Angiogenesis inhibitor therapies: focus on kidney toxicity and hypertension.

Angiogenesis inhibitors that target the epidermal growth factor (EGF) receptor (EGFR) and vascular endothelial growth factor (VEGF) constitute an important addition to the therapeutic armamentarium for the treatment of patients with metastatic disease. However, because the same growth factors are expressed in the kidneys, these treatment molecules have renal side effects. EGFR is expressed mainly in tubules (mainly distal and collecting segments) and mesangial and parietal epithelial cells. EGF is involved in maintaining tubular integrity and is a potent mitogen for cultured mesangial cells. Few cases of acute renal failure have been reported related to EGFR inhibitors. VEGF and VEGF receptors are still highly expressed in the kidney. VEGF is expressed in podocytes in the glomerulus, and VEGF receptors are present on endothelial, mesangial, and peritubular capillary cells. Signaling between endothelial cells and podocytes is essential for the proper development and maintenance of the filtration function of the kidney glomerulus. The most common renal class effects of VEGF antagonists are both manageable; hypertension and proteinuria commonly regressive on drug withdrawal. There was a dose-dependent increase in risk of proteinuria and hypertension in patients with cancer who received targeted therapies. Furthermore, few patients with glomerulonephritis or thrombotic microangiopathy secondary to treatment were reported. Hypertension is believed to be nitric oxide dependent, whereas proteinuria seems to be related to downregulation of podocyte tight junction protein. This article reviews data relating to hypertension and proteinuria associated with the use of these drugs.

[1]  H. Izzedine,et al.  Thrombotic microangiopathy and anti-VEGF agents. , 2007, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[2]  W. Dahut,et al.  Risks of proteinuria and hypertension with bevacizumab, an antibody against vascular endothelial growth factor: systematic review and meta-analysis. , 2007, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[3]  R. Toto,et al.  Nephrotic syndrome after bevacizumab: case report and literature review. , 2007, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[4]  P. Campochiaro,et al.  A phase I trial of an IV-administered vascular endothelial growth factor trap for treatment in patients with choroidal neovascularization due to age-related macular degeneration. , 2006, Ophthalmology.

[5]  H. Sugiyama,et al.  Regulation of angiogenic factors in angiotensin II infusion model in association with tubulointerstitial injuries. , 2006, American journal of hypertension.

[6]  N. Yao,et al.  Acute Renal Failure Associated with Gefitinib Therapy , 2006, Lung.

[7]  B. Jensen Cardiotoxic consequences of anthracycline-containing therapy in patients with breast cancer. , 2006, Seminars in oncology.

[8]  G. Rosner,et al.  Phase II placebo-controlled randomized discontinuation trial of sorafenib in patients with metastatic renal cell carcinoma. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[9]  A. Hara,et al.  Blockade of VEGF accelerates proteinuria, via decrease in nephrin expression in rat crescentic glomerulonephritis. , 2006, Kidney international.

[10]  K. Flaherty,et al.  Mechanisms of hypertension associated with BAY 43-9006. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[11]  R. Duisters,et al.  Imatinib Attenuates End-Organ Damage in Hypertensive Homozygous TGR(mRen2)27 Rats , 2006, Hypertension.

[12]  Christopher U. Jones,et al.  Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. , 2006, The New England journal of medicine.

[13]  Betty Y. Y. Tam,et al.  VEGF-dependent plasticity of fenestrated capillaries in the normal adult microvasculature. , 2006, American journal of physiology. Heart and circulatory physiology.

[14]  J. Samuels,et al.  Acute Renal Failure Secondary to Imatinib Mesylate Treatment in Prostate Cancer , 2005, The Annals of pharmacotherapy.

[15]  M. Madaio,et al.  VEGF regulation of endothelial nitric oxide synthase in glomerular endothelial cells. , 2005, Kidney international.

[16]  R. Herbst,et al.  Phase I trial of the oral antiangiogenesis agent AG-013736 in patients with advanced solid tumors: pharmacokinetic and clinical results. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[17]  Eric Masson,et al.  Phase I study of the safety, tolerability, pharmacokinetics, and pharmacodynamics of PTK787/ZK 222584 administered twice daily in patients with advanced cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[18]  F. Kabbinavar,et al.  Combined analysis of efficacy: the addition of bevacizumab to fluorouracil/leucovorin improves survival for patients with metastatic colorectal cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[19]  J. Drevs,et al.  Phase I clinical evaluation of AZD2171, a highly potent VEGF receptor tyrosine kinase inhibitor, in patients with advanced tumors , 2005 .

[20]  R. Motzer,et al.  AG-013736, a multi-target tyrosine kinase receptor inhibitor, demonstrates anti-tumor activity in a Phase 2 study of cytokine-refractory, metastatic renal cell cancer (RCC) , 2005 .

[21]  J. Ajani,et al.  Increased rates of hypertension (HTN) among patients with advanced carcinoid treated with bevacizumab , 2005 .

[22]  J. Hainsworth,et al.  A randomized, double-blind, placebo-controlled, phase III study in patients (Pts) with metastatic adenocarcinoma of the colon or rectum receiving first-line chemotherapy with oxaliplatin/5-fluorouracil/leucovorin and PTK787/ZK 222584 or placebo (CONFIRM-1) , 2005 .

