Megakaryocytes, malignancy and bone marrow vascular niches

Journal of Thrombosis and Haemostasis

Volumn 10, Issue 2, 2012, Pages 177-188

  Psaila, B ^a,b   Lyden, D ^b   Roberts, I ^a  

^a IMPERIAL COLLEGE SCHOOL OF MEDICINE   (United Kingdom)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN 1; CD31 ANTIGEN; CD34 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; COLLAGEN TYPE 3; COLLAGEN TYPE 4; FIBROBLAST GROWTH FACTOR 4; GELATINASE A; GELATINASE B; PADGEM PROTEIN; STROMAL CELL DERIVED FACTOR 1; THROMBOPOIETIN; TRANSCRIPTION FACTOR GATA 1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN; VON WILLEBRAND FACTOR;

BONE MARROW CANCER; BONE MARROW METASTASIS; CARCINOGENESIS; CELL ADHESION; CELL FATE; CELL HOMING; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; ENDOTHELIUM CELL; GRANULE CELL; HEMATOPOIETIC STEM CELL; HUMAN; MEGAKARYOCYTE; NONHUMAN; OSTEOBLAST; OSTEOCLAST; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTOPOIESIS; TUMOR MICROENVIRONMENT; VASCULARIZATION;

ANIMALS; BLOOD PLATELETS; BONE MARROW NEOPLASMS; CELL COMMUNICATION; ENDOTHELIAL CELLS; HEMATOPOIETIC STEM CELLS; HUMANS; MEGAKARYOCYTES; NEOPLASM INVASIVENESS; OSTEOBLASTS; SIGNAL TRANSDUCTION; STEM CELL NICHE; STROMAL CELLS;

EID: 84856517458     PISSN: 15387933     EISSN: 15387836     Source Type: Journal    
DOI: 10.1111/j.1538-7836.2011.04571.x     Document Type: Review

References (158)

1. Adams GB, Scadden DT. The hematopoietic stem cell in its place. Nat Immunol 2006; 7: 333-7.
2. Balduino A, Hurtado S, Frazao P, Takiya C, Alves L, Nasciutti L, El-Cheikh M, Borojevic R. Bone marrow subendosteal microenvironment harbours functionally distinct haemosupportive stromal cell populations. Cell Tissue Res 2005; 319: 255-66.
3. Haylock DN, Nilsson SK. Stem cell regulation by the hematopoietic stem cell niche. Cell Cycle 2005; 4: 1353-5.
4. Kaplan RN, Psaila B, Lyden D. Niche-to-Niche migration of bone marrow-derived cells. Trends Mol Med 2007; 13: 72-81.
5. Li L, Neaves WB. Normal stem cells and cancer stem cells: the niche matters. Cancer Res 2006; 66: 4553-7.
6. Nilsson SK, Johnston HM, Coverdale JA. Spatial localization of transplanted hemopoietic stem cells: inferences for the localization of stem cell niches. Blood 2001; 97: 2293-9.
7. Scadden DT. The stem-cell niche as an entity of action. Nature 2006; 441: 1075-9.
8. Yin T, Li L. The stem cell niches in bone. J Clin Invest 2006; 116: 1195-201.
9. Kiel MJ, Morrison SJ. Uncertainty in the niches that maintain haematopoietic stem cells. Nat Rev Immunol 2008; 8: 290-301.
10. Wilson A, Laurenti E, Trumpp A. Balancing dormant and self-renewing hematopoietic stem cells. Curr Opin Genet Dev 2009; 19: 461-8.
11. Taichman RS, Emerson SG. Human osteoblasts support hematopoiesis through the production of granulocyte colony-stimulating factor. J Exp Med 1994; 179: 1677-82.
12. Lord BI, Testa NG, Hendry JH. The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood 1975; 46: 65-72.
13. 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. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003; 425: 841-6.
14. Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, Ross J, Haug J, Johnson T, Feng JQ, Harris S, Wiedemann LM, Mishina Y, Li L. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425: 836-41.
15. Arai F, Hirao A, Ohmura M, Sato H, Matsuoka S, Takubo K, Ito K, Koh GY, Suda T. Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell 2004; 118: 149-61.
16. Yoshihara H, Arai F, Hosokawa K, Hagiwara T, Takubo K, Nakamura Y, Gomei Y, Iwasaki H, Matsuoka S, Miyamoto K, Miyazaki H, Takahashi T, Suda T. Thrombopoietin/MPL signaling regulates hematopoietic stem cell quiescence and interaction with the osteoblastic niche. Cell Stem Cell 2007; 1: 685-97.
