Thrombospondins deployed by thrombopoietic cells determine angiogenic switch and extent of revascularization

Journal of Clinical Investigation

Volumn 116, Issue 12, 2006, Pages 3277-3291

  Kopp, Hans Georg ^a,b   Hooper, Andrea T ^a   Broekman, M Johan ^c   Avecilla, Scott T ^a   Petit, Isabelle ^a   Luo, Min ^c   Milde, Till ^a   Ramos, Carlos A ^d   Zhang, Fan ^a   Kopp, Tabitha ^a   Bornstein, Paul ^e   Jin, David K ^a   Marcus, Aaron J ^c   Rafii, Shahin ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c WMCCU   (United States)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENIC FACTOR; GELATINASE B; STROMAL CELL DERIVED FACTOR 1; THROMBOSPONDIN; THROMBOSPONDIN 1; THROMBOSPONDIN 2;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ARTICLE; BONE MARROW SUPPRESSION; CONTROLLED STUDY; LIMB ISCHEMIA; MEGAKARYOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVASCULARIZATION; THROMBOCYTE FUNCTION; THROMBOCYTOPOIESIS;

ANIMALS; BLOOD PLATELETS; BONE MARROW; CHEMOKINES, CXC; HEMATOPOIETIC STEM CELLS; HINDLIMB; ISCHEMIA; MEGAKARYOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; STILBENES; THROMBOPOIESIS; THROMBOPOIETIN; THROMBOSPONDIN 1; THROMBOSPONDINS;

EID: 33845314302     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI29314     Document Type: Article

References (68)

