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PMID: 14524530 Published · ppublish English Journal Article

Inhibition of alpha(v)beta3 integrin reduces angiogenesis, bone turnover, and tumor cell proliferation in experimental prostate cancer bone metastases.

Clinical & experimental metastasis ·Vol. 20 ·No. 5 ·2003-00-00 ·Pages 413-20

Nemeth JA, Cher ML, Zhou Z, Mullins C, Bhagat S, Trikha M

Abstract

The growth of metastatic prostate cancer cells in the bone involves an intimate interaction between the tumor cells and various elements of the bone microenvironment, resulting in increased rate of bone turnover and rapid tumor growth. The alpha(v)beta3 integrin has been shown to play an important role in tumor growth and angiogenesis, and is known to be critical to osteoclast formation and activity. This study was designed to examine the role of alpha(v)beta3 expressed by cells native to the bone in the growth and pathogenesis of prostate cancer bone metastases. Human prostate cancer cells which do not express alpha(v)beta3 or alpha(IIb)beta3 integrins were injected directly into human bone fragments previously implanted subcutaneously in SCID mice (SCID-human-bone model). At the same time treatment with anti-beta3 antibody fragment (m7E3 F(ab')2) i.p. at 300 microg/dose 3 x per week was initiated and continued for 2 weeks. In this system, m7E3 F(ab')2 only recognizes human bone-derived alpha(v)beta3. Antibody inhibition of alpha(v)beta3 integrin in vivo resulted in a specific reduction in the proportion of antigenically-human blood vessels within tumor-bearing bone implants (from 73.5% +/- 3.93 in controls to 17.74% +/- 5.64 in treated animals). Proliferation of the alpha(v)beta3-negative tumor cells was also reduced, although the overall vessel density was maintained by compensating mouse vasculature. Blockage of human bone-derived alpha(v)beta3 also significantly reduced the recruitment of osteoclasts in response to tumor cells, as well as degradation of calcified bone tissue. Together these observations confirm the importance of alpha(v)beta3 in bone metabolism and angiogenesis, and point to the role of these processes in controlling growth of metastatic prostate cancer cells in the bone.