17. Wilson A, Murphy MJ, Oskarsson T, Kaloulis K, Bettess MD, Oser GM, Pasche AC, Knabenhans C, Macdonald HR, Trumpp A. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 2004; 18: 2747-63.
18. Kiel MJ, Acar M, Radice GL, Morrison SJ. Hematopoietic stem cells do not depend on N-cadherin to regulate their maintenance. Cell Stem Cell. 2009; 4: 170-9.
19. Adams GB, Chabner KT, Alley IR, Olson DP, Szczepiorkowski ZM, Poznansky MC, Kos CH, Pollak MR, Brown EM, Scadden DT. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006; 439: 599-603.
20. Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, Tesio M, Samstein RM, Goichberg P, Spiegel A, Elson A, Lapidot T. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006; 12: 657-64.
21. Rafii S, Mohle R, Shapiro F, Frey BM, Moore MA. Regulation of hematopoiesis by microvascular endothelium. Leuk Lymphoma 1997; 27: 375-86.
22. Rafii S, Shapiro F, Pettengell R, Ferris B, Nachman RL, Moore MA, Asch AS. Human bone marrow microvascular endothelial cells support long-term proliferation and differentiation of myeloid and megakaryocytic progenitors. Blood 1995; 86: 3353-63.
23. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 2005; 121: 1109-21.
24. Kopp HG, Avecilla ST, Hooper AT, Rafii S. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda) 2005; 20: 349-56.
25. Avecilla ST, Hattori K, Heissig B, Tejada R, Liao F, Shido K, Jin DK, Dias S, Zhang F, Hartman TE, Hackett NR, Crystal RG, Witte L, Hicklin DJ, Bohlen P, Eaton D, Lyden D, de Sauvage F, Rafii S. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat Med 2004; 10: 64-71.
26. Doan PL, Chute JP. The vascular niche: home for normal and malignant hematopoietic stem cells. Leukemia 2011; doi: 10.1038/leu.2011.236.
27. Hooper AT, Butler JM, Nolan DJ, Kranz A, Iida K, Kobayashi M, Kopp HG, Shido K, Petit I, Yanger K, James D, Witte L, Zhu Z, Wu Y, Pytowski B, Rosenwaks Z, Mittal V, Sato TN, Rafii S. Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells. Cell Stem Cell 2009; 4: 263-74.
28. Colmone A, Sipkins DA. Beyond angiogenesis: the role of the endothelium in teh bone marrow vascular niche. Transl Res 2008; 151: 1-9.
29. Shen Q, Wang Y, Kokovay E, Lin G, Chuang SM, Goderie SK, Roysam B, Temple S. Adult SVZ stem cells lie in a vascular niche: a quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008; 3: 289-300.
30. Li W, Johnson SA, Shelley WC, Yoder MC. Hematopoietic stem cell repopulating ability can be maintained in vitro by some primary endothelial cells. Exp Hematol 2004; 32: 1226-37.
31. Rafii S, Shapiro F, Rimarachin J, Nachman RL, Ferris B, Weksler B, Moore MA, Asch AS. Isolation and characterization of human bone marrow microvascular endothelial cells: hematopoietic progenitor cell adhesion. Blood 1994; 84: 10-9.
32. Naiyer AJ, Jo DY, Ahn J, Mohle R, Peichev M, Lam G, Silverstein RL, Moore MA, Rafii S. Stromal derived factor-1-induced chemokinesis of cord blood CD34(+) cells (long-term culture-initiating cells) through endothelial cells is mediated by E-selectin. Blood 1999; 94: 4011-9.
33. Kiel MJ, Morrison SJ. Maintaining hematopoietic stem cells in the vascular niche. Immunity 2006; 25: 862-4.
34. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977-88.
35. Méndez-Ferrer S, Michurina TV, Ferraro F, Mazloom A, MacArthur B, Lira S, Scadden DT, Ma'ayan A, Enikolopov GN, Frenette PS. Coordinated Regulation of Hematopoietic and Mesenchymal Stem Cells in a Bone Marrow Niche. Blood (ASH annual meeting abstracts) 2009; 114: 2.
36. Mendez-Ferrer S, Lucas D, Battista M, Frenette PS. Haematopoietic stem cell release is regulated by circadian oscillations. Nature 2008; 452: 442-7.
37. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007; 131: 324-36.
38. Ellis SL, Grassinger J, Jones A, Borg J, Camenisch T, Haylock D, Bertoncello I, Nilsson SK. The relationship between bone, hemopoietic stem cells, and vasculature. Blood 2011; 118: 1516-24.
39. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake-Lye S, Fujisaki J, Cote D, Rowe DW, Lin CP, Scadden DT. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009; 457: 92-6.
40. Xie Y, Yin T, Wiegraebe W, He XC, Miller D, Stark D, Perko K, Alexander R, Schwartz J, Grindley JC, Park J, Haug JS, Wunderlich JP, Li H, Zhang S, Johnson T, Feldman RA, Li L. Detection of functional haematopoietic stem cell niche using real-time imaging. Nature 2009; 457: 97-101.
41. Kaushansky K. The molecular mechanisms that control thrombopoiesis. J Clin Invest 2005; 115: 3339-47.
42. Kaushansky K. Historical review: megakaryopoiesis and thrombopoiesis. Blood 2008; 111: 981-6.
43. Geddis AE. Megakaryopoiesis. Semin Hematol 2011; 47: 212-9.
44. Dhanjal TS, Pendaries C, Ross EA, Larson MK, Protty MB, Buckley CD, Watson SP. A novel role for PECAM-1 in megakaryocytokinesis and recovery of platelet counts in thrombocytopenic mice. Blood 2007; 109: 4237-44.
45. Junt T, Schulz H, Chen Z, Massberg S, Goerge T, Krueger A, Wagner DD, Graf T, Italiano JEJ, Shivdasani RA, von Andrian UH. Dynamic visualization of thrombopoiesis within bone marrow. Science 2007; 317: 1767-70.
46. Wang JF, Liu ZY, Groopman JE. The alpha-chemokine receptor CXCR4 is expressed on the megakaryocytic lineage from progenitor to platelets and modulates migration and adhesion. Blood 1998; 92: 756-64.
47. Hamada T, Mohle R, Hesselgesser J, Hoxie J, Nachman RL, Moore MA, Rafii S. Transendothelial migration of megakaryocytes in response to stromal cell-derived factor-1 (SDF-1) enhances platelet formation. J Exp Med 1998; 188: 539-48.
48. Kopp HG, Rafii S. Thrombopoietic cells and the bone marrow vascular niche. Ann NY Acad Sci 2007; 1106: 175-9.
49. Balduini A, Pallotta I, Malara A, Lova P, Pecci A, Viarengo G, Balduini CL, Torti M. Adhesive receptors, extracellular proteins and myosin IIA orchestrate proplatelet formation by human megakaryocytes. J Thromb Haemost 2008; 6: 1900-7.
50. Nilsson SK, Debatis ME, Dooner MS, Madri JA, Quesenberry PJ, Becker PS. Immunofluorescence characterization of key extracellular matrix proteins in murine bone marrow in situ. J Histochem Cytochem 1998; 46: 371-7.
51. Pallotta I, Lovett M, Rice W, Kaplan DL, Balduini A. Bone marrow osteoblastic niche: a new model to study physiological regulation of megakaryopoiesis. PLoS ONE 2009; 4: e8359.
52. Leven RM, Tablin F. Extracellular matrix stimulation of guinea pig megakaryocyte proplatelet formation in vitro is mediated through the vitronectin receptor. Exp Hematol 1992; 20: 1316-22.
53. Fox NE, Kaushansky K. Engagement of integrin alpha4beta1 enhances thrombopoietin-induced megakaryopoiesis. Exp Hematol 2005; 33: 94-9.
54. Dunois-Larde C, Capron C, Fichelson S, Bauer T, Cramer-Borde E, Baruch D. Exposure of human megakaryocytes to high shear rates accelerates platelet production. Blood 2009; 114: 1875-83.
55. Kacena MA, Gundberg CM, Horowitz MC. A reciprocal regulatory interaction between megakaryocytes, bone cells, and hematopoietic stem cells. Bone 2006; 39: 978-84.
56. Kacena MA, Nelson T, Clough ME, Lee SK, Lorenzo JA, Gundberg CM, Horowitz MC. Megakaryocyte-mediated inhibition of osteoclast development. Bone 2006; 39: 991-9.
57. Ciovacco WA, Cheng YH, Horowitz MC, Kacena MA. Immature and mature megakaryocytes enhance osteoblast proliferation and inhibit osteoclast formation. J Cell Biochem 2010; 109: 774-81.
58. Lemieux JM, Horowitz MC, Kacena MA. Involvement of integrins alpha(3)beta(1) and alpha(5)beta(1) and glycoprotein IIb in megakaryocyte-induced osteoblast proliferation. J Cell Biochem 2010; 109: 927-32.
