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Blood, Vol. 93 No. 9 (May 1), 1999: pp. 3064-3073

Bone Marrow Neovascularization, Plasma Cell Angiogenic Potential, and Matrix Metalloproteinase-2 Secretion Parallel Progression of Human Multiple Myeloma

Angelo Vacca, Domenico Ribatti, Marco Presta, Monica Minischetti, Monica Iurlaro, Roberto Ria, Adriana Albini, Federico Bussolino, and Franco Dammacco

From the Department of Biomedical Sciences and Human Oncology, and the Institute of Human Anatomy, Histology and Embryology, School of Medicine, University of Bari, Bari; the Department of Biomedical Sciences and Biotechnology, School of Medicine, University of Brescia, Brescia; Advanced Biotechnology Center, National Institute for Cancer Research, Genova; and the Institute for Cancer Research and Treatment (IRCC), School of Medicine, University of Torino, Torino, Italy.

To assess whether the progression of plasma cell tumors is accompanied by angiogenesis and secretion of matrix-degrading enzymes, bone marrow biopsy specimens from 20 patients with monoclonal gammopathy of undetermined significance (MGUS), 18 patients with nonactive multiple myeloma (MM), and 26 patients with active MM were evaluated for their angiogenic potential and matrix-metalloproteinase (MMP) production. A fivefold increase of the factor VIII+ microvessel area was measured by a planimetric method of point counting in the bone marrow of patients with active MM as compared with nonactive MM and MGUS patients (P < .01). When serum-free conditioned media (CM) of plasma cells isolated from the bone marrow of each patient were tested in vivo for their angiogenic activity in the chick embryo chorioallantoic membrane (CAM) assay, the incidence of angiogenic samples was significantly higher (P < .01) in the active MM group (76%) compared with nonactive MM (33%) and MGUS (20%) groups. Moreover, a linear correlation (P < .01) was found between the extent of vascularization of the bone marrow of a given patient and the angiogenic activity exerted in the CAM assay by the plasma cells isolated from the same bone marrow. In vitro, a significantly higher fraction of the plasma cell CM samples from the active MM group stimulated human umbilical vein endothelial cell (HUVEC) proliferation (53%, P < .01), migration (42%, P < .05), and/or monocyte chemotaxis (38%, P < .05) when compared with nonactive MM and MGUS groups (ranging between 5% and 15% of the samples). Also, immunoassay of plasma cell extracts showed significantly higher (P < .01) levels of the angiogenic basic fibroblast growth factor (FGF)-2 in the active MM patients than in nonactive MM and MGUS patients (153 ± 59, 23 ± 17, and 31 ± 18 pg FGF-2/100 µg of protein, respectively). Accordingly, neutralizing anti-FGF-2 antibody caused a significant inhibition (ranging from 54% to 68%) of the biological activity exerted on cultured endothelial cells and in the CAM assay by plasma cell CM samples from active MM patients. Finally, in situ hybridization of bone marrow plasma cells and gelatin-zymography of their CM showed that active MM patients express significantly higher (P < .01) levels of MMP-2 mRNA and protein when compared with nonactive MM and MGUS patients, whereas MMP-9 expression was similar in all groups. Taken together, these findings indicate that the progression of plasma cell tumors is accompanied by an increase of bone marrow neovascularization. This is paralleled by an increased angiogenic and invasive potential of bone marrow plasma cells, which is dependent, at least in part, by FGF-2 and MMP-2 production. Induction of angiogenesis and secretion of MMPs by plasma cells in active disease may play a role in their medullary and extramedullary dissemination, raising the hypothesis that angiostatic/anti-MMP agents may be used for therapy of MM.