MeSH Terms
Animals Apoptosis Bone Neoplasms/pathology Bone and Bones/metabolism Cell Division Flow Cytometry Humans Immunohistochemistry Integrin alphaVbeta3/antagonists & inhibitors Male Mice Mice, SCID Microscopy, Fluorescence Neoplasm Metastasis Neovascularization, Pathologic Osteoclasts/metabolism Prostatic Neoplasms/pathology Tumor Cells, Cultured
Chemicals
Integrin alphaVbeta3
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Nemeth Jeffrey A
Department of Oncology Research, Centocor, Inc., Malvern, Pennsylvania 19355, USA.
Cher Michael L
Zhou Zhao
Mullins Chadwick
Bhagat Sunita
Trikha Mohit
References (51)
51 references, click to expand
  1. Requirement of vascular integrin alpha v beta 3 for angiogenesis.
    Science. 1994 Apr 22;264(5158):569-71 PMID: 7512751
  2. Differential expression of alpha 6 and alpha 2 very late antigen integrins in the normal, hyperplastic, and neoplastic prostate: simultaneous demonstration of cell surface receptors and their extracellular ligands.
    Hum Pathol. 1993 Mar;24(3):243-8 PMID: 7681030
  3. Human prostate carcinoma cells express functional alphaIIb(beta)3 integrin.
    Cancer Res. 1996 Nov 1;56(21):5071-8 PMID: 8895766
  4. Adhesion molecules, extracellular matrix, and proteases in prostate carcinoma.
    J Cell Biochem Suppl. 1994;19:232-7 PMID: 7823596
  5. The osteoclast functional antigen, implicated in the regulation of bone resorption, is biochemically related to the vitronectin receptor.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1817-26 PMID: 2477382
  6. Origin of osteoclasts: mature monocytes and macrophages are capable of differentiating into osteoclasts under a suitable microenvironment prepared by bone marrow-derived stromal cells.
    Proc Natl Acad Sci U S A. 1990 Sep;87(18):7260-4 PMID: 2169622
  7. Stimulation of human prostate cancer cell lines by factors present in human osteoblast-like cells but not in bone marrow.
    Prostate. 1995 Nov;27(5):287-93 PMID: 7479396
  8. The clinical manipulation of angiogenesis: pathology, side-effects, surprises, and opportunities with novel human therapies.
    J Pathol. 2000 Feb;190(3):330-7 PMID: 10685066
  9. Multiple roles for platelet GPIIb/IIIa and alphavbeta3 integrins in tumor growth, angiogenesis, and metastasis.
    Cancer Res. 2002 May 15;62(10):2824-33 PMID: 12019160
  10. Arg-Gly-Asp (RGD) peptides and the anti-vitronectin receptor antibody 23C6 inhibit dentine resorption and cell spreading by osteoclasts.
    Exp Cell Res. 1991 Aug;195(2):368-75 PMID: 1712731
  11. A peptidomimetic antagonist of the alpha(v)beta3 integrin inhibits bone resorption in vitro and prevents osteoporosis in vivo.
    J Clin Invest. 1997 May 1;99(9):2284-92 PMID: 9151803
  12. Prostatic carcinoma cell migration via alpha(v)beta3 integrin is modulated by a focal adhesion kinase pathway.
    Cancer Res. 1999 Apr 1;59(7):1655-64 PMID: 10197643
  13. Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation.
    Pharmacol Rev. 2000 Jun;52(2):237-68 PMID: 10835101
  14. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis.
    Prostate. 2000 Jul 1;44(2):91-103 Jul 1;44(2) PMID: 10881018
  15. Abciximab (ReoPro, chimeric 7E3 Fab) demonstrates equivalent affinity and functional blockade of glycoprotein IIb/IIIa and alpha(v)beta3 integrins.
    Circulation. 1998 Sep 15;98(11):1085-91 PMID: 9736595
  16. The role of alphav integrins during angiogenesis: insights into potential mechanisms of action and clinical development.
    J Clin Invest. 1999 May;103(9):1227-30 PMID: 10225964
  17. Integrin expression and usage by prostate cancer cell lines on laminin substrata.
    Cell Growth Differ. 2001 Feb;12(2):99-107 PMID: 11243469
  18. Perspectives: adhesion receptors in bone.
    J Bone Miner Res. 1989 Dec;4(6):803-8 PMID: 2481941
  19. Echistatin is a potent inhibitor of bone resorption in culture.
    J Cell Biol. 1990 Oct;111(4):1713-23 PMID: 2211834
  20. Differential expression of extracellular matrix molecules and the alpha 6-integrins in the normal and neoplastic prostate.
    Am J Pathol. 1994 Jul;145(1):167-74 PMID: 8030747
  21. Integrin alpha v beta 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels.
    Cell. 1994 Dec 30;79(7):1157-64 PMID: 7528107
  22. Persistence of human vascular endothelium in experimental human prostate cancer bone tumors.
    Clin Exp Metastasis. 2000;18(3):231-7 PMID: 11315096
  23. Integrins and cancer.
    Curr Opin Cell Biol. 1996 Oct;8(5):724-30 PMID: 8939661