59. Tanum G. The megakaryocyte DNA content and platelet formation after the sublethal whole body irradiation of rats. Blood 1984; 63: 917-20.
60. Dominici M, Rasini V, Bussolari R, Chen X, Hofmann TJ, Spano C, Bernabei D, Veronesi E, Bertoni F, Paolucci P, Conte P, Horwitz EM. Restoration and reversible expansion of the osteoblastic hematopoietic stem cell niche after marrow radioablation. Blood 2009; 114: 2333-43.
61. Mohle R, Green D, Moore MA, Nachman RL, Rafii S. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc Natl Acad Sci U S A 1997; 94: 663-8.
62. Varner JA. The sticky truth about angiogenesis and thrombospondins. J Clin Invest 2006; 116: 3111-3.
63. Kopp HG, Hooper AT, Broekman MJ, Avecilla ST, Petit I, Luo M, Milde T, Ramos CA, Zhang F, Kopp T, Bornstein P, Jin DK, Marcus AJ, Rafii S. Thrombospondins deployed by thrombopoietic cells determine angiogenic switch and extent of revascularization. J Clin Invest 2006; 116: 3277-91.
64. Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, Bouck NP. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci U S A 1990; 87: 6624-8.
65. Blair P, Flaumenhaft R. Platelet alpha-granules: basic biology and clinical correlates. Blood Rev 2009; 23: 177-89.
66. Italiano JE Jr, Battinelli EM. Selective sorting of alpha-granule proteins. J Thromb Haemost 2009; 7(Suppl 1): 173-6.
67. Italiano JE Jr, Richardson JL, Patel-Hett S, Battinelli E, Zaslavsky A, Short S, Ryeom S, Folkman J, Klement GL. Angiogenesis is regulated by a novel mechanism: pro- and antiangiogenic proteins are organized into separate platelet alpha granules and differentially released. Blood 2008; 111: 1227-33.
68. Sehgal S, Storrie B. Evidence that differential packaging of the major platelet granule proteins von Willebrand factor and fibrinogen can support their differential release. J Thromb Haemost 2007; 5: 2009-16.
69. Villeneuve J, Block A, Le Bousse-Kerdiles MC, Lepreux S, Nurden P, Ripoche J, Nurden AT. Tissue inhibitors of matrix metalloproteinases in platelets and megakaryocytes: a novel organization for these secreted proteins. Exp Hematol 2009; 37: 849-56.
70. Kamykowski J, Carlton P, Sehgal S, Storrie B. Quantitative immunofluorescence mapping reveals little functional coclustering of proteins within platelet {alpha}-granules. Blood 2011; 118: 1370-3.
71. Ma L, Perini R, McKnight W, Dicay M, Klein A, Hollenberg MD, Wallace JL. Proteinase-activated receptors 1 and 4 counter-regulate endostatin and VEGF release from human platelets. Proc Natl Acad Sci U S A 2005; 102: 216-20.
72. Nierodzik ML, Chen K, Takeshita K, Li JJ, Huang YQ, Feng XS, D'Andrea MR, Andrade-Gordon P, Karpatkin S. Protease-activated receptor 1 (PAR-1) is required and rate-limiting for thrombin-enhanced experimental pulmonary metastasis. Blood 1998; 92: 3694-700.
73. Nierodzik ML, Bain RM, Liu LX, Shivji M, Takeshita K, Karpatkin S. Presence of the seven transmembrane thrombin receptor on human tumour cells: effect of activation on tumour adhesion to platelets and tumor tyrosine phosphorylation. Br J Haematol 1996; 92: 452-7.
74. Battinelli EM, Markens BA, Italiano JE Jr. Release of angiogenesis regulatory proteins from platelet alpha granules: modulation of physiologic and pathologic angiogenesis. Blood 2011; 118: 1359-69.
75. Siegelman ES, Needleman L. Venous thrombosis and cancer. N Engl J Med 1993; 328: 885.
76. Gupta GP, Massague J. Platelets and metastasis: a novel fatty link. J Clin Invest 2004; 114: 1696-3.
77. Karpatkin S, Pearlstein E. Role of Platelets in tumor cell metastases. Ann Intern Med 1981; 95: 646-1.
78. Gasic GJ, Gasic TB, Stewart CC. Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA 1968; 61: 46-52.
79. Honn KV, Tang DG, Crissman JD. Platelets and cancer metastasis: a causal relationship? Cancer Metastasis Rev 1992; 11: 325-51.
