The vasostatin‐1 fragment of chromogranin A preserves a quiescent phenotype in hypoxia‐driven endothelial cells and regulates tumor neovascularization

The angiogenic switch is a fundamental process for many diseases and for tumor growth. The main proangiogenic stimulus is hypoxia, through activation of the hypoxia‐inducible factor (HIF)‐1α pathway in endothelial cells (ECs). We have previously shown that the vasostatin‐1 (VS‐1) fragment of chromogranin A inhibits TNF‐α‐induced vessel permeability and VEGF‐induced EC proliferation, together with migration and matrix invasion, which are all critical steps in angiogenesis. The present study was undertaken to investigate the effect of VS‐1 on tumor angiogenesis. We found mouse mammary adenocarcinomas (TS/A), genetically engineered to secrete VS‐1 (TS/A 1B8), to be characterized by reduced vascular density and more regular vessels, compared with nontransfected tumors [TS/A wild type (WT)]. Supernatants from TS/A WT cells, but not those from TS/A 1B8, generated tip cells and promoted the permeability of primary human umbilical vein ECs, via VE‐cadherin redistribution and cytoskeletal disorganization. These effects were abrogated by mAb 5A8, a VS‐1‐blocking antibody. Furthermore, VS‐1 inhibited hypoxia‐driven EC morphological changes, VE‐cadherin redistribution, intercellular gap formation, tube morphogenesis, and HIF‐1α nuclear translocation in vitro. Our findings highlight a previously undescribed function of VS‐1 as a regulator of tumor vascularization.—Veschini, L., Crippa, L., Dondossola, E., Doglioni, C., Corti, A., Ferrero, E. The vasostatin‐1 fragment of chromogranin a preserves a quiescent phenotype in hypoxia‐driven endothelial cells and regulates tumor neovascularization. FASEB J. 25, 3906–3914 (2011). www.fasebj.org

[1]  A. Morganti,et al.  Chromogranin A: a novel factor acting at the cross road between the neuroendocrine and the cardiovascular systems , 2011, Journal of hypertension.

[2]  S. Rong,et al.  The Neuropeptide Catestatin Acts As a Novel Angiogenic Cytokine via a Basic Fibroblast Growth Factor–Dependent Mechanism , 2010, Circulation research.

[3]  K. Helle Regulatory Peptides from Chromogranin A and Secretogranin II , 2010, Cellular and Molecular Neurobiology.

[4]  A. Corti Chromogranin A and the Tumor Microenvironment , 2010, Cellular and Molecular Neurobiology.

[5]  A. Malik,et al.  Krüppel-Like Factor-4 Transcriptionally Regulates VE-Cadherin Expression and Endothelial Barrier Function , 2010, Circulation research.

[6]  Dengwen Li,et al.  CYLD regulates angiogenesis by mediating vascular endothelial cell migration. , 2010, Blood.

[7]  R. Levi,et al.  Vasostatin 1 activates eNOS in endothelial cells through a proteoglycan‐dependent mechanism , 2010, Journal of cellular biochemistry.

[8]  M. Ferrarini,et al.  Bortezomib induces autophagic death in proliferating human endothelial cells. , 2010, Experimental cell research.

[9]  O. Alfieri,et al.  Increased expression and secretion of resistin in epicardial adipose tissue of patients with acute coronary syndrome. , 2010, American journal of physiology. Heart and circulatory physiology.

[10]  N. Mahapatra,et al.  Chromogranin A: a novel susceptibility gene for essential hypertension , 2010, Cellular and Molecular Life Sciences.

[11]  G. Semenza Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics , 2010, Oncogene.

[12]  Laura Fernández-Martín,et al.  Adherens junctions connect stress fibres between adjacent endothelial cells , 2010, BMC Biology.

[13]  S. Indraccolo,et al.  The angiogenic switch: implications in the regulation of tumor dormancy. , 2009, Current molecular medicine.

[14]  Frederik De Smet,et al.  Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way , 2009, Nature Reviews Clinical Oncology.

[15]  Peter Carmeliet,et al.  Endothelial oxygen sensors regulate tumor vessel abnormalization by instructing phalanx endothelial cells , 2009, Journal of Molecular Medicine.

[16]  Peter Carmeliet,et al.  Mechanisms of Vessel Branching: Filopodia on Endothelial Tip Cells Lead the Way , 2009, Arteriosclerosis, thrombosis, and vascular biology.

[17]  V. Bautch Endothelial Cells Form a Phalanx to Block Tumor Metastasis , 2009, Cell.

[18]  Frederik De Smet,et al.  Heterozygous Deficiency of PHD2 Restores Tumor Oxygenation and Inhibits Metastasis via Endothelial Normalization , 2009, Cell.

[19]  Christian Fischer,et al.  FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? , 2008, Nature Reviews Cancer.

[20]  K. Helle,et al.  The vasostatin‐I fragment of chromogranin A inhibits VEGF‐induced endothelial cell proliferation and migration , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[21]  Dai Fukumura,et al.  Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. , 2007, Microvascular research.

[22]  Dai Fukumura,et al.  Tumor microenvironment abnormalities: Causes, consequences, and strategies to normalize , 2007, Journal of cellular biochemistry.

[23]  M. Ferrarini,et al.  Hypoxia-inducible transcription factor-1 alpha determines sensitivity of endothelial cells to the proteosome inhibitor bortezomib. , 2007, Blood.

[24]  R. Shoemaker,et al.  Hypoxic induction of an HIF-1alpha-dependent bFGF autocrine loop drives angiogenesis in human endothelial cells. , 2006, Blood.

[25]  J. Pouysségur,et al.  Transcriptional regulation of the Vascular Endothelial Growth Factor gene--a concert of activating factors. , 2005, Cardiovascular research.

[26]  R. Jain Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy , 2005, Science.

[27]  A. Villa,et al.  Chromogranin A protects vessels against tumor necrosis factor α‐induced vascular leakage , 2004, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[28]  G. Semenza Angiogenesis in ischemic and neoplastic disorders. , 2003, Annual review of medicine.

[29]  A. Corti,et al.  Chromogranin A expression in neoplastic cells affects tumor growth and morphogenesis in mouse models. , 2002, Cancer research.

[30]  R. Longhi,et al.  Production and structure characterisation of recombinant chromogranin A N-terminal fragments (vasostatins) -- evidence of dimer-monomer equilibria. , 1997, European journal of biochemistry.

[31]  W. Aird Endothelium in health and disease. , 2008, Pharmacological reports : PR.

[32]  A. Bikfalvi,et al.  Tumor angiogenesis , 2020, Advances in cancer research.

[33]  Richard P. Hill,et al.  The hypoxic tumour microenvironment and metastatic progression , 2004, Clinical & Experimental Metastasis.