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  • 1.
    Bäckman, Ulrika
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Svensson, Åsa
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Christofferson, Rolf
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Surgical Sciences.
    Importance of Vascular Endothelial Growth Factor A in the Progression of Experimental Neuroblastoma2002In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 5, no 4, p. 267-274Article in journal (Refereed)
    Abstract [en]

    Vascular endothelial growth factor A (VEGF-A) and its receptor tyrosine kinases located on endothelial cells seem to play an important role in the multistep pathway of angiogenesis. SU5416 is a small molecule which inhibits angiogenesis by acting as an inhibitor of VEGF receptor-2 tyrosine kinase. We have developed a reproducible murine model for neuroblastoma, a childhood cancer, based on s.c. xenotransplantation of SH-SY5Y neuroblastoma cells. We found that SH-SY5Y cells expressed VEGF-A on both the mRNA and protein levels, that plasma concentrations of VEGF-A were significantly elevated in animals with neuroblastoma with a volume > 1.4 ml, and that there was a correlation between VEGF-A levels in plasma and tumor size in untreated tumor-bearing animals. Treatment with SU5416 reduced the growth of neuroblastoma tumors by 65% without apparent toxicity. SU5416 treatment also suppressed tumor angiogenesis, despite an increase in plasma VEGF-A levels per ml tumor volume during therapy. Our experimental data suggest that the angiogenesis inhibitor SU5416 may be beneficial in the treatment of solid tumors of childhood such as neuroblastoma.

  • 2.
    Cedervall, Jessica
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Zhang, Yanyu
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Ringvall, Maria
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Thulin, Åsa
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Sciences, Coagulation and inflammation science.
    Moustakas, Aristidis
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Medicinska och farmaceutiska vetenskapsområdet, centrumbildningar mm, Ludwig Institute for Cancer Research.
    Jahnen-Dechent, Willi
    Biointerface Laboratory, Department of Biomedical Engineering, RWTH Aachen University, Pauwelsstrasse 30, 52074 Aachen, Germany.
    Siegbahn, Agneta
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Sciences, Coagulation and inflammation science.
    Olsson, Anna-Karin
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    HRG regulates tumor progression, epithelial to mesenchymal transition and metastasis via platelet-induced signaling in the pre-tumorigenic microenvironment2013In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 16, no 4, p. 889-902Article in journal (Refereed)
    Abstract [en]

    Mice lacking histidine-rich glycoprotein (HRG) display an accelerated angiogenic switch and larger tumors-a phenotype caused by enhanced platelet activation in the HRG-deficient mice. Here we show that platelets induce molecular changes in the pre-tumorigenic environment in HRG-deficient mice, promoting cell survival, angiogenesis and epithelial-to-mesenchymal transition (EMT) and that these effects involved signaling via TBK1, Akt2 and PDGFR beta. These early events subsequently translate into an enhanced rate of spontaneous metastasis to distant organs in mice lacking HRG. Later in tumor development characteristic features of pathological angiogenesis, such as decreased perfusion and pericyte coverage, are more pronounced in HRG-deficient mice. At this stage, platelets are essential to support the larger tumor volumes formed in mice lacking HRG by keeping their tumor vasculature sufficiently functional. We conclude that HRG-deficiency promotes tumor progression via enhanced platelet activity and that platelets play a dual role in this process. During early stages of transformation, activated platelets promote tumor cell survival, the angiogenic switch and invasiveness. In the more progressed tumor, platelets support the enhanced pathological angiogenesis and hence increased tumor growth seen in the absence of HRG. Altogether, our findings strengthen the notion of HRG as a potent tumor suppressor, with capacity to attenuate the angiogenic switch, tumor growth, EMT and subsequent metastatic spread, by regulating platelet activity.

