin DW, Klippel S, Hideshima T, Chauhan D, Richardson PG, Munshi NC, Anderson KC (2007) The role of the bone marrow microenvironment in the pathophysiology of myeloma and its significance in the development of more effective therapies. Hematol Oncol Clin North Am 21:1007–1034
  6. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420:860–867
  7. Rafii S, Lyden D, Benezra R, Hattori K, Heissig B (2002) Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2:826–835
  8. Kaplan RN, Rafii S, Lyden D (2006) Preparing the “soil”: the premetastatic niche. Cancer Res 66:11089–11093
  9. Schatteman GC, Dunnwald M, Jiao C (2007) Biology of bone marrow-derived endothelial cell precursors. Am J Physiol Heart Circ Physiol 292:H1–18
  10. Loges S, Fehse B, Brockmann MA, Lamszus K, Butzal M, Guckenbiehl M, Schuch G, Ergun S, Fischer U, Zander AR, Hossfeld DK, Fiedler W, Gehling UM (2004) Identification of the adult human hemangioblast. Stem Cells Dev 13:229–242
  11. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125:725–732
  12. Eichmann A, Marcelle C, Breant C, Le Douarin NM (1993) Two molecules related to the VEGF receptor are expressed in early endothelial cells during avian embryonic development. Mech Dev 42:33–48
  13. Bailey AS, Jiang S, Afentoulis M, Baumann CI, Schroeder DA, Olson SB, Wong MH, Fleming WH (2004) Transplanted adult hematopoietic stems cells differentiate into functional endothelial cells. Blood 103:13–19
  14. Rabbany SY, Heissig B, Hattori K, Rafii S (2003) Molecular pathways regulating mobilization of marrow-derived stem cells for tissue revascularization. Trends Mol Med 9:109–117
  15. Bertolini F, Shaked Y, Mancuso P, Kerbel RS (2006) The multifaceted circulating endothelial cell in cancer: towards marker and target identification. Nat Rev Cancer 6:835–845
  16. Bertolini F, Mancuso P, Kerbel RS (2005) Circulating endothelial progenitor cells. N Engl J Med 353:2613–2616
  17. Urbich C, Dimmeler S (2004) Endothelial progenitor cells: characterization and role in vascular biology. Circ Res 95:343–353
  18. Dennis JE, Merriam A, Awadallah A, Yoo JU, Johnstone B, Caplan AI (1999) A quadripotential mesenchymal progenitor cell isolated from the marrow of an adult mouse. J Bone Miner Res 14:700–709
  19. Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ (2003) Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827–1835
  20. Kemp KC, Hows J, Donaldson C (2005) Bone marrow-derived mesenchymal stem cells. Leuk Lymphoma 46:1531–1544
  21. Le Blanc K (2006) Mesenchymal stromal cells: tissue repair and immune modulation. Cytotherapy 8:559–561
  22. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276:71–74
  23. Etheridge SL, Spencer GJ, Heath DJ, Genever PG (2004) Expression profiling and functional analysis of wnt signaling mechanisms in mesenchymal stem cells. Stem Cells 22:849–860
  24. Heissig B, Ohki Y, Sato Y, Rafii S, Werb Z, Hattori K (2005) A role for niches in hematopoietic cell development. Hematology 10:247–253
  25. Yaniv I, Stein J, Farkas DL, Askenasy N (2006) The tale of early hematopoietic cell seeding in the bone marrow niche. Stem Cells Dev 15:4–16
  26. Kaplan RN, Psaila B, Lyden D (2007) Niche-to-niche migration of bone-marrow-derived cells. Trends Mol Med 13:72–81
  27. Taichman RS, Reilly MJ, Emerson SG (1996) Human osteoblasts support human hematopoietic progenitor cells in vitro bone marrow cultures. Blood 87:518–524
  28. Visnjic D, Kalajzic Z, Rowe DW, Katavic V, Lorenzo J, Aguila HL (2004) Hematopoiesis is severely altered in mice with an induced osteoblast deficiency. Blood 103:3258–3264