80. Sierko E, Wojtukiewicz MD. Platelets and angiogenesis in malignancy. Semin Thromb Hemost 2004; 30: 95-108.
81. Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-6.
82. Folkman J. Role of angiogenesis in tumor growth and metastasis. Semin Oncol 2002; 29: 15-8.
83. Folkman J, Kalluri R. Cancer without disease. Nature 2004; 427: 787.
84. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996; 86: 353-64.
85. Rafii DC, Psaila B, Butler J, Jin DK, Lyden D. Regulation of vasculogenesis by platelet-mediated recruitment of bone marrow-derived cells. Arterioscler Thromb Vasc Biol 2008; 28: 217-22.
86. Massberg S, Konrad I, Schurzinger K, Lorenz M, Schneider S, Zohlnhoefer D, Hoppe K, Schiemann M, Kennerknecht E, Sauer S, Schulz C, Kerstan S, Rudelius M, Seidl S, Sorge F, Langer H, Peluso M, Goyal P, Vestweber D, Emambokus NR, et al. Platelets secrete stromal cell-derived factor 1a and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med 2006; 203: 1211-33.
87. 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, et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4(+) hemangiocytes. Nat Med 2006; 12: 557-66.
88. Daub K, Langer H, Seizer P, Stellos K, May AE, Goyal P, Bigalke B, Schonberger T, Geisler T, Siegel-Axel D, Oostendorp RA, Lindemann S, Gawaz M. Platelets induce differentiation of human CD34+ progenitor cells into foam cells and endothelial cells. FASEB J 2006; 20: 2559-61.
89. de Boer HC, Verseyden C, Ulfman LH, Zwaginga JJ, Bot I, Biessen EA, Rabelink TJ, van Zonneveld AJ. Fibrin and activated platelets cooperatively guide stem cells to a vascular injury and promote differentiation towards an endothelial cell phenotype. Arterioscler Thromb Vasc Biol 2006; 26: 1653-9.
90. Langer H, May AE, Daub K, Heinzmann U, Lang P, Schumm M, Vestweber D, Massberg S, Schonberger T, Pfisterer I, Hatzopoulos AK, Gawaz M. Adherent platelets recruit and induce differentiation of murine embryonic endothelial progenitor cells to mature endothelial cells in vitro. Circ Res 2006; 98: e2-10.
91. Langer HF, Daub K, Braun G, Schonberger T, May AE, Schaller M, Stein GM, Stellos K, Bueltmann A, Siegel-Axel D, Wendel HP, Aebert H, Roecken M, Seizer P, Santoso S, Wesselborg S, Brossart P, Gawaz M. Platelets recruit human dendritic cells via Mac-1/JAM-C interaction and modulate dendritic cell function in vitro. Arterioscler Thromb Vasc Biol 2007; 27: 1463-70.
92. Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 1999; 59: 1295-300.
93. Kopp HG, Placke T, Salih HR. Platelet-derived transforming growth factor-beta down-regulates NKG2D thereby inhibiting natural killer cell antitumor reactivity. Cancer Res 2009; 69: 7775-83.
94. Heinmoller E, Weinel RJ, Heidtmann HH, Salge U, Seitz R, Schmitz I, Muller KM, Zirngibl H. Studies on tumor-cell-induced platelet aggregation in human lung cancer cell lines. J Cancer Res Clin Oncol 1996; 122: 735-44.
95. Heinmoller E, Schropp T, Kisker O, Simon B, Seitz R, Weinel RJ. Tumor cell-induced platelet aggregation in vitro by human pancreatic cancer cell lines. Scand J Gastroenterol 1995; 30: 1008-16.
96. Burdick MM, Konstantopoulos K. Platelet-induced enhancement of LS174T colon carcinoma and THP-1 monocytoid cell adhesion to vascular endothelium under flow. Am J Physiol Cell Physiol 2004; 287: C539-47.
97. Karpatkin S, Pearlstein E, Ambrogio C, Coller BS. Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest 1988; 81: 1012-9.
98. Jain S, Zuka M, Liu J, Russell S, Dent J, Guerrero JA, Forsyth J, Maruszak B, Gartner TK, Felding-Habermann B, Ware J. Platelet glycoprotein Ib alpha supports experimental lung metastasis. Proc Natl Acad Sci U S A 2007; 104: 9024-8.
99. Labelle M, Begum S, Hynes RO. Direct Signaling between Platelets and Cancer Cells Induces an Epithelial-Mesenchymal-Like Transition and Promotes Metastasis. Cancer Cell 2011; 20: 576-90.