  • 3.
    Christoffersson, Gustav
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology, Integrative Physiology.
    Zang, Guangxiang
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Zhuang, Zhen W.
    Vågesjö, Evelina
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology, Integrative Physiology.
    Simons, Michael
    Phillipson, Mia
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology, Integrative Physiology.
    Welsh, Michael
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Vascular adaptation to a dysfunctional endothelium as a consequence of Shb deficiency2012In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 15, no 3, p. 469-480Article in journal (Refereed)
    Abstract [en]

    Vascular endothelial growth factor (VEGF)-A regulates angiogenesis, vascular morphology and permeability by signaling through its receptor VEGFR-2. The Shb adapter protein has previously been found to relay certain VEGFR-2 dependent signals and consequently vascular physiology and structure was assessed in Shb knockout mice. X-ray computed tomography of vessels larger than 24 mm diameter (micro-CT) after contrast injection revealed an increased frequency of 48-96 µm arterioles in the hindlimb calf muscle in Shb knockout mice. Intravital microscopy of the cremaster muscle demonstrated a less regular vasculature with fewer branch points and increased vessel tortuosity, changes that led to an increased blood flow velocity. Reduced in vivo angiogenesis was observed in Shb knockout MatrigelTM plugs. Unlike the wild-type situation, VEGF-A did not provoke a dissociation of VE-cadherin from adherens junctions in Shb knockout venules. The reduced angiogenesis and altered properties of junctions had consequences for two patho-physiological responses to arterial occlusion: vascular permeability was reduced in the Shb knockout cremaster muscle after ligation of one supplying artery and heat-induced blood flow determined by Laser-Doppler measurements was decreased in the hindlimb after ligation of the femoral artery. Consequently, the Shb knockout mouse exhibited structural and functional (angiogenesis and vascular permeability) vascular abnormalities that have implications for understanding the function of VEGF-A under physiological conditions.

  • 4. Coltrini, Daniela
    et al.
    Di Salle, Emanuela
    Ronca, Roberto
    Belleri, Mirella
    Testini, Chiara
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology.
    Presta, Marco
    Matrigel plug assay: evaluation of the angiogenic response by reverse transcription-quantitative PCR2012In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209Article in journal (Refereed)
  • 5. Coma, Silvia
    et al.
    Allard-Ratick, Marc
    Akino, Tomoshige
    van Meeteren, Laurens A.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology.
    Mammoto, Akiko
    Klagsbrun, Michael
    GATA2 and Lmo2 control angiogenesis and lymphangiogenesis via direct transcriptional regulation of neuropilin-22013In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 16, no 4, p. 939-952Article in journal (Refereed)
    Abstract [en]

    GATA-binding protein 2 (GATA2) and LIM domain only 2 (Lmo2) form common transcription complexes during hematopoietic differentiation. Here we show that these two transcription factors also play a key role in endothelial cells (EC) and lymphatic EC (LEC) function. Primary EC and tumor-associated blood vessels expressed GATA2 and Lmo2. VEGF-induced sprouting angiogenesis in both differentiating embryonic stem cells (embryoid bodies) and primary EC increased GATA2 and Lmo2 levels. Conversely, silencing of GATA2 and Lmo2 expression in primary EC inhibited VEGF-induced angiogenic activity, including EC migration and sprouting in vitro, two key steps of angiogenesis in vivo. This inhibition of EC function was associated with downregulated expression of neuropilin-2 (NRP2), a co-receptor of VEGFRs for VEGF, at the protein, mRNA and promoter levels. NRP2 overexpression partially rescued the impaired angiogenic sprouting in the GATA2/Lmo2 knockdown EC, confirming that GATA2 and Lmo2 mediated EC function, at least in part, by directly regulating NRP2 gene expression. Furthermore, it was found that primary LEC expressed GATA2 and Lmo2 as well. Silencing of GATA2 and Lmo2 expression in LEC inhibited VEGF-induced LEC sprouting, also in a NRP2-dependent manner. In conclusion, our results demonstrate that GATA2 and Lmo2 cooperatively regulate VEGF-induced angiogenesis and lymphangiogenesis via NRP2.