  24. Integrin function in osteoclasts.
    J Endocrinol. 1997 Sep;154 Suppl:S47-56 PMID: 9379137
  25. Stimulation of human prostatic carcinoma cell growth by factors present in human bone marrow.
    J Clin Invest. 1989 Jul;84(1):43-50 PMID: 2786890
  26. Interactions between the bone matrix proteins osteopontin and bone sialoprotein and the osteoclast integrin alpha v beta 3 potentiate bone resorption.
    J Biol Chem. 1993 May 5;268(13):9901-7 PMID: 8486670
  27. Peptidomimetic antagonists of alphavbeta3 inhibit bone resorption by inhibiting osteoclast bone resorptive activity, not osteoclast adhesion to bone.
    J Endocrinol. 2000 Jun;165(3):587-98 PMID: 10828842
  28. Should bisphosphonates be the treatment of choice for metastatic bone disease?
    Semin Oncol. 2001 Aug;28(4 Suppl 11):35-41 PMID: 11544574
  29. A peptidomimetic antagonist of the integrin alpha(v)beta3 inhibits Leydig cell tumor growth and the development of hypercalcemia of malignancy.
    Cancer Res. 1998 May 1;58(9):1930-5 PMID: 9581835
  30. JC70: a new monoclonal antibody that detects vascular endothelium associated antigen on routinely processed tissue sections.
    J Clin Pathol. 1990 Sep;43(9):752-7 PMID: 2212067
  31. Matrix metalloproteinase activity, bone matrix turnover, and tumor cell proliferation in prostate cancer bone metastasis.
    J Natl Cancer Inst. 2002 Jan 2;94(1):17-25 PMID: 11773278
  32. Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines.
    Int J Cancer. 1998 Sep 11;77(6):887-94 PMID: 9714059
  33. Ectopic expression of platelet integrin alphaIIb beta3 in tumor cells from various species and histological origin.
    Int J Cancer. 1997 Aug 7;72(4):642-8 PMID: 9259405
  34. Mechanisms of osteolytic bone destruction.
    Bone. 1991;12 Suppl 1:S1-6 PMID: 1954046
  35. Aggregation of mononucleated precursors triggers cell surface expression of alphavbeta3 integrin, essential to formation of osteoclast-like multinucleated cells.
    J Cell Sci. 1998 Sep;111 ( Pt 17):2563-74 PMID: 9701555
  36. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  37. The synergistic activity of alphavbeta3 integrin and PDGF receptor increases cell migration.
    J Cell Sci. 1998 Feb;111 ( Pt 4):469-78 PMID: 9443896
  38. Integrin alpha V beta 3 expression by bone-residing breast cancer metastases.
    Diagn Mol Pathol. 1996 Jun;5(2):127-35 PMID: 8727100
  39. Suppression of p53 activity and p21WAF1/CIP1 expression by vascular cell integrin alphaVbeta3 during angiogenesis.
    J Clin Invest. 1996 Jul 15;98(2):426-33 PMID: 8755653
  40. Role of the alpha v beta 3 integrin in human melanoma cell invasion.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1557-61 PMID: 1371877
  41. Integrin expression in human bone.
    J Bone Miner Res. 1993 May;8(5):527-33 PMID: 8511980
  42. Mice lacking beta3 integrins are osteosclerotic because of dysfunctional osteoclasts.
    J Clin Invest. 2000 Feb;105(4):433-40 PMID: 10683372
  43. Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin.
    J Clin Invest. 1995 Oct;96(4):1815-22 PMID: 7560073
  44. Acceleration of human prostate cancer growth in vivo by factors produced by prostate and bone fibroblasts.
    Cancer Res. 1991 Jul 15;51(14):3753-61 PMID: 1712249
  45. Expression of hemidesmosomal and extracellular matrix proteins by normal and malignant human prostate tissue.
    Am J Pathol. 1995 Jun;146(6):1498-507 PMID: 7778688
  46. Severe combined immunodeficient-hu model of human prostate cancer metastasis to human bone.
    Cancer Res. 1999 Apr 15;59(8):1987-93 PMID: 10213511
  47. Metabolic bone disease induced by prostate cancer: rationale for the use of bisphosphonates.
    J Urol. 2001 Dec;166(6):2023-31 PMID: 11696699
  48. Modulation of tumor cell response to chemotherapy by the organ environment.
    Cancer Metastasis Rev. 1994 Jun;13(2):209-22 PMID: 7923551
  49. Vitronectin and its receptors.
    Curr Opin Cell Biol. 1993 Oct;5(5):864-8 PMID: 7694604
  50. Definition of two angiogenic pathways by distinct alpha v integrins.
    Science. 1995 Dec 1;270(5241):1500-2 PMID: 7491498
  51. Inhibition of angiogenesis and tumor growth by murine 7E3, the parent antibody of c7E3 Fab (abciximab; ReoPro).
    Angiogenesis. 1999;3(1):53-60 PMID: 14517444
Article Info
Journal
Clinical & experimental metastasis
Abbr.
Clin Exp Metastasis
ISSN
0262-0898
Published
2003-00-00
Pages
413-20
Language
English
Region
Netherlands
NLM ID
8409970
Subset
IM
Analysis Services
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