100. Hussong JW, Rodgers GM, Shami PJ. Evidence of increased angiogenesis in patients with acute myeloid leukemia. Blood 2000; 95: 309-13.
101. Perez-Atayde AR, Sallan SE, Tedrow U, Connors S, Allred E, Folkman J. Spectrum of tumor angiogenesis in the bone marrow of children with acute lymphoblastic leukemia. Am J Pathol 1997; 150: 815-21.
102. Lundberg LG, Lerner R, Sundelin P, Rogers R, Folkman J, Palmblad J. Bone marrow in polycythemia vera, chronic myelocytic leukemia, and myelofibrosis has an increased vascularity. Am J Pathol 2000; 157: 15-9.
103. Mesa RA, Hanson CA, Rajkumar SV, Schroeder G, Tefferi A. Evaluation and clinical correlations of bone marrow angiogenesis in myelofibrosis with myeloid metaplasia. Blood 2000; 96: 3374-80.
104. Pruneri G, Bertolini F, Soligo D, Carboni N, Cortelezzi A, Ferrucci PF, Buffa R, Lambertenghi-Deliliers G, Pezzella F. Angiogenesis in myelodysplastic syndromes. Br J Cancer 1999; 81: 1398-401.
105. Vacca A, Ribatti D, Roncali L, Dammacco F. Angiogenesis in B cell lymphoproliferative diseases. Biological and clinical studies. Leuk Lymphoma 1995; 20: 27-38.
106. Shanafelt TD, Kay NE. The clinical and biologic importance of neovascularization and angiogenic signaling pathways in chronic lymphocytic leukemia. Semin Oncol 2006; 33: 174-85.
107. Ghannadan M, Wimazal F, Simonitsch I, Sperr WR, Mayerhofer M, Sillaber C, Hauswirth AW, Gadner H, Chott A, Horny HP, Lechner K, Valent P. Immunohistochemical detection of VEGF in the bone marrow of patients with acute myeloid leukemia. Correlation between VEGF expression and the FAB category. Am J Clin Pathol 2003; 119: 663-71.
108. Dias S, Hattori K, Zhu Z, Heissig B, Choy M, Lane W, Wu Y, Chadburn A, Hyjek E, Gill M, Hicklin DJ, Witte L, Moore MA, Rafii S. Autocrine stimulation of VEGFR-2 activates human leukemic cell growth and migration. J Clin Invest 2000; 106: 511-21.
109. Fragoso R, Pereira T, Wu Y, Zhu Z, Cabecadas J, Dias S. VEGFR-1 (FLT-1) activation modulates acute lymphoblastic leukemia localization and survival within the bone marrow, determining the onset of extramedullary disease. Blood 2006; 107: 1608-16.
110. Veiga JP, Costa LF, Sallan SE, Nadler LM, Cardoso AA. Leukemia-stimulated bone marrow endothelium promotes leukemia cell survival. Exp Hematol 2006; 34: 610-21.
111. Gallay N, Anani L, Lopez A, Colombat P, Binet C, Domenech J, Weksler BB, Malavasi F, Herault O. The role of platelet/endothelial cell adhesion molecule 1 (CD31) and CD38 antigens in marrow microenvironmental retention of acute myelogenous leukemia cells. Cancer Res 2007; 67: 8624-32.
112. Zeng Z, Samudio IJ, Munsell M, An J, Huang Z, Estey E, Andreeff M, Konopleva M. Inhibition of CXCR4 with the novel RCP168 peptide overcomes stroma-mediated chemoresistance in chronic and acute leukemias. Mol Cancer Ther 2006; 5: 3113-21.
113. Paget S. The distribution of secondary growths in cancer of the breast. Lancet 1889; 1: 571-3.
114. Joyce JA, Hanahan D. Multiple roles for cysteine cathepsins in cancer. Cell Cycle 2004; 3: 1516-619.
115. Weigelt B, Bissell MJ. Unraveling the microenvironmental influences on the normal mammary gland and breast cancer. Semin Cancer Biol 2008; 18: 311-21.
116. Gao D, Nolan DJ, Mellick AS, Bambino K, McDonnell K, Mittal V. Endothelial progenitor cells control the angiogenic switch in mouse lung metastasis. Science 2008; 319: 195-8.
117. 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, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438: 820-7.