  29. Taichman RS (2005) Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 105:2631–2639
  30. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 118:149–161
  31. Nilsson SK, Johnston HM, Whitty GA, Williams B, Webb RJ, Denhardt DT, Bertoncello I, Bendall LJ, Simmons PJ, Haylock DN (2005) Osteopontin, a key component of the hematopoietic stem cell niche and regulator of primitive hematopoietic progenitor cells. Blood 106:1232–1239
  32. Hattori K, Heissig B, Rafii S (2003) The regulation of hematopoietic stem cell and progenitor mobilization by chemokine SDF-1. Leuk Lymphoma 44:575–582
  33. Arai F, Suda T (2007) Maintenance of quiescent hematopoietic stem cells in the osteoblastic niche. Ann N Y Acad Sci 1106:41–53
  34. Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, Crystal RG, Besmer P, Lyden D, Moore MA, Werb Z, Rafii S (2002) Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109:625–637
  35. Takafuji V, Forgues M, Unsworth E, Goldsmith P, Wang XW (2007) An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 26:6361–6371
  36. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T (2006) Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 12:657–664
  37. McQuibban GA, Butler GS, Gong JH, Bendall L, Power C, Clark-Lewis I, Overall CM (2001) Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J Biol Chem 276:43503–43508
  38. Yu X, Collin-Osdoby P, Osdoby P (2003) SDF-1 increases recruitment of osteoclast precursors by upregulation of matrix metalloproteinase-9 activity. Connect Tissue Res 44 Suppl 1:79–84
  39. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T (2002) G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 3:687–694
  40. Kopp H.-G., The Bone Marrow Vascular Niche: Home of HSC Differentiation and Mobilization, 10.1152/physiol.00025.2005
  41. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow? Lancet 357:539–545
  42. Hattori K, Heissig B, Wu Y, Dias S, Tejada R, Ferris B, Hicklin DJ, Zhu Z, Bohlen P, Witte L, Hendrikx J, Hackett NR, Crystal RG, Moore MA, Werb Z, Lyden D, Rafii S (2002) Placental growth factor reconstitutes hematopoiesis by recruiting VEGFR1(+) stem cells from bone-marrow microenvironment. Nat Med 8:841–849
  43. Hattori K, Dias S, Heissig B, Hackett NR, Lyden D, Tateno M, Hicklin DJ, Zhu Z, Witte L, Crystal RG, Moore MA, Rafii S (2001) Vascular endothelial growth factor and angiopoietin-1 stimulate postnatal hematopoiesis by recruitment of vasculogenic and hematopoietic stem cells. J Exp Med 193:1005–1014
  44. Gerber HP, Malik AK, Solar GP, Sherman D, Liang XH, Meng G, Hong K, Marsters JC, Ferrara N (2002) VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417:954–958
  45. Allavena P, Sica A, Solinas G, Porta C, Mantovani A (2008) The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages. Crit Rev Oncol Hematol 66:1–9
  46. de Visser KE, Coussens LM (2006) The inflammatory tumor microenvironment and its impact on cancer development. Contrib Microbiol 13:118–137
  47. de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411–423
  48. Maeda H, Akaike T (1998) Nitric oxide and oxygen radicals in infection, inflammation, and cancer. Biochemistry (Mosc) 63:854–865
  49. Pollard JW (2004) Tumour-educated macrophages promote tumour progression and metastasis. Nat Rev Cancer 4:71–78
  50. Hudson JD, Shoaibi MA, Maestro R, Carnero A, Hannon GJ, Beach DH (1999) A proinflammatory cytokine inhibits p53 tumor suppressor activity. J Exp Med 190:1375–1382