1. Billroth, T. 1878. Lectures on surgical pathology and therapeutics. A handbook for students and practitioners. New Syndenham Society. London, United Kingdom. 355 pp.
2. Honn, K.V., Tang, D.G., and Crissman, J.D. 1992. Platelets and cancer metastasis: a causal relationship? Cancer Metastasis Rev. 11:325-351.
3. Sierko, E., and Wojtukiewicz, M.Z. 2004. Platelets and angiogenesis in malignancy. Semin. Thromb. Hemost. 30:95-108.
4. Rhee, J.S., et al. 2004. The functional role of blood platelet components in angiogenesis. Thromb. Haemost. 92:394-402.
5. Mohle, R., Green, D., Moore, M.A., Nachman, R.L., and Rafii, S. 1997. Constitutive production and thrombin-induced release of vascular endothelial growth factor by human megakaryocytes and platelets. Proc. Natl. Acad. Sci. U. S. A. 94:663-668.
6. Pintucci, G., et al. 2002. Trophic effects of platelets on cultured endothelial cells are mediated by platelet-associated fibroblast growth factor-2 (FGF-2) and vascular endothelial growth factor (VEGF). Thromb. Haemost. 88:834-842.
7. Fernandez-Patron, C., et al. 1999. Differential regulation of platelet aggregation by matrix metalloproteinases-9 and -2. Thromb. Haemost. 82:1730-1735.
8. Amano, H., Hackett, N.R., Rafii, S., and Crystal, R.G. 2005. Thrombopoietin gene transfer-mediated enhancement of angiogenic responses to acute ischemia. Circ. Res. 97:337-345.
9. Verheul, H.M., et al. 1997. Platelet: transporter of vascular endothelial growth factor. Clin. Cancer Res. 3:2187-2190.
10. English, D., et al. 2000. Sphingosine 1-phosphate released from platelets during clotting accounts for the potent endothelial cell chemotactic activity of blood serum and provides a novel link between hemostasis and angiogenesis. FASEB J. 14:2255-2265.
11. English, D., Garcia, J.G., and Brindley, D.N. 2001. Platelet-released phospholipids link haemostasis and angiogenesis. Cardiovasc. Res. 49:588-599.
12. Pipili-Synetos, E., Papadimitriou, E., and Maragoudakis, M.E. 1998. Evidence that platelets promote tube formation by endothelial cells on matrigel. Br. J. Pharmacol. 125:1252-1257.
13. Gasic, G.J., Gasic, T.B., and Stewart, C.C. 1968. Antimetastatic effects associated with platelet reduction. Proc. Natl. Acad. Sci. U. S. A. 61:46-52.
14. Amirkhosravi, A., et al. 2003. Inhibition of tumor cell-induced platelet aggregation and lung metastasis by the oral GpIIb/IIIa antagonist XV454. Thromb. Haemost. 90:549-554.
15. Varner, J.A., Nakada, M.T., Jordan, R.E., and Coller, B.S. 1999. Inhibition of angiogenesis and tumor growth by murine 7E3, the parent antibody of c7E3 Fab (abciximab; ReoPro). Angiogenesis. 3:53-60.
16. Falanga, A., and Piccioli, A. 2005. Effect of anticoagulant drugs in cancer. Curr. Opin. Pulm. Med. 11:403-407.
17. Kisucka, J., et al. 2006. Platelets and platelet adhesion support angiogenesis while preventing excessive hemorrhage. Proc. Natl. Acad. Sci. U. S. A. 103:855-860.
18. Maione, T.E., et al. 1990. Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science. 247:77-79.
19. Iruela-Arispe, M.L., Bornstein, P., and Sage, H. 1991. Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cells in vitro. Proc. Natl. Acad. Sci. U. S. A. 88:5026-5030.
20. Baenziger, N.L., Brodie, G.N., and Majerus, P.W. 1971. A thrombin-sensitive protein of human platelet membranes. Proc. Natl. Acad. Sci. U. S. A. 68:240-243.
21. Lawler, J. 1986. The structural and functional properties of thrombospondin. Blood. 67:1197-1209.
22. Good, D.J., et al. 1990. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc. Natl. Acad. Sci. U. S. A. 87:6624-6628.
23. Bornstein, P., Devarayalu, S., Li, P., Disteche, C.M., and Framson, P. 1991. A second thrombospondin gene in the mouse is similar in organization to thrombospondin 1 but does not respond to serum. Proc. Natl. Acad. Sci. U. S. A. 88:8636-8640.
24. Adams, J.C., and Lawler, J. 2004. The thrombospondins. Int. J. Biochem. Cell Biol. 36:961-968.
25. Bornstein, P. 2001. Thrombospondins as matricellular modulators of cell function. J. Clin. Invest. 107:929-934.
26. Chen, H., Herndon, M.E., and Lawler, J. 2000. The cell biology of thrombospondin-1. Matrix Biol. 19:597-614.
27. Lawler, J. 2002. Thrombospondin-1 as an endogenous inhibitor of angiogenesis and tumor growth. J. Cell. Mol. Med. 6:1-12.
28. Murphy-Ullrich, J.E., and Poczatek, M. 2000. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor Rev. 11:59-69.
29. Rodriguez-Manzaneque, J.C., et al. 2001. Thrombospondin-1 suppresses spontaneous tumor growth and inhibits activation of matrix metalloproteinase-9 and mobilization of vascular endothelial growth factor. Proc. Natl. Acad. Sci. U. S. A. 98:12485-12490.
30. Yao, L., et al. 2000. Thrombospondin-1 expression in oral squamous cell carcinomas: correlations with tumor vascularity, clinicopathological features and survival. Oral Oncol. 36:539-544.
31. Bleuel, K., Popp, S., Fusenig, N.E., Stanbridge, E.J., and Boukamp, P. 1999. Tumor suppression in human skin carcinoma cells by chromosome 15 transfer or thrombospondin-1 overexpression through halted tumor vascularization. Proc. Natl. Acad. Sci. U. S. A. 96:2065-2070.
32. Clezardin, P., Frappart, L., Clerget, M., Pechoux, C., and Delmas, P.D. 1993. Expression of thrombospondin (TSP1) and its receptors (CD36 and CD51) in normal, hyperplastic, and neoplastic human breast. Cancer Res. 53:1421-1430.
33. Coppinger, J.A., et al. 2004. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood. 103:2096-2104.
34. Ishida-Yamamoto, A., et al. 2000. Decreased deiminated keratin K1 in psoriatic hyperproliferative epidermis. J. Invest. Dermatol. 114:701-705.
35. Kopp, H.G., et al. 2005. Tie2 activation contributes to hemangiogenic regeneration after myelosuppression. Blood. 106:505-513.
36. Chen, Y.Z., et al. 1997. Thrombospondin, a negative modulator of megakaryocytopoiesis. J. Lab. Clin. Med. 129:231-238.