118. Psaila B, Lyden D. The metastatic niche: adapting the foreign soil. Nat Rev Cancer 2009; 9: 285-93.
119. Mantovani A, Allavena P, Sica A, Balkwill F. Cancer-related inflammation. Nature 2008; 454: 436-44.
120. Sipkins DA, Wei X, Wu JW, Runnels JM, Cote D, Means JK, Luster AD, Scadden DT, Lin CP. In vivo imaging of specialized bone marrow endothelial microdomains for tumour engraftment. Nature 2005; 435: 969-73.
121. Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 2008; 322: 1861-5.
122. Winkelmann M, Stockler J, Grassmuck J, Pfitzer P, Schneider W. Ploidy pattern of megakaryocytes in patients with metastatic tumors with and without paraneoplastic thrombosis and in controls. Haemostasis 1984; 14: 501-7.
123. Sharnoff JG, Kim ES. Evaluation of pulmonary megakaryocytes. AMA Arch Pathol 1958; 66: 176-82.
124. Aabo K, Hansen KB. Megakaryocytes in pulmonary blood vessels. I. Incidence at autopsy, clinicopathological relations especially to disseminated intravascular coagulation. Acta Pathol Microbiol Scand A 1978; 86: 285-91.
125. Soares FA. Increased numbers of pulmonary megakaryocytes in patients with arterial pulmonary tumour embolism and with lung metastases seen at necropsy. J Clin Pathol 1992; 45: 140-2.
126. McGary CT, Miele ME, Welch DR. Highly metastatic 13762NF rat mammary adenocarcinoma cell clones stimulate bone marrow by secretion of granulocyte-macrophage colony-stimulating factor/interleukin-3 activity. Am J Pathol 1995; 147: 1668-81.
127. Bakewell SJ, Nestor P, Prasad S, Tomasson MH, Dowland N, Mehrotra M, Scarborough R, Kanter J, Abe K, Phillips D, Weilbaecher KN. Platelet and osteoclast beta3 integrins are critical for bone metastasis. Proc Natl Acad Sci U S A 2003; 100: 14205-10.
128. Calverley DC, Phang TL, Choudhury QG, Gao B, Oton AB, Weyant MJ, Geraci MW. Significant downregulation of platelet gene expression in metastatic lung cancer. Clin Transl Sci 2010; 3: 227-32.
129. Toksoz D, Zsebo KM, Smith KA, Hu S, Brankow D, Suggs SV, Martin FH, Williams DA. Support of human hematopoiesis in long-term bone marrow cultures by murine stromal cells selectively expressing the membrane-bound and secreted forms of the human homolog of the steel gene product, stem cell factor. Proc Natl Acad Sci U S A 1992; 89: 7350-4.
130. Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 2002; 195: 1145-54.
131. Broxmeyer HE, Hangoc G, Cooper S, Campbell T, Ito S, Mantel C. AMD3100 and CD26 modulate mobilization, engraftment, and survival of hematopoietic stem and progenitor cells mediated by the SDF-1/CXCL12-CXCR4 axis. Ann N Y Acad Sci 2007; 1106: 1-19.
132. Asahara T, Chen D, Takahashi T, Fujikawa K, Kearney M, Magner M, Yancopoulos GD, Isner JM. Tie2 receptor ligands, angiopoietin-1 and angiopoietin-2, modulate VEGF-induced postnatal neovascularization. Circ Res 1998; 83: 233-40.
133. Qian H, Buza-Vidas N, Hyland CD, Jensen CT, Antonchuk J, Mansson R, Thoren LA, Ekblom M, Alexander WS, Jacobsen SE. Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell 2007; 1: 671-84.
134. Bord S, Frith E, Ireland DC, Scott MA, Craig JI, Compston JE. Synthesis of osteoprotegerin and RANKL by megakaryocytes is modulated by oestrogen. Br J Haematol 2004; 126: 244-51.
135. Nachman RL, Rafii S. Platelets, petechiae, and preservation of the vascular wall. N Engl J Med 2008; 359: 1261-70.
136. Lambert MP, Rauova L, Bailey M, Sola-Visner MC, Kowalska MA, Poncz M. Platelet factor 4 is a negative autocrine in vivo regulator of megakaryopoiesis: clinical and therapeutic implications. Blood 2007; 110: 1153-60.
137. Akhurst RJ, Derynck R. TGF-beta signaling in cancer - a double-edged sword. Trends Cell Biol 2001; 11: S44-51.
138. Kolber DL, Knisely TL, Maione TE. Inhibition of development of murine melanoma lung metastases by systemic administration of recombinant platelet factor 4. J Natl Cancer Inst 1995; 87: 304-9.