  • 6.
    Dieterich, Lothar C.
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology.
    Huang, Hua
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Massena, Sara
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Golenhofen, Nikola
    Phillipson, Mia
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Cell Biology.
    Dimberg, Anna
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    alpha B-crystallin/HspB5 regulates endothelial-leukocyte interactions by enhancing NF-kappa B-induced up-regulation of adhesion molecules ICAM-1, VCAM-1 and E-selectin2013In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 16, no 4, p. 975-983Article in journal (Refereed)
    Abstract [en]

    alpha B-crystallin is a small heat shock protein, which has pro-angiogenic properties by increasing survival of endothelial cells and secretion of vascular endothelial growth factor A. Here we demonstrate an additional role of alpha B-crystallin in regulating vascular function, through enhancing tumor necrosis factor alpha (TNF-alpha) induced expression of endothelial adhesion molecules involved in leukocyte recruitment. Ectopic expression of alpha B-crystallin in endothelial cells increases the level of E-selectin expression in response to TNF-alpha, and enhances leukocyte-endothelial interaction in vitro. Conversely, TNF-alpha-induced expression of intercellular adhesion molecule 1, vascular cell adhesion molecule 1 and E-selectin is markedly inhibited in endothelial cells isolated from alpha B-crystallin-deficient mice. This is associated with elevated levels of I kappa B in alpha B-crystallin deficient cells and incomplete degradation upon TNF-alpha stimulation. Consistent with this, endothelial adhesion molecule expression is reduced in inflamed vessels of alpha B-crystallin deficient mice, and leukocyte rolling velocity is increased. Our data identify alpha B-crystallin as a new regulator of leukocyte recruitment, by enhancing pro-inflammatory nuclear factor kappa B-signaling and endothelial adhesion molecule expression during endothelial activation.

  • 7. Ebarasi, Lwaki
    et al.
    Gaengel, Konstantin
    Majumdar, Arindam
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Betsholtz, Christer
    Evidence for the presence of pericytes in the zebrafish2013In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 16, no 1, p. 273-273Article in journal (Other academic)
  • 8.
    Femel, Julia
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Huijbers, Elisabeth J. M.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Saupe, Falk
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Cedervall, Jessica
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Zhang, Lei
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Dimberg, Anna
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Hellman, Lars
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Chemical Biology.
    Progression of metastatic breast cancer can be attenuated by therapeutic vaccination against the tumor vascular marker ED-A2014In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 17, no 3, p. 769-769Article in journal (Other academic)
  • 9. Gaengel, Konstantin
    et al.
    Niaudet, Colin
    Hagikura, Kazuhiro
    Siemsen, Lavina Barbara
    Muhl, Lar
    Hofmann, J. Jennifer
    Ebarasi, Lwaki
    Nystrom, Staffan
    Rymo, Simin
    Long, Chen Long
    Mei-Fong, Pang
    Yi, Jin
    Raschperger, Elisabeth
    Roswall, Pernilla
    Schulte, Doerte
    Benedito, Rui
    Larsson, Jimmy
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Hellstrom, Mats
    Fuxe, Jonas
    Uhlen, Per
    Adams, Ralf
    Jakobsson, Lars
    Majumdar, Arindam
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Cancer and Vascular Biology.
    Vestweber, Dietmar
    Uv, Anne
    Betsholtz, Christer
    The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VE-cadherin and VEGFR22013In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 16, no 1, p. 246-247Article in journal (Other academic)
  • 10. Huijbers, Elisabeth J. M.
    et al.
    van Beijnum, Judy R.
    Kerkhoven, Ron M.
    de Rink, Iris A.
    Baban, S.
    Griffioen, Arjan W.
    Genomic screening of the embryo for novel targets in the tumor endothelium2014In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 17, no 3, p. 774-775Article in journal (Other academic)
  • 11.
    Kilarski, Witold W
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Petersson, Ludvig
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Fuchs, Peder Fredlund
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Zielinski, Marcin S
    Institute of Bioengineering and Swiss Institute of Experimental, Cancer Research (ISREC), École Polytechnique Fédérale de Lausanne (EPFL).
    Gerwins, Pär
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Radiology, Oncology and Radiation Science, Radiology.
    An in vivo neovascularization assay for screening regulators of angiogenesis and assessing their effects on pre-existing vessels2012In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 15, no 4, p. 643-655Article in journal (Refereed)
    Abstract [en]