  51. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, Segall JE, Pollard JW, Condeelis J (2007) Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 67:2649–2656
  52. Condeelis J, Pollard JW (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124:263–266
  53. Coussens LM, Tinkle CL, Hanahan D, Werb Z (2000) MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103:481–490
  54. Wedemeyer J, Galli SJ (2005) Decreased susceptibility of mast cell-deficient Kit(W)/Kit(W-v) mice to the development of 1, 2-dimethylhydrazine-induced intestinal tumors. Lab Invest 85:388–396
  55. Starkey JR, Crowle PK, Taubenberger S (1988) Mast-cell-deficient W/Wv mice exhibit a decreased rate of tumor angiogenesis. Int J Cancer 42:48–52
  56. Nozawa H, Chiu C, Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 103:12493–12498
  57. Coussens LM, Raymond WW, Bergers G, Laig-Webster M, Behrendtsen O, Werb Z, Caughey GH, Hanahan D (1999) Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev 13:1382–1397
  58. Karnoub AE, Dash AB, Vo AP, Sullivan A, Brooks MW, Bell GW, Richardson AL, Polyak K, Tubo R, Weinberg RA (2007) Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449:557–563
  59. Kopp HG, Ramos CA, Rafii S (2006) Contribution of endothelial progenitors and proangiogenic hematopoietic cells to vascularization of tumor and ischemic tissue. Curr Opin Hematol 13:175–181
  60. Balkwill F, Coussens LM (2004) Cancer: an inflammatory link. Nature 431:405–406
  61. Salcedo Rosalba, Wasserman Ken, Young Howard A., Grimm Michael C., Howard O. M. Zack, Anver Miriam R., Kleinman Hynda K., Murphy William J., Oppenheim Joost J., Vascular Endothelial Growth Factor and Basic Fibroblast Growth Factor Induce Expression of CXCR4 on Human Endothelial Cells, 10.1016/s0002-9440(10)65365-5
  62. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, Hattori K, Zhang F, Hicklin DJ, Wu Y, Zhu Z, Dunn A, Salari H, Werb Z, Hackett NR, Crystal RG, Lyden D, Rafii S (2006) Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 12:557–567
  63. Bergers G, Brekken R, McMahon G, Vu TH, Itoh T, Tamaki K, Tanzawa K, Thorpe P, Itohara S, Werb Z, Hanahan D (2000) Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2:737–744
  64. Huang S., Contributions of Stromal Metalloproteinase-9 to Angiogenesis and Growth of Human Ovarian Carcinoma in Mice, 10.1093/jnci/94.15.1134
  65. Chantrain CF, Shimada H, Jodele S, Groshen S, Ye W, Shalinsky DR, Werb Z, Coussens LM, DeClerck YA (2004) Stromal matrix metalloproteinase-9 regulates the vascular architecture in neuroblastoma by promoting pericyte recruitment. Cancer Res 64:1675–1686
  66. Jodele S, Chantrain CF, Blavier L, Lutzko C, Crooks GM, Shimada H, Coussens LM, DeClerck YA (2005) The contribution of bone marrow-derived cells to the tumor vasculature in neuroblastoma is matrix metalloproteinase-9 dependent. Cancer Res 65:3200–3208
  67. Urbich C, Heeschen C, Aicher A, Dernbach E, Zeiher AM, Dimmeler S (2003) Relevance of monocytic features for neovascularization capacity of circulating endothelial progenitor cells. Circulation 108:2511–2516
  68. 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 tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6:409–421
  69. De Palma M, Naldini L (2006) Role of haematopoietic cells and endothelial progenitors in tumour angiogenesis. Biochim Biophys Acta 1766:159–166
  70. Li B, Sharpe EE, Maupin AB, Teleron AA, Pyle AL, Carmeliet P, Young PP (2006) VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization. FASEB J 20:1495–1497