139. Sharpe RJ, Byers HR, Scott CF, Bauer SI, Maione TE. Growth inhibition of murine melanoma and human colon carcinoma by recombinant human platelet factor 4. J Natl Cancer Inst 1990; 82: 848-53.
140. Tanaka T, Manome Y, Wen P, Kufe DW, Fine HA. Viral vector-mediated transduction of a modified platelet factor 4 cDNA inhibits angiogenesis and tumor growth. Nat Med 1997; 3: 437-42.
141. Gupta SK, Singh JP. Inhibition of endothelial cell proliferation by platelet factor-4 involves a unique action on S phase progression. J Cell Biol 1994; 127: 1121-7.
142. Gentilini G, Kirschbaum NE, Augustine JA, Aster RH, Visentin GP. Inhibition of human umbilical vein endothelial cell proliferation by the CXC chemokine, platelet factor 4 (PF4), is associated with impaired downregulation of p21(Cip1/WAF1). Blood 1999; 93: 25-33.
143. Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol 1997; 138: 707-17.
144. Lawler J, Miao WM, Duquette M, Bouck N, Bronson RT, Hynes RO. Thrombospondin-1 gene expression affects survival and tumor spectrum of p53-deficient mice. Am J Pathol 2001; 159: 1949-56.
145. Brown LF, Guidi AJ, Schnitt SJ, van de Water L, Iruela-Arispe ML, Yeo TK, Tognazzi K, Dvorak HF. Vascular stroma formation in carcinoma in situ, invasive carcinoma, and metastatic carcinoma of the breast. Clin Cancer Res 1999; 5: 1041-56.
146. Bertin N, Clezardin P, Kubiak R, Frappart L. Thrombospondin-1 and -2 messenger RNA expression in normal, benign, and neoplastic human breast tissues: correlation with prognostic factors, tumor angiogenesis, and fibroblastic desmoplasia. Cancer Res 1997; 57: 396-9.
147. Tuszynski GP, Gasic TB, Rothman VL, Knudsen KA, Gasic GJ. Thrombospondin, a potentiator of tumor cell metastasis. Cancer Res 1987; 47: 4130-3.
148. Yee KO, Connolly CM, Duquette M, Kazerounian S, Washington R, Lawler J. The effect of thrombospondin-1 on breast cancer metastasis. Breast Cancer Res Treat 2009; 114: 85-96.
149. Taraboletti G, Roberts DD, Liotta LA. Thrombospondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains. J Cell Biol 1987; 105: 2409-15.
150. Ko HM, Kang JH, Jung B, Kim HA, Park SJ, Kim KJ, Kang YR, Lee HK, Im SY. Critical role for matrix metalloproteinase-9 in platelet-activating factor-induced experimental tumor metastasis. Int J Cancer 2007; 120: 1277-83.
151. Caunt M, Hu L, Tang T, Brooks PC, Ibrahim S, Karpatkin S. Growth-regulated oncogene is pivotal in thrombin-induced angiogenesis. Cancer Res 2006; 66: 4125-32.
152. Hu L, Roth JM, Brooks P, Luty J, Karpatkin S. Thrombin up-regulates cathepsin D which enhances angiogenesis, growth, and metastasis. Cancer Res 2008; 68: 4666-73.
153. Hu L, Roth JM, Brooks P, Ibrahim S, Karpatkin S. Twist is required for thrombin-induced tumor angiogenesis and growth. Cancer Res 2008; 68: 4296-302.
154. Mueller BM, Reisfeld RA, Edgington TS, Ruf W. Expression of tissue factor by melanoma cells promotes efficient hematogenous metastasis. Proc Natl Acad Sci U S A 1992; 89: 11832-6.
155. Fischer EG, Ruf W, Mueller BM. Tissue factor-initiated thrombin generation activates the signaling thrombin receptor on malignant melanoma cells. Cancer Res 1995; 55: 1629-32.
156. Paik JH, Skoura A, Chae SS, Cowan AE, Han DK, Proia RL, Hla T. Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization. Genes Dev 2004; 18: 2392-403.
157. Brill A, Dashevsky O, Rivo J, Gozal Y, Varon D. Platelet-derived microparticles induce angiogenesis and stimulate post-ischemic revascularization. Cardiovasc Res 2005; 67: 30-8.
158. Boucharaba A, Guillet B, Menaa F, Hneino M, van Wijnen AJ, Philippe C, Oliver P. Bioactive lipids lysophosphatidic acid and sphingosine 1-phosphate mediate breast cancer cell biological functions through distinct mechanisms. Oncol Res 2009; 18: 173-84.