    Therapeutic regulation of tissue vascularization has appeared as an attractive approach to treat a number of human diseases. In vivo neovascularization assays that reflect physiological and pathological formation of neovessels are important in this effort. In this report we present an assay where the effects of activators and inhibitors of angiogenesis can be quantitatively and qualitatively measured. A provisional matrix composed of collagen I and fibrin was formed in a plastic cylinder and implanted onto the chick chorioallantoic membrane. A nylon mesh separated the implanted matrix from the underlying tissue to distinguish new from pre-existing vessels. Vascularization of the matrix in response to fibroblast growth factor-2 or platelet-derived growth factor-BB was scored in a double-blinded manner, or vessel density was measured using a semi-automated image analysis procedure. Thalidomide, fumagillin, U0126 and TGFβ inhibited neovessel growth while hydrocortisone exerted a negative and wortmannin a toxic effect on the pre-existing vasculature. This quantitative, inexpensive and rapid in vivo angiogenesis assay might be a valuable tool in screening and characterizing factors that influence wound or tumor induced vascularization and in assessing their effects on the normal vasculature.

  • 12.
    Lidian, Adnan
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Surgical Sciences, Otolaryngology and Head and Neck Surgery.
    Necrosis of the upper lip, lateral nasal cartilage and forehead skin after embolization of a HHT patient2018In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 21, no 1, p. 145-145Article in journal (Other academic)
  • 13.
    Martinez-Corral, Ines
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Stanczuk, Lukas
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Frye, Maike
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Ulvmar, Maria Helena
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Diegez-Hurtado, Rodrigo
    Olmeda, David
    Mäkinen, Taija
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Ortega, Sagrario
    Vegfr3-CreER (T2) mouse, a new genetic tool for targeting the lymphatic system2016In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 19, no 3, p. 433-445Article in journal (Refereed)
    Abstract [en]

    The lymphatic system is essential in many physiological and pathological processes. Still, much remains to be known about the molecular mechanisms that control its development and function and how to modulate them therapeutically. The study of these mechanisms will benefit from better controlled genetic mouse models targeting specifically lymphatic endothelial cells. Among the genes expressed predominantly in lymphatic endothelium, Vegfr3 was the first one identified and is still considered to be one of the best lymphatic markers and a key regulator of the lymphatic system. Here, we report the generation of a Vegfr3-CreER (T2) knockin mouse by gene targeting in embryonic stem cells. This mouse expresses the tamoxifen-inducible CreER(T2) recombinase under the endogenous transcriptional control of the Vegfr3 gene without altering its physiological expression or regulation. The Vegfr3-CreER (T2) allele drives efficient recombination of floxed sequences upon tamoxifen administration specifically in Vegfr3-expressing cells, both in vitro, in primary lymphatic endothelial cells, and in vivo, at different stages of mouse embryonic development and postnatal life. Thus, our Vegfr3-CreER (T2) mouse constitutes a new powerful genetic tool for lineage tracing analysis and for conditional gene manipulation in the lymphatic endothelium that will contribute to improve our current understanding of this system.

  • 14.
    Niaudet, Colin
    et al.
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Petkova, Milena
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Jung, Bongnam
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Lu, S.
    Max Planck Inst Heart & Lung Res, Dept Pharmacol, D-61231 Bad Nauheim, Germany.
    Laviña, Bàrbara
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Offermanns, S.
    Max Planck Inst Heart & Lung Res, Dept Pharmacol, D-61231 Bad Nauheim, Germany.
    Brakebusch, C.
    Univ Copenhagen, Biotech Res & Innovat Ctr, Ole Maaloes Vej 5, DK-2200 Copenhagen, Denmark.
    Betsholtz, Christer
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Adgrf5 contributes to patterning of the endothelial deep layer in retina2019In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 22, no 4, p. 491-505Article in journal (Refereed)
    Abstract [en]