[23]  R. Bukowski,et al.  Randomized phase III trial of the Raf kinase and VEGFR inhibitor sorafenib (BAY 43–9006) in patients with advanced renal cell carcinoma (RCC) , 2005 .

[24]  Edward S. Kim,et al.  Phase I/II trial evaluating the anti-vascular endothelial growth factor monoclonal antibody bevacizumab in combination with the HER-1/epidermal growth factor receptor tyrosine kinase inhibitor erlotinib for patients with recurrent non-small-cell lung cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[25]  M. Gellens,et al.  Thrombotic thrombocytopenic purpura in a patient treated with imatinib mesylate: true association or mere coincidence? , 2005, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[26]  L. Ellis,et al.  Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[27]  M. Cooper,et al.  Imatinib attenuates diabetic nephropathy in apolipoprotein E-knockout mice. , 2005, Journal of the American Society of Nephrology : JASN.

[28]  P Kelly Marcom,et al.  Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[29]  P M Harari,et al.  Epidermal growth factor receptor inhibition strategies in oncology. , 2004, Endocrine-related cancer.

[30]  S. Abman,et al.  Inhaled nitric oxide attenuates pulmonary hypertension and improves lung growth in infant rats after neonatal treatment with a VEGF receptor inhibitor. , 2004, American journal of physiology. Lung cellular and molecular physiology.

[31]  L. Emens,et al.  Trastuzumab in breast cancer. , 2004, Oncology.

[32]  E. Winer,et al.  New targets for therapy in breast cancer: Small molecule tyrosine kinase inhibitors , 2004, Breast Cancer Research.

[33]  Armando Santoro,et al.  Cetuximab monotherapy and cetuximab plus irinotecan in irinotecan-refractory metastatic colorectal cancer. , 2004, The New England journal of medicine.

[34]  R. Roskoski The ErbB/HER receptor protein-tyrosine kinases and cancer. , 2004, Biochemical and biophysical research communications.

[35]  K. Shirato,et al.  Side effects of therapy: case 1. Nephrotic syndrome associated with gefitinib therapy. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[36]  J. Berlin,et al.  Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. , 2004, The New England journal of medicine.

[37]  R. Roskoski The ErbB/HER receptor protein-tyrosine kinases and cancer*1 , 2004 .

[38]  David M Jablons,et al.  Randomized phase II trial comparing bevacizumab plus carboplatin and paclitaxel with carboplatin and paclitaxel alone in previously untreated locally advanced or metastatic non-small-cell lung cancer. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[39]  Hiroshi Tanaka,et al.  Acute lung injury as an adverse event of gefitinib , 2004, Anti-cancer drugs.

[40]  M. Flamant,et al.  Prevention of renal vascular and glomerular fibrosis by epidermal growth factor receptor inhibition , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[41]  M. Ranson,et al.  Gefitinib, a novel, orally administered agent for the treatment of cancer , 2004, Journal of clinical pharmacy and therapeutics.

[42]  T. Spector,et al.  Perinatal outcome of singletons and twins after assisted conception: a systematic review of controlled studies , 2004, The New England journal of medicine.

[43]  D. Gilliland,et al.  CHIC2 deletion, a surrogate for FIP1L1-PDGFRA fusion, occurs in systemic mastocytosis associated with eosinophilia and predicts response to imatinib mesylate therapy. , 2003, Blood.

[44]  Seth M Steinberg,et al.  A randomized trial of bevacizumab, an anti-vascular endothelial growth factor antibody, for metastatic renal cancer. , 2003, The New England journal of medicine.

[45]  M. Solé,et al.  Acute Renal Failure Secondary to Imatinib Mesylate Treatment in Chronic Myeloid Leukemia , 2003, Leukemia & lymphoma.

[46]  H. Struijker‐Boudier,et al.  Current Perspectives on Arterial Stiffness and Pulse Pressure in Hypertension and Cardiovascular Diseases , 2003, Circulation.

[47]  M. Hidalgo,et al.  Development of the epidermal growth factor receptor inhibitor OSI-774. , 2003, Seminars in Oncology.

[48]  N. Ferrara,et al.  The biology of VEGF and its receptors , 2003, Nature Medicine.

[49]  R. Kalluri,et al.  Neutralization of Circulating Vascular Endothelial Growth Factor (VEGF) by Anti-VEGF Antibodies and Soluble VEGF Receptor 1 (sFlt-1) Induces Proteinuria* , 2003, The Journal of Biological Chemistry.

[50]  Peter Marynen,et al.  A tyrosine kinase created by fusion of the PDGFRA and FIP1L1 genes as a therapeutic target of imatinib in idiopathic hypereosinophilic syndrome. , 2003, The New England journal of medicine.

[51]  Brian H Annex,et al.  The VIVA Trial Vascular Endothelial Growth Factor in Ischemia for Vascular Angiogenesis , 2003 .

[52]  J. Haigh,et al.  Glomerular-specific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. , 2003, The Journal of clinical investigation.