  71. Goon PK, Lip GY, Boos CJ, Stonelake PS, Blann AD (2006) Circulating endothelial cells, endothelial progenitor cells, and endothelial microparticles in cancer. Neoplasia 8:79–88
  72. Lamagna C, Bergers G (2006) The bone marrow constitutes a reservoir of pericyte progenitors. J Leukoc Biol 80:677–681
  73. Song S, Ewald AJ, Stallcup W, Werb Z, Bergers G (2005) PDGFRbeta + perivascular progenitor cells in tumours regulate pericyte differentiation and vascular survival. Nat Cell Biol 7:870–879
  74. Rajantie I, Ilmonen M, Alminaite A, Ozerdem U, Alitalo K, Salven P (2004) Adult bone marrow-derived cells recruited during angiogenesis comprise precursors for periendothelial vascular mural cells. Blood 104:2084–2086
  75. De Palma M, Venneri MA, Galli R, Sergi SL, Politi LS, Sampaolesi M, Naldini L (2005) Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 8:211–226
  76. Coukos G, Benencia F, Buckanovich RJ, Conejo-Garcia JR (2005) The role of dendritic cell precursors in tumour vasculogenesis. Br J Cancer 92:1182–1187
  77. Muller V, Hayes DF, Pantel K (2006) Recent translational research: circulating tumor cells in breast cancer patients. Breast Cancer Res 8:110
  78. Elshimali YI, Grody WW (2006) The clinical significance of circulating tumor cells in the peripheral blood. Diagn Mol Pathol 15:187–194
  79. Sun YX, Wang JC, Shelburne CE, Lopatin DE, Chinnaiyan AM, Rubin MA, Pienta KJ, Taichman RS (2003) Expression of CXCR4, CXCL12 (SDF-1) in human prostate cancers (PCa) in vivo. J Cell Biochem 89:462–473
  80. Geminder H., Sagi-Assif O., Goldberg L., Meshel T., Rechavi G., Witz I. P., Ben-Baruch A., A Possible Role for CXCR4 and Its Ligand, the CXC Chemokine Stromal Cell-Derived Factor-1, in the Development of Bone Marrow Metastases in Neuroblastoma, 10.4049/jimmunol.167.8.4747
  81. Kozlow W, Guise TA (2005) Breast cancer metastasis to bone: mechanisms of osteolysis and implications for therapy. J Mammary Gland Biol Neoplasia 10:169–180
  82. Strahm B, Durbin AD, Sexsmith E, Malkin D (2008) The CXCR4-SDF1alpha axis is a critical mediator of rhabdomyosarcoma metastatic signaling induced by bone marrow stroma. Clin Exp Metastasis 25:1–10
  83. Zhang L, Yeger H, Das B, Irwin MS, Baruchel S (2007) Tissue microenvironment modulates CXCR4 expression and tumor metastasis in neuroblastoma. Neoplasia 9:36–46
  84. Muller A, Homey B, Soto H, Ge N, Catron D, Buchanan ME, McClanahan T, Murphy E, Yuan W, Wagner SN, Barrera JL, Mohar A, Verastegui E, Zlotnik A (2001) Involvement of chemokine receptors in breast cancer metastasis. Nature 410:50–56
  85. Goldberg-Bittman L, Sagi-Assif O, Meshel T, Nevo I, Levy-Nissenbaum O, Yron I, Witz IP, Ben Baruch A (2005) Cellular characteristics of neuroblastoma cells: regulation by the ELR-CXC chemokine CXCL10 and expression of a CXCR3-like receptor. Cytokine 29:105–117
  86. Yin T, Li L (2006) The stem cell niches in bone. J Clin Invest 116:1195–1201
  87. 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 Invest 98:1544–1549
  88. Kitazawa S, Kitazawa R (2002) RANK ligand is a prerequisite for cancer-associated osteolytic lesions. J Pathol 198:228–236
  89. Teitelbaum SL (2000) Bone resorption by osteoclasts. Science 289:1504–1508
  90. Kostenuik PJ, Shalhoub V (2001) Osteoprotegerin: a physiological and pharmacological inhibitor of bone resorption. Curr Pharm Des 7:613–635
  91. Sohara Y, Shimada H, DeClerck YA (2005) Mechanisms of bone invasion and metastasis in human neuroblastoma. Cancer Lett 228:203–209
  92. Callander NS, Roodman GD (2001) Myeloma bone disease. Semin Hematol 38:276–285