    Neovascularization of the inner retinal space is a major cause of vision loss. In retinal angiomatous proliferation (RAP) syndrome, newly formed vessels originate from the retinal plexus and invade the inner retinal space. However, the molecular pathways preventing subretinal vascularization remain largely unknown. In most murine models of RAP, pathological neo-vascularization occurs concomitantly with the development of the retinal vasculature. Here, we demonstrate that disturbing the sequence of morphogenetic events that shape the three-layered retinal vascular network leads to subretinal vascularization. Sprouts emerging from the perivenous region after the first postnatal week extended toward the retinal space where they merged into the deep layer. The small GTPase Rac1 was required for the formation of these vascular extensions and the vascular inner plexus is formed coaxially to the overarching veins. The adhesion receptor Adgrf5 was highly expressed in the endothelium of the central nervous system, where it regulates blood-brain barrier formation. The vascular superficial plexus of Adgrf5 mutant mouse retinae exhibited an increased vascular density in the perivenous areas with increased projections toward the inner plexus where they subsequently created hyper-dense endothelial cells (EC) clusters. Disturbing the perivenous pool of EC thus significantly altered the inner plexus formation. These abnormalities culminated in transient vascular protrusions in the inner retinal space. Taken together, these results reveal a previously unobserved vascular morphogenetic defect in Adgrf5 knockout mice, implicating a role for ADGRF5 in the initiation of subretinal vascularization. Our findings also illustrate how vein-derived EC shape the inner retinal layer formation and could control the appearance of angiomatous malformations.

