Breast cancer: the role of angiogenesis and antiangiogenic therapy.

Angiogenesis plays a role in breast cancer development. Preclinical and clinical evidence is reviewed. Development of targeted antiangiogenic agents provides new challenges to clinical trial design. Current antiangiogenic therapy with traditional agents and novel agents are classified and reviewed.

[1]  J. Nemunaitis,et al.  A double-blind placebo-controlled, randomised study comparing gemcitabine and marimastat with gemcitabine and placebo as first line therapy in patients with advanced pancreatic cancer , 2002, British Journal of Cancer.

[2]  J. Bahi,et al.  Angiogenesis and risk of breast cancer in women with fibrocystic disease. , 1994, Journal of the National Cancer Institute.

[3]  Michael S. Pepper,et al.  The endogenous oestrogen metabolite 2-methoxyoestradiol inhibits angiogenesis and suppresses tumour growth , 1994, Nature.

[4]  G. Sledge,et al.  Redefining the target: chemotherapeutics as antiangiogenics. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[5]  H. Degani,et al.  Tamoxifen enhances cell death in implanted MCF7 breast cancer by inhibiting endothelium growth. , 1994, Cancer research.

[6]  N. Weidner,et al.  Tumor microvessel density, p53 expression, tumor size, and peritumoral lymphatic vessel invasion are relevant prognostic markers in node-negative breast carcinoma. , 1994, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[7]  D. Collins,et al.  Inhibition of angiogenesis by antiestrogens. , 1993, Cancer research.

[8]  A. Harris,et al.  Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[9]  L. Norton,et al.  Phase I and pharmacologic study of paclitaxel administered weekly in patients with relapsed ovarian cancer. , 1997, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[10]  J. Caro,et al.  Hypoxia-inducible factor 1alpha (HIF-1alpha) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions. Its stabilization by hypoxia depends on redox-induced changes. , 1997, The Journal of biological chemistry.

[11]  James N Ingle,et al.  Randomized phase III trial of marimastat versus placebo in patients with metastatic breast cancer who have responding or stable disease after first-line chemotherapy: Eastern Cooperative Oncology Group trial E2196. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[12]  E Biganzoli,et al.  Vascular integrin alpha(v)beta3: a new prognostic indicator in breast cancer. , 1998, Clinical cancer research : an official journal of the American Association for Cancer Research.

[13]  S. Steinberg,et al.  Phase I clinical trial of oral COL-3, a matrix metalloproteinase inhibitor, in patients with refractory metastatic cancer. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[14]  M. Toi,et al.  [Significance of tumor angiogenesis as an independent prognostic factor in axillary node-negative breast cancer]. , 1995, Gan to kagaku ryoho. Cancer & chemotherapy.

[15]  S. Fox,et al.  Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenes , 1997, Cancer research.

[16]  N. Brünner,et al.  S-phase fraction and urokinase plasminogen activator are better markers for distant recurrences than Nottingham Prognostic Index and histologic grade in a prospective study of premenopausal lymph node-negative breast cancer. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[17]  A. Howell,et al.  TUMOUR ANGIOGENESIS AS A PROGNOSTIC MARKER IN INFILTRATING LOBULAR CARCINOMA OF THE BREAST , 1996, The Journal of pathology.

[18]  M. Nooij,et al.  "Classical" CMF versus a 3-weekly intravenous CMF schedule in postmenopausal patients with advanced breast cancer. An EORTC Breast Cancer Co-operative Group Phase III Trial (10808). , 1991, European journal of cancer.

[19]  Bing Li,et al.  Inhibition of vascular endothelial growth factor-induced angiogenesis suppresses tumour growth in vivo , 1993, Nature.

[20]  F. Sarkar,et al.  Antiintegrin alpha v beta 3 blocks human breast cancer growth and angiogenesis in human skin. , 1995, The Journal of clinical investigation.

[21]  O. Nanni,et al.  Tumor microvessel density and prognosis in node‐negative breast cancer , 2000, International journal of cancer.

[22]  J. Connolly,et al.  Suppression of tumor-forming ability and related traits in MCF-7 human breast cancer cells by fusion with immortal mammary epithelial cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[23]  D. Cheresh,et al.  Disruption of Angiogenesis by PEX, a Noncatalytic Metalloproteinase Fragment with Integrin Binding Activity , 1998, Cell.

[24]  Shigeyoshi Itohara,et al.  Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis , 2000, Nature Cell Biology.

[25]  G. Semenza,et al.  Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Anthony J. Guidi,et al.  Microvessel density and distribution in ductal carcinoma in situ of the breast. , 1994, Journal of the National Cancer Institute.

[27]  D. Lindner,et al.  Effects of tamoxifen and interferon‐β or the combination on tumor‐induced angiogenesis , 1997, International journal of cancer.

[28]  Brian H. Mayall,et al.  Re: Tumor Angiogenesis as a Prognostic Assay for Invasive Ductal Breast Carcinoma , 1995 .