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K. Neben, T. Moehler, G. Egerer, A. Kraemer, J. Hillengass, A. Benner, A. D. Ho, and H. Goldschmidt
High Plasma Basic Fibroblast Growth Factor Concentration Is Associated with Response to Thalidomide in Progressive Multiple Myeloma
Clin. Cancer Res., September 1, 2001; 7(9): 2675 - 2681.
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J. De Vos, G. Couderc, K. Tarte, M. Jourdan, G. Requirand, M.-C. Delteil, J.-F. Rossi, N. Mechti, and B. Klein
Identifying intercellular signaling genes expressed in malignant plasma cells by using complementary DNA arrays
Blood, August 1, 2001; 98(3): 771 - 780.
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K. Podar, Y.-T. Tai, F. E. Davies, S. Lentzsch, M. Sattler, T. Hideshima, B. K. Lin, D. Gupta, Y. Shima, D. Chauhan, et al.
Vascular endothelial growth factor triggers signaling cascades mediating multiple myeloma cell growth and migration
Blood, July 15, 2001; 98(2): 428 - 435.
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JCOHome page
O. Sezer, C. Jakob, K. Niemoller, R. T.P. Poon, S.-T. Fan, and J. Wong
Angiogenesis in Cancer
J. Clin. Oncol., July 1, 2001; 19(13): 3299 - 3301.
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Cancer Res.Home page
L. Sun, M. Vitolo, and A. Passaniti
Runt-related Gene 2 in Endothelial Cells: Inducible Expression and Specific Regulation of Cell Migration and Invasion
Cancer Res., July 1, 2001; 61(13): 4994 - 5001.
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Cancer Res.Home page
T. Hideshima, P. Richardson, D. Chauhan, V. J. Palombella, P. J. Elliott, J. Adams, and K. C. Anderson
The Proteasome Inhibitor PS-341 Inhibits Growth, Induces Apoptosis, and Overcomes Drug Resistance in Human Multiple Myeloma Cells
Cancer Res., April 1, 2001; 61(7): 3071 - 3076.
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JCOHome page
K. D. Miller, C. J. Sweeney, and G. W. Sledge Jr
Redefining the Target: Chemotherapeutics as Antiangiogenics
J. Clin. Oncol., February 15, 2001; 19(4): 1195 - 1206.
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W. S. Dalton, P. L. Bergsagel, W. M. Kuehl, K. C. Anderson, and J. L. Harousseau
Multiple Myeloma
Hematology, January 1, 2001; 2001(1): 157 - 177.
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R. J. Klasa, A. F. List, and B. D. Cheson
Rational Approaches to Design of Therapeutics Targeting Molecular Markers
Hematology, January 1, 2001; 2001(1): 443 - 462.
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R. A. Mesa, C. A. Hanson, S. V. Rajkumar, G. Schroeder, and A. Tefferi
Evaluation and clinical correlations of bone marrow angiogenesis in myelofibrosis with myeloid metaplasia
Blood, November 15, 2000; 96(10): 3374 - 3380.
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T. Hideshima, D. Chauhan, Y. Shima, N. Raje, F. E. Davies, Y.-T. Tai, S. P. Treon, B. Lin, R. L. Schlossman, P. Richardson, et al.
Thalidomide and its analogs overcome drug resistance of human multiple myeloma cells to conventional therapy
Blood, November 1, 2000; 96(9): 2943 - 2950.
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M. A. Dimopoulos, L. A. Moulopoulos, A. Maniatis, and R. Alexanian
Solitary plasmacytoma of bone and asymptomatic multiple myeloma
Blood, September 15, 2000; 96(6): 2037 - 2044.
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Am. J. Pathol.Home page
L. G. Lundberg, R. Lerner, P. Sundelin, R. Rogers, J. Folkman, and J. Palmblad
Bone Marrow in Polycythemia Vera, Chronic Myelocytic Leukemia, and Myelofibrosis Has an Increased Vascularity
Am. J. Pathol., July 1, 2000; 157(1): 15 - 19.
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F. Bertolini, L. Fusetti, P. Mancuso, A. Gobbi, C. Corsini, P. F. Ferrucci, G. Martinelli, and G. Pruneri
Endostatin, an antiangiogenic drug, induces tumor stabilization after chemotherapy or anti-CD20 therapy in a NOD/SCID mouse model of human high-grade non-Hodgkin lymphoma
Blood, July 1, 2000; 96(1): 282 - 287.
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Cancer Res.Home page
L. Fusetti, G. Pruneri, A. Gobbi, C. Rabascio, N. Carboni, F. Peccatori, G. Martinelli, and F. Bertolini
Human Myeloid and Lymphoid Malignancies in the Non-Obese Diabetic/Severe Combined Immunodeficiency Mouse Model: Frequency of Apoptotic Cells in Solid Tumors and Efficiency and Speed of Engraftment Correlate with Vascular Endothelial Growth Factor Production
Cancer Res., May 1, 2000; 60(9): 2527 - 2534.
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B. Dankbar, T. Padro, R. Leo, B. Feldmann, M. Kropff, R. M. Mesters, H. Serve, W. E. Berdel, and J. Kienast
Vascular endothelial growth factor and interleukin-6 in paracrine tumor-stromal cell interactions in multiple myeloma
Blood, April 15, 2000; 95(8): 2630 - 2636.
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T. Padro, S. Ruiz, R. Bieker, H. Burger, M. Steins, J. Kienast, T. Buchner, W. E. Berdel, and R. M. Mesters
Increased angiogenesis in the bone marrow of patients with acute myeloid leukemia
Blood, April 15, 2000; 95(8): 2637 - 2644.
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Proc. Natl. Acad. Sci. USAHome page
J. Fang, Y. Shing, D. Wiederschain, L. Yan, C. Butterfield, G. Jackson, J. Harper, G. Tamvakopoulos, and M. A. Moses
Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model
PNAS, April 11, 2000; 97(8): 3884 - 3889.
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A. Vacca, M. Iurlaro, D. Ribatti, M. Minischetti, B. Nico, R. Ria, A. Pellegrino, and F. Dammacco
Antiangiogenesis Is Produced by Nontoxic Doses of Vinblastine
Blood, December 15, 1999; 94(12): 4143 - 4155.
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NEJMHome page
S. Singhal, J. Mehta, R. Desikan, D. Ayers, P. Roberson, P. Eddlemon, N. Munshi, E. Anaissie, C. Wilson, M. Dhodapkar, et al.
Antitumor Activity of Thalidomide in Refractory Multiple Myeloma
N. Engl. J. Med., November 18, 1999; 341(21): 1565 - 1571.
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NEJMHome page
N. Raje and K. Anderson
Thalidomide -- A Revival Story
N. Engl. J. Med., November 18, 1999; 341(21): 1606 - 1609.
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