  • 15.
    Nowak-Sliwinska, Patrycja
    et al.
    Univ Lausanne, Univ Geneva, Fac Sci, Mol Pharmacol Grp,Sch Pharmaceut Sci,CMU, Rue Michel Servet 1, CH-1211 Geneva 4, Switzerland;Univ Geneva, Translat Res Ctr Oncohaematol, Geneva, Switzerland.
    Alitalo, Kari
    Univ Helsinki, Wihuri Res Inst & Translat Canc Biol Program, Helsinki, Finland.
    Allen, Elizabeth
    Katholieke Univ Leuven, Dept Oncol, Lab Tumor Microenvironm & Therapeut Resistance, VIB Ctr Canc Biol, Louvain, Belgium.
    Anisimov, Andrey
    Univ Helsinki, Wihuri Res Inst & Translat Canc Biol Program, Helsinki, Finland.
    Aplin, Alfred C.
    Univ Washington, Dept Pathol, Seattle, WA 98195 USA.
    Auerbach, Robert
    Univ Wisconsin, Madison, WI USA.
    Augustin, Hellmut G.
    Heidelberg Univ, Med Fac Mannheim, European Ctr Angiosci, Heidelberg, Germany;German Canc Res Ctr, Div Vasc Oncol & Metastasis Res, Heidelberg, Germany;German Canc Consortium, Heidelberg, Germany.
    Bates, David O.
    Univ Nottingham, Sch Med, Div Canc & Stem Cells, Nottingham, England.
    van Beijnum, Judy R.
    Vrije Univ Amsterdam, Dept Med Oncol, Canc Ctr Amsterdam, Angiogenesis Lab,Med Ctr, Boelelaan 1117, NL-1081 HV Amsterdam, Netherlands.
    Bender, R. Hugh F.
    Univ Calif Irvine, Dept Mol Biol & Biochem, Irvine, CA 92717 USA.
    Bergers, Gabriele
    Katholieke Univ Leuven, Dept Oncol, Lab Tumor Microenvironm & Therapeut Resistance, VIB Ctr Canc Biol, Louvain, Belgium;Univ Calif San Francisco, Dept Neurol Surg, Brain Tumor Res Ctr,Dept Neurol Surg, Helen Diller Family Comprehens Canc Ctr, San Francisco, CA USA.
    Bikfalvi, Andreas
    Univ Bordeaux, Angiogenesis & Tumor Microenvironm Lab, INSERM, U1029, Pessac, France.
    Bischoff, Joyce
    Harvard Med Sch, Boston Childrens Hosp, Vasc Biol Program, Boston, MA USA;Harvard Med Sch, Boston Childrens Hosp, Dept Surg, Boston, MA USA.
    Boeck, Barbara C.
    Heidelberg Univ, Med Fac Mannheim, European Ctr Angiosci, Heidelberg, Germany;German Canc Res Ctr, Div Vasc Oncol & Metastasis Res, Heidelberg, Germany;German Canc Consortium, Heidelberg, Germany.
    Brooks, Peter C.
    Maine Med Ctr Res Inst, Ctr Mol Med, Scarborough, ME USA.
    Bussolino, Federico
    Univ Torino, Dept Oncol, Turin, Italy;Candiolo Canc Inst FPO IRCCS, I-10060 Candiolo, Italy.
    Cakir, Bertan
    Harvard Med Sch, Boston Childrens Hosp, Dept Ophthalmol, Boston, MA USA.
    Carmeliet, Peter
    Katholieke Univ Leuven, Dept Oncol, Lab Angiogenesis & Vasc Metab, Leuven, Belgium;Katholieke Univ Leuven, Leuven Canc Inst LKI, Leuven, Belgium;VIB, Ctr Canc Biol, Lab Angiogenesis & Vasc Metab, Leuven, Belgium.
    Castranova, Daniel
    Eunice Kennedy Shriver Natl Inst Child Hlth & Hum, Div Dev Biol, NIH, Bethesda, MD USA.
    Cimpean, Anca M.
    Victor Babes Univ Med & Pharm, Dept Microscop Morphol Histol, Angiogenesis Res Ctr, Timisoara, Romania.
    Cleaver, Ondine
    Univ Texas Southwestern Med Ctr Dallas, Dept Mol Biol, Ctr Regenerat Sci & Med, Dallas, TX 75390 USA.
    Coukos, George
    Univ Lausanne, Ludwig Inst Canc Res, Dept Oncol, Lausanne, Switzerland.
    Davis, George E.
    Univ Missouri, Sch Med, Dept Med Pharmacol & Physiol, Columbia, MO USA;Dalton Cardiovasc Ctr, Columbia, MO USA.
    De Palma, Michele
    Swiss Fed Inst Technol, Sch Life Sci, Lausanne, Switzerland.
    Dimberg, Anna
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Immunology, Genetics and Pathology, Vascular Biology.
    Dings, Ruud P. M.
    Univ Arkansas Med Sci, Dept Radiat Oncol, Little Rock, AR 72205 USA.
    Djonov, Valentin
    Univ Bern, Inst Anat, Bern, Switzerland.
    Dudley, Andrew C.