37. Avecilla, S.T., et al. 2004. Chemokine-mediated interaction of hematopoietic progenitors with the bone marrow vascular niche is required for thrombopoiesis. Nat. Med. 10:64-71.
38. Radley, J.M., Hodgson, G.S., and Levin, J. 1980. Platelet production after administration of antiplatelet serum and 5-fluorouracil. Blood. 55:164-166.
39. Chenaille, P.J., Steward, S.A., Ashmun, R.A., and Jackson, C.W. 1990. Prolonged thrombocytosis in mice after 5-fluorouracil results from failure to down-regulate megakaryocyte concentration. An experimental model that dissociates regulation of megakaryocyte size and DNA content from megakaryocyte concentration. Blood. 76:508-515.
40. Ebbe, S., Yee, T., and Phalen, E. 1989. 5-fluorouracil-induced thrombocytosis in mice is independent of the spleen and can be partially reproduced by repeated doses of cytosine arabinoside. Exp. Hematol. 17:822-826.
41. Kopp, H.G., Avecilla, S.T., Hooper, A.T., and Rafii, S. 2005. The bone marrow vascular niche: home of HSC differentiation and mobilization. Physiology (Bethesda). 20:349-356.
42. Han, Z.C., and Caen, J.P. 1993. Are megakaryocytes and endothelial cells sisters? J. Lab. Clin. Med. 121:821-825.
43. Fliedner, T.M., Graessle, D., Paulsen, C., and Reimers, K. 2002. Structure and function of bone marrow hemopoiesis: mechanisms of response to ionizing radiation exposure. Cancer Biother. Radiopharm. 17:405-426.
44. Vincent, L., et al. 2005. Combretastatin A4 phosphate induces rapid regression of tumor neovessels and growth through interference with vascular endothelial-cadherin signaling. J. Clin. Invest. 115:2992-3006. doi:10.1172/JCI24586.
45. Jin, D.K., et al. 2006. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4(+) hemangiocytes. Nat. Med. 12:557-567.
46. Bornstein, P., Agah, A., and Kyriakides, T.R. 2004. The role of thrombospondins 1 and 2 in the regulation of cell-matrix interactions, collagen fibril formation, and the response to injury. Int. J. Biochem. Cell Biol. 36:1115-1125.
47. Shaw, T., Chesterman, C.N., and Morgan, F.J. 1984. In vitro synthesis of low molecular weight proteins in human platelets: absence of labelled release products. Thromb. Res. 36:619-631.
48. McRedmond, J.P., et al. 2004. Integration of proteomics and genomics in platelets: a profile of platelet proteins and platelet-specific genes. Mol. Cell. Proteomics. 3:133-144.
49. Kieffer, N., Guichard, J., Farcet, J.P., Vainchenker, W., and Breton-Gorius, J. 1987. Biosynthesis of major platelet proteins in human blood platelets. Eur. J. Biochem. 164:189-195.
50. Jackson, K.A., Snyder, D.S., and Goodell, M.A. 2004. Skeletal muscle fiber-specific green autofluorescence: potential for stem cell engraftment artifacts. Stem Cells. 22:180-187.
51. Yamaguchi, J., et al. 2003. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization. Circulation. 107:1322-1328.
52. Salcedo, R., et al. 1999. Vascular endothelial growth factor and basic fibroblast growth factor induce expression of CXCR4 on human endothelial cells: in vivo neovascularization induced by stromal-derived factor-1alpha. Am. J. Pathol. 154:1125-1135.
53. Grunewald, M., et al. 2006. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell. 124:175-189.
54. Jurasz, P., Chung, A.W., Radomski, A., and Radomski, M.W. 2002. Nonremodeling properties of matrix metalloproteinases: the platelet connection. Circ. Res. 90:1041-1043.
55. Lane, W.J., et al. 2000. Stromal-derived factor 1-induced megakaryocyte migration and platelet production is dependent on matrix metalloproteinases. Blood. 96:4152-4159.
56. Bein, K., and Simons, M. 2000. Thrombospondin type 1 repeats interact with matrix metalloproteinase 2. Regulation of metalloproteinase activity. J. Biol. Chem. 275:32167-32173.
57. Massberg, S., et al. 2006. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J. Exp. Med. 203:1221-1233.
58. Hankenson, K.D., and Bornstein, P. 2002. The secreted protein thrombospondin 2 is an autocrine inhibitor of marrow stromal cell proliferation. J. Bone Miner. Res. 17:415-425.
59. Kyriakides, T.R., et al. 2003. Megakaryocytes require thrombospondin-2 for normal platelet formation and function. Blood. 101:3915-3923.
60. Brill, A., Dashevsky, O., Rivo, J., Gozal, Y., and Varon, D. 2005. Platelet-derived microparticles induce angiogenesis and stimulate post-ischemic revascularization. Cardiovasc. Res. 67:30-38.
61. Lawler, J., et al. 1998. Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia. J. Clin. Invest. 101:982-992.
62. Kyriakides, T.R., et al. 1998. Mice that lack thrombospondin 2 display connective tissue abnormalities that are associated with disordered collagen fibrillogenesis, an increased vascular density, and a bleeding diathesis. J. Cell Biol. 140:419-430.
63. Slayton, W.B., et al. 2002. The spleen is a major site of megakaryopoiesis following transplantation of murine hematopoietic stem cells. Blood. 100:3975-3982.
64. Lehr, H.A., van der Loos, C.M., Teeling, P., and Gown, A.M. 1999. Complete chromogen separation and analysis in double immunohistochemical stains using Photoshop-based image analysis. J. Histochem. Cytochem. 47:119-126.
65. Marcus, A.J., et al. 1991. Inhibition of platelet function by an aspirin-insensitive endothelial cell ADPase. Thromboregulation by endothelial cells. J. Clin. Invest. 88:1690-1696.
66. Santos, M.T., et al. 1991. Enhancement of platelet reactivity and modulation of eicosanoid production by intact erythrocytes. A new approach to platelet activation and recruitment. J. Clin. Invest. 87:571-580.
67. Drosopoulos, J.H., et al. 2000. Site-directed mutagenesis of human endothelial cell ecto-ADPase/soluble CD39: requirement of glutamate 174 and serine 218 for enzyme activity and inhibition of platelet recruitment. Biochemistry. 39:6936-6943.
68. Semerad, C.L., et al. 2005. G-CSF potently inhibits osteoblast activity and CXCL12 mRNA expression in the bone marrow. Blood. 106:3020-3027.