  93. Sohara Y, Shimada H, Minkin C, Erdreich-Epstein A, Nolta JA, DeClerck YA (2005) Bone marrow mesenchymal stem cells provide an alternate pathway of osteoclast activation and bone destruction by cancer cells. Cancer Res 65:1129–1135
  94. Ara T, Shimada H, Keshelava N, Metelitsa LS, Song LP, Groshen SG, Seeger RC, DeClerck YA (2008) IL-6 promotes the growth and survival of neuroblastoma cells. Cancer Res (in press)
  95. Anderson K. C., Multiple Myeloma: New Insights and Therapeutic Approaches, 10.1182/asheducation-2000.1.147
  96. Kim JB, Leucht P, Lam K, Luppen C, Ten Berge D, Nusse R, Helms JA (2007) Bone regeneration is regulated by wnt signaling. J Bone Miner Res 22:1913–1923
  97. Niehrs C (2006) Function and biological roles of the Dickkopf family of Wnt modulators. Oncogene 25:7469–7481
  98. Voorzanger-Rousselot N, Goehrig D, Journe F, Doriath V, Body JJ, Clezardin P, Garnero P (2007) Increased Dickkopf-1 expression in breast cancer bone metastases. Br J Cancer 97:964–970
  99. Qian J, Xie J, Hong S, Yang J, Zhang L, Han X, Wang M, Zhan F, Shaughnessy JD Jr., Epstein J, Kwak LW, Yi Q (2007) Dickkopf-1 (DKK1) is a widely expressed and potent tumor-associated antigen in multiple myeloma. Blood 110:1587–1594
  100. Giuliani N, Morandi F, Tagliaferri S, Lazzaretti M, Donofrio G, Bonomini S, Sala R, Mangoni M, Rizzoli V (2007) Production of Wnt inhibitors by myeloma cells: potential effects on canonical Wnt pathway in the bone microenvironment. Cancer Res 67:7665–7674
  101. Feeley BT, Gamradt SC, Hsu WK, Liu N, Krenek L, Robbins P, Huard J, Lieberman JR (2005) Influence of BMPs on the formation of osteoblastic lesions in metastatic prostate cancer. J Bone Miner Res 20:2189–2199
  102. 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 438:820–827
  103. Psaila Bethan, Kaplan Rosandra N., Port Elisa R., Lyden David, Priming the ‘Soil’ for Breast Cancer Metastasis: The Pre-Metastatic Niche, 10.3233/bd-2007-26106
  104. Heissig B, Rafii S, Akiyama H, Ohki Y, Sato Y, Rafael T, Zhu Z, Hicklin DJ, Okumura K, Ogawa H, Werb Z, Hattori K (2005) Low-dose irradiation promotes tissue revascularization through VEGF release from mast cells and MMP-9-mediated progenitor cell mobilization. J Exp Med 202:739–750
  105. Shaked Y, Ciarrocchi A, Franco M, Lee CR, Man S, Cheung AM, Hicklin DJ, Chaplin D, Foster FS, Benezra R, Kerbel RS (2006) Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors. Science 313:1785–1787
  106. Bertolini F, Paul S, Mancuso P, Monestiroli S, Gobbi A, Shaked Y, Kerbel RS (2003) Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res 63:4342–4346
  107. Furstenberger G, von Moos R, Lucas R, Thurlimann B, Senn HJ, Hamacher J, Boneberg EM (2006) Circulating endothelial cells and angiogenic serum factors during neoadjuvant chemotherapy of primary breast cancer. Br J Cancer 94:524–531
  108. Shaked Y, Kerbel RS (2007) Antiangiogenic strategies on defense: on the possibility of blocking rebounds by the tumor vasculature after chemotherapy. Cancer Res 67:7055–7058
  109. Rosti V, Massa M, Campanelli R, De Amici M, Piccolo G, Perfetti V (2007) Vascular endothelial growth factor promoted endothelial progenitor cell mobilization into the peripheral blood of a patient with POEMS syndrome. Haematologica 92:1291–1292
  110. Coussens LM, Fingleton B, Matrisian LM (2002) Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295:2387–2392
  111. Hatse S, Princen K, Bridger G, De Clercq E, Schols D (2002) Chemokine receptor inhibition by AMD3100 is strictly confined to CXCR4. FEBS Lett 527:255–262