    Univ Virginia, Dept Microbiol Immunol & Canc Biol, Charlottesville, VA USA;Univ Virginia, Emily Cour Canc Ctr, Charlottesville, VA USA.
    Dufton, Neil P.
    Imperial Coll London, Vasc Sci, Imperial Ctr Translat & Expt Med, Natl Heart & Lung Inst, London, England.
    Fendt, Sarah-Maria
    VIB Ctr Canc Biol, Lab Cellular Metab & Metab Regulat, Leuven, Belgium;Katholieke Univ Leuven, Lab Cellular Metab & Metab Regulat, Dept Oncol, Leuven, Belgium;Leuven Canc Inst, Leuven, Belgium.
    Ferrara, Napoleone
    Univ Calif San Diego, La Jolla, CA 92093 USA.
    Fruttiger, Marcus
    UCL, Inst Ophthalmol, London, England.
    Fukumura, Dai
    Massachusetts Gen Hosp, Dept Radiat Oncol, Edwin L Steele Labs, Boston, MA 02114 USA;Harvard Med Sch, Boston, MA 02114 USA.
    Ghesquiere, Bart
    VIB, VIB Ctr Canc Biol, Metabol Expertise Ctr, Leuven, Belgium;Katholieke Univ Leuven, Dept Oncol, Metabol Expertise Ctr, Leuven, Belgium.
    Gong, Yan
    Harvard Med Sch, Boston Childrens Hosp, Dept Ophthalmol, Boston, MA USA.
    Griffin, Robert J.
    Univ Arkansas Med Sci, Dept Radiat Oncol, Little Rock, AR 72205 USA.
    Harris, Adrian L.
    Univ Oxford, John Radcliffe Hosp, Mol Oncol Labs, Weatherall Inst Mol Med,Dept Oncol, Oxford, England.
    Hughes, Christopher C. W.
    Univ Calif Irvine, Dept Mol Biol & Biochem, Irvine, CA 92717 USA.
    Hultgren, Nan W.
    Univ Calif Irvine, Dept Mol Biol & Biochem, Irvine, CA 92717 USA.
    Iruela-Arispe, M. Luisa
    Univ Calif Los Angeles, MCDB, Los Angeles, CA USA.
    Irving, Melita
    Univ Lausanne, Ludwig Inst Canc Res, Dept Oncol, Lausanne, Switzerland.
    Jain, Rakesh K.
    Massachusetts Gen Hosp, Dept Radiat Oncol, Edwin L Steele Labs, Boston, MA 02114 USA;Harvard Med Sch, Boston, MA 02114 USA.
    Kalluri, Raghu
    Univ Texas MD Anderson Canc Ctr, Dept Canc Biol, Metastasis Res Ctr, Houston, TX 77030 USA.
    Kalucka, Joanna
    Katholieke Univ Leuven, Dept Oncol, Lab Angiogenesis & Vasc Metab, Leuven, Belgium;Katholieke Univ Leuven, Leuven Canc Inst LKI, Leuven, Belgium;VIB, Ctr Canc Biol, Lab Angiogenesis & Vasc Metab, Leuven, Belgium.
    Kerbel, Robert S.
    Univ Toronto, Dept Med Biophys, Sunnybrook Res Inst, Biol Sci Platform, Toronto, ON, Canada.
    Kitajewski, Jan
    Univ Illinois, Dept Physiol & Biophys, Chicago, IL 60680 USA.
    Klaassen, Ingeborg
    Univ Amsterdam, Ocular Angiogenesis Grp, Dept Ophthalmol, Acad Med Ctr, Amsterdam, Netherlands;Univ Amsterdam, Ocular Angiogenesis Grp, Dept Med Biol, Acad Med Ctr, Amsterdam, Netherlands.
    Kleinmann, Hynda K.
    George Washington Univ, Sch Med, Washington, DC USA.
    Koolwijk, Pieter
    Univ Lausanne, Dept Ophthalmol, Jules Gonin Eye Hosp, Fdn Asile Aveugles, Lausanne, Switzerland.
    Kuczynski, Elisabeth
    Univ Toronto, Dept Med Biophys, Sunnybrook Res Inst, Biol Sci Platform, Toronto, ON, Canada.
    Kwak, Brenda R.
    Univ Geneva, Dept Pathol & Immunol, Geneva, Switzerland.
    Marien, Koen
    HistoGeneX, Antwerp, Belgium.
    Melero-Martin, Juan M.
    Harvard Med Sch, Boston Childrens Hosp, Dept Cardiac Surg, Boston, MA USA.
    Munn, Lance L.
    Massachusetts Gen Hosp, Dept Radiat Oncol, Edwin L Steele Labs, Boston, MA 02114 USA;Harvard Med Sch, Boston, MA 02114 USA.
    Nicosia, Roberto F.
    Univ Washington, Dept Pathol, Seattle, WA 98195 USA;VA Puget Sound Hlth Care Syst, Pathol & Lab Med Serv, Seattle, WA USA.
    Noel, Agnes
    Univ Liege, Lab Tumor & Dev Biol, GIGA Canc, Liege, Belgium.
    Nurro, Jussi
    Univ Eastern Finland, Dept Biotechnol & Mol Med, Kuopio, Finland.
    Olsson, Anna-Karin
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology. Uppsala University, Science for Life Laboratory, SciLifeLab.