[29]  T. Canda,et al.  The role of angiogenesis, laminin and CD44 expression in metastatic behavior of early-stage low-grade invasive breast carcinomas. , 1997, Cancer letters.

[30]  A. Harris,et al.  Distinct Angiogenic patterns are associated with high‐grade in situ ductal carcinomas of the breast , 1997, The Journal of pathology.

[31]  G. Semenza,et al.  Levels of Hypoxia-Inducible Factor-1α During Breast Carcinogenesis , 2001 .

[32]  R. Kerbel,et al.  Protracted low-dose effects on human endothelial cell proliferation and survival in vitro reveal a selective antiangiogenic window for various chemotherapeutic drugs. , 2002, Cancer research.

[33]  O. Vinante,et al.  Prognostic significance of vascular endothelial growth factor protein in node-negative breast carcinoma. , 1997, Journal of the National Cancer Institute.

[34]  Anthony J. Guidi,et al.  Vascular permeability factor (Vascular endothelial growth factor) expression and angiogenesis in patients with ductal carcinoma in situ of the breast , 1997, Cancer.

[35]  J. Folkman,et al.  Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. , 2000, Cancer research.

[36]  P. Boracchi,et al.  Prognostic significance of p53, angiogenesis, and other conventional features in operable breast cancer: subanalysis in node-positive and node-negative patients. , 1998, International journal of oncology.

[37]  J. Scholefield,et al.  Marimastat as maintenance therapy for patients with advanced gastric cancer: a randomised trial , 2002, British Journal of Cancer.

[38]  G. Sledge,et al.  Phase I safety and pharmacokinetic study of recombinant human anti-vascular endothelial growth factor in patients with advanced cancer. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[39]  P H Watson,et al.  Hypoxia-inducible expression of tumor-associated carbonic anhydrases. , 2000, Cancer research.

[40]  J. Folkman,et al.  Tumor angiogenesis and metastasis--correlation in invasive breast carcinoma. , 1991, The New England journal of medicine.

[41]  P. Vermeulen,et al.  Clinical relevance of vascular endothelial growth factor and thymidine phosphorylase in patients with node-positive breast cancer treated with either adjuvant chemotherapy or hormone therapy. , 1999, The cancer journal from Scientific American.

[42]  A. Choy,et al.  Association between tumour angiogenesis and tumour cell shedding into effluent venous blood during breast cancer surgery , 1995, The Lancet.

[43]  M. Hidalgo,et al.  Development of matrix metalloproteinase inhibitors in cancer therapy. , 2001, Journal of the National Cancer Institute.

[44]  A. Lee,et al.  Microvessel quantitation and prognosis in invasive breast carcinoma. , 1992, Human pathology.

[45]  M. Toi,et al.  Tumor angiogenesis in breast cancer: Its importance as a prognostic indicator and the association with vascular endothelial growth factor expression , 2004, Breast Cancer Research and Treatment.

[46]  I. Hart,et al.  Matrix metalloproteinases and metastatic cancer. , 1998, Biochemical Society symposium.

[47]  T. H. van der Kwast,et al.  High tumor levels of vascular endothelial growth factor predict poor response to systemic therapy in advanced breast cancer. , 2001, Cancer research.

[48]  G. Sledge,et al.  A Randomized Phase II Feasibility Trial of BMS-275291 in Patients with Early Stage Breast Cancer , 2004, Clinical Cancer Research.

[49]  A. Howell,et al.  Assessment of tumour vascularity as a prognostic factor in lymph node negative invasive breast cancer. , 1993, European journal of cancer.

[50]  W. Gradishar,et al.  A randomized phase II pilot trial of adjuvant marimastat in patients with early-stage breast cancer. , 2002, Annals of oncology : official journal of the European Society for Medical Oncology.

[51]  S. Eccles,et al.  Control of lymphatic and hematogenous metastasis of a rat mammary carcinoma by the matrix metalloproteinase inhibitor batimastat (BB-94). , 1996, Cancer research.

[52]  R. Weichselbaum,et al.  Angiogenesis as a predictor of long-term survival for patients with node-negative breast cancer. , 1996, Journal of the National Cancer Institute.

[53]  H. Wiseman Tamoxifen: new membrane-mediated mechanisms of action and therapeutic advances. , 1994, Trends in pharmacological sciences.

[54]  L. Liotta,et al.  Laminin receptors, collagenase IV and prognosis in node‐negative breast cancers , 1991, International journal of cancer.

[55]  D. Cheresh,et al.  Requirement of vascular integrin alpha v beta 3 for angiogenesis. , 1994, Science.

[56]  A. Kossakowska,et al.  Comparative analysis of the expression patterns of metalloproteinases and their inhibitors in breast neoplasia, sporadic colorectal neoplasia, pulmonary carcinomas and malignant non-Hodgkin's lymphomas in humans. , 1996, British Journal of Cancer.

[57]  G. Sledge,et al.  Effect of matrix metalloproteinase inhibitor batimastat on breast cancer regrowth and metastasis in athymic mice. , 1995, Journal of the National Cancer Institute.