[53]  G. Jerums,et al.  Expression of the slit-diaphragm protein, nephrin, in experimental diabetic nephropathy: differing effects of anti-proteinuric therapies. , 2002, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[54]  Lieve Moons,et al.  Loss of the VEGF(164) and VEGF(188) isoforms impairs postnatal glomerular angiogenesis and renal arteriogenesis in mice. , 2002, Journal of the American Society of Nephrology : JASN.

[55]  A. Tefferi,et al.  Treatment of hypereosinophilic syndrome with imatinib mesilate , 2002, The Lancet.

[56]  C. Kitiyakara,et al.  Renal failure associated with a specific inhibitor of BCR-ABL tyrosine kinase, STI 571. , 2002, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[57]  P. D. Dal Cin,et al.  Growth inhibition of dermatofibrosarcoma protuberans tumors by the platelet-derived growth factor receptor antagonist STI571 through induction of apoptosis. , 2001, Cancer research.

[58]  D. Tuveson,et al.  Effect of the tyrosine kinase inhibitor STI571 in a patient with a metastatic gastrointestinal stromal tumor. , 2001, The New England journal of medicine.

[59]  R. Atkins,et al.  PDGF signal transduction inhibition ameliorates experimental mesangial proliferative glomerulonephritis. , 2001, Kidney international.

[60]  P. Black,et al.  Intracranial inhibition of platelet-derived growth factor-mediated glioblastoma cell growth by an orally active kinase inhibitor of the 2-phenylaminopyrimidine class. , 2000, Cancer research.

[61]  L. Gnudi,et al.  Vascular endothelial growth factor receptors in human mesangium in vitro and in glomerular disease. , 2000, Journal of the American Society of Nephrology : JASN.

[62]  J. Mestan,et al.  PTK787/ZK 222584, a novel and potent inhibitor of vascular endothelial growth factor receptor tyrosine kinases, impairs vascular endothelial growth factor-induced responses and tumor growth after oral administration. , 2000, Cancer research.

[63]  L. Norton,et al.  Phase I studies of anti-epidermal growth factor receptor chimeric antibody C225 alone and in combination with cisplatin. , 2000, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[64]  H. Rennke,et al.  Collapsing glomerulopathy in HIV and non-HIV patients: a clinicopathological and follow-up study. , 1999, Kidney international.

[65]  N. Ferrara Molecular and biological properties of vascular endothelial growth factor , 1999, Journal of Molecular Medicine.

[66]  L. Pustilnik,et al.  Induction of apoptosis and cell cycle arrest by CP-358,774, an inhibitor of epidermal growth factor receptor tyrosine kinase. , 1997, Cancer research.

[67]  Jürg Zimmermann,et al.  Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr–Abl positive cells , 1996, Nature Medicine.

[68]  C. Vlachopoulos,et al.  Medial necrosis and acute alterations in aortic distensibility following removal of the vasa vasorum of canine ascending aorta. , 1993, Cardiovascular research.

[69]  J. Winer,et al.  The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. , 1991, Molecular endocrinology.

[70]  J. Fiddes,et al.  The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. , 1991, The Journal of biological chemistry.

[71]  P. Kincaid‐smith The renal lesion of preeclampsia revisited. , 1991, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[72]  K. Yoshioka,et al.  Identification and localization of epidermal growth factor and its receptor in the human glomerulus. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[73]  A. Belldegrun,et al.  Epidermal growth factor receptor gene expression in normal human kidney and renal cell carcinoma. , 1989, The Journal of urology.

[74]  J. Folkman,et al.  Proceedings: Tumor angiogenesis factor. , 1974, Cancer research.

[75]  Yasufumi Sato,et al.  The vasohibin family: a negative regulatory system of angiogenesis genetically programmed in endothelial cells. , 2007, Arteriosclerosis, thrombosis, and vascular biology.

[76]  R. Figlin,et al.  Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[77]  E. Raymond,et al.  Safety, pharmacokinetic, and antitumor activity of SU11248, a novel oral multitarget tyrosine kinase inhibitor, in patients with cancer. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[78]  Napoleone Ferrara,et al.  The role of vascular endothelial growth factor in pathological angiogenesis , 2004, Breast Cancer Research and Treatment.

[79]  D. Sane,et al.  Angiogenic growth factors and hypertension , 2004, Angiogenesis.

[80]  F. Kabbinavar,et al.  Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. , 2003, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[81]  M. Foster Relevance of systemic lupus erythematosus nephritis animal models to human disease. , 1999, Seminars in nephrology.

[82]  K. Stefanaki,et al.  Immunohistochemical study of epidermal growth factor receptor (EGFR) in various types of renal injury. , 1994, Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association.

[83]  A. Macleod,et al.  An Immunohistological Study Of Epidermal Growth Factor Receptor And Neu Receptor Expression In Proliferative Glomerulonephritis , 1993 .

[84]  Sue E. Huether,et al.  Pathophysiology: The Biologic Basis for Disease in Adults and Children , 1990 .

[85]  B. J. Helyer,et al.  The immunology and pathology of NZB mice. , 1968, Advances in immunology.