[58]  W Vach,et al.  The prognostic value of angiogenesis by Chalkley counting in a confirmatory study design on 836 breast cancer patients. , 2000, Clinical cancer research : an official journal of the American Association for Cancer Research.

[59]  C. Dinney,et al.  Interferon-alpha-mediated down-regulation of angiogenesis-related genes and therapy of bladder cancer are dependent on optimization of biological dose and schedule. , 1999, Clinical cancer research : an official journal of the American Association for Cancer Research.

[60]  S. Kumar,et al.  Breast carcinoma: vascular density determined using CD105 antibody correlates with tumor prognosis. , 1999, Cancer research.

[61]  S. Fox,et al.  The prognostic value of quantitative angiogenesis in breast cancer and role of adhesion molecule expression in tumor endothelium , 2004, Breast Cancer Research and Treatment.

[62]  N. Weidner,et al.  Prognostic value of intratumoral microvessel density, a measure of tumor angiogenesis, in node-negative breast carcinoma — results of a multiparametric study , 2004, Breast Cancer Research and Treatment.

[63]  D. Cheresh,et al.  Integrin α v β 3 antagonists promote tumor regression by inducing apoptosis of angiogenic blood vessels , 1994, Cell.

[64]  B. Hennig,et al.  Antiestrogens inhibit endothelial cell growth stimulated by angiogenic growth factors. , 1996, Anticancer research.

[65]  J. Fargnoli,et al.  Inhibition of angiogenesis and metastasis in two murine models by the matrix metalloproteinase inhibitor, BMS-275291. , 2001, Cancer research.

[66]  J. Monson,et al.  Is the relationship between angiogenesis and metastasis in breast cancer real? , 1992, Surgical oncology.

[67]  A. Kaider,et al.  Vascular endothelial growth factor (VEGF) in human breast cancer: Correlation with disease‐free survival , 1997, International journal of cancer.

[68]  A. Rosemurgy,et al.  Marimastat as first-line therapy for patients with unresectable pancreatic cancer: a randomized trial. , 2001, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[69]  J. Foekens,et al.  Markers of tumor angiogenesis and proteolysis independently define high- and low-risk subsets of node-negative breast cancer patients. , 1998, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[70]  Peter Bohlen,et al.  Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity , 2000 .

[71]  J. Russo,et al.  Tamoxifen down-regulates CD36 messenger RNA levels in normal and neoplastic human breast tissues. , 1997, Cancer research.

[72]  Y. Chung,et al.  Microvessel quantitation in invasive breast cancer by staining for factor VIII-related antigen. , 1995, British Journal of Cancer.

[73]  S. Fox,et al.  Association of tumor angiogenesis with bone marrow micrometastases in breast cancer patients. , 1997, Journal of the National Cancer Institute.

[74]  L. Norton,et al.  Ninety-six-hour paclitaxel infusion after progression during short taxane exposure: a phase II pharmacokinetic and pharmacodynamic study in metastatic breast cancer. , 1996, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[75]  H. Aronen,et al.  Prognostic value of vascular density and cell proliferation in breast cancer patients. , 1999, Pathology, research and practice.

[76]  F Pozza,et al.  Tumor angiogenesis: a new significant and independent prognostic indicator in early-stage breast carcinoma. , 1992, Journal of the National Cancer Institute.

[77]  Gabriele Bergers,et al.  Less is more, regularly: metronomic dosing of cytotoxic drugs can target tumor angiogenesis in mice. , 2000, The Journal of clinical investigation.

[78]  P. Hahnfeldt,et al.  Tumor development under angiogenic signaling: a dynamical theory of tumor growth, treatment response, and postvascular dormancy. , 1999, Cancer research.

[79]  M. Toi,et al.  Association of Vascular Endothelial Growth Factor Expression with Tumor Angiogenesis and with Early Relapse in Primary Breast Cancer , 1994, Japanese journal of cancer research : Gann.

[80]  J. Sloan,et al.  Phase I study of the matrix metalloproteinase inhibitor, BAY 12-9566. , 2001, Annals of oncology : official journal of the European Society for Medical Oncology.

[81]  A. Vincent-Salomon,et al.  Long term outcome of small size invasive breast carcinomas independent from angiogenesis in a series of 685 cases , 2001, Cancer.

[82]  H. Arvaniti,et al.  Tumor angiogenesis in node-negative breast cancer: relationship with relapse free survival. , 1996, Anticancer research.

[83]  D. Carney,et al.  Prognostic significance of microvessel density in lymph node negative breast carcinoma. , 1995, Human pathology.

[84]  S. Fox,et al.  Tumor angiogenesis in node-negative breast carcinomas — relationship with epidermal growth factor receptor, estrogen receptor, and survival , 2004, Breast Cancer Research and Treatment.

[85]  C Kurz,et al.  Microvessel density and vessel invasion in lymph‐node‐negative breast cancer: Effect on recurrence‐free survival , 1995, International journal of cancer.