    Petrova, Tatiana V.
    Ludwig Inst Canc Res Lausanne, Dept Oncol UNIL CHUV, Lausanne, Switzerland.
    Pietras, Kristian
    Dept Lab Med, Div Translat Canc Res, Lund, Sweden.
    Pili, Roberto
    Indiana Univ, Simon Canc Ctr, Genitourinary Program, Indianapolis, IN 46204 USA.
    Pollard, Jeffrey W.
    Univ Edinburgh, Med Res Council, Ctr Reprod Hlth, Coll Med & Vet Med, Edinburgh, Midlothian, Scotland.
    Post, Mark J.
    Maastricht Univ, Dept Physiol, Maastricht, Netherlands.
    Quax, Paul H. A.
    LUMC, Einthoven Lab Expt Vasc Med, Dept Surg, Leiden, Netherlands.
    Rabinovich, Gabriel A.
    Consejo Nacl Invest Cient & Tecn, Natl Council Sci & Tech Invest, Lab Immunopathol, Inst Biol & Expt Med, Buenos Aires, DF, Argentina.
    Raica, Marius
    Victor Babes Univ Med & Pharm, Dept Microscop Morphol Histol, Angiogenesis Res Ctr, Timisoara, Romania.
    Randi, Anna M.
    Imperial Coll London, Vasc Sci, Imperial Ctr Translat & Expt Med, Natl Heart & Lung Inst, London, England.
    Ribatti, Domenico
    Univ Bari, Med Sch, Dept Basic Med Sci Neurosci & Sensory Organs, Bari, Italy;Natl Canc Inst Giovanni Paolo II, Bari, Italy.
    Ruegg, Curzio
    Univ Fribourg, Dept Oncol Microbiol & Immunol, Fac Sci & Med, Fribourg, Switzerland.
    Schlingemann, Reinier O.
    Univ Amsterdam, Ocular Angiogenesis Grp, Dept Ophthalmol, Acad Med Ctr, Amsterdam, Netherlands;Univ Amsterdam, Ocular Angiogenesis Grp, Dept Med Biol, Acad Med Ctr, Amsterdam, Netherlands;Univ Lausanne, Dept Ophthalmol, Jules Gonin Eye Hosp, Fdn Asile Aveugles, Lausanne, Switzerland.
    Schulte-Merker, Stefan
    WWU, Inst Cardiovasc Organogenesis & Regenerat, Fac Med, Munster, Germany.
    Smith, Lois E. H.
    Harvard Med Sch, Boston Childrens Hosp, Dept Ophthalmol, Boston, MA USA.
    Song, Jonathan W.
    Ohio State Univ, Dept Mech & Aerosp Engn, Columbus, OH 43210 USA;Ohio State Univ, Ctr Comprehens Canc, Columbus, OH 43210 USA.
    Stacker, Steven A.
    Univ Melbourne, Tumour Angiogenesis & Microenvironm Program, Peter MacCallum Canc Ctr & Sir Peter MacCallum, Dept Oncol, Melbourne, Vic, Australia.
    Stalin, Jimmy
    WWU, Inst Cardiovasc Organogenesis & Regenerat, Fac Med, Munster, Germany.
    Stratman, Amber N.
    Eunice Kennedy Shriver Natl Inst Child Hlth & Hum, Div Dev Biol, NIH, Bethesda, MD USA.
    Van de Velde, Maureen
    Univ Liege, Lab Tumor & Dev Biol, GIGA Canc, Liege, Belgium.
    van Hinsbergh, Victor W. M.
    Univ Lausanne, Dept Ophthalmol, Jules Gonin Eye Hosp, Fdn Asile Aveugles, Lausanne, Switzerland.
    Vermeulen, Peter B.
    HistoGeneX, Antwerp, Belgium;Sint Augustinus & Univ Antwerp, Translat Canc Res Unit, GZA Hosp, Antwerp, Belgium.
    Waltenberger, Johannes
    Univ Munster, Med Fac, Albert Schweitzer Campus 1, Munster, Germany.
    Weinstein, Brant M.
    Eunice Kennedy Shriver Natl Inst Child Hlth & Hum, Div Dev Biol, NIH, Bethesda, MD USA.
    Xin, Hong
    Univ Calif San Diego, La Jolla, CA 92093 USA.
    Yetkin-Arik, Bahar
    Univ Amsterdam, Ocular Angiogenesis Grp, Dept Ophthalmol, Acad Med Ctr, Amsterdam, Netherlands;Univ Amsterdam, Ocular Angiogenesis Grp, Dept Med Biol, Acad Med Ctr, Amsterdam, Netherlands.
    Yla-Herttuala, Seppo
    Univ Eastern Finland, Dept Biotechnol & Mol Med, Kuopio, Finland.
    Yoder, Mervin C.
    Indiana Univ Sch Med, Dept Pediat, Indianapolis, IN 46202 USA.
    Griffioen, Arjan W.
    Vrije Univ Amsterdam, Dept Med Oncol, Canc Ctr Amsterdam, Angiogenesis Lab,Med Ctr, Boelelaan 1117, NL-1081 HV Amsterdam, Netherlands.
    Consensus guidelines for the use and interpretation of angiogenesis assays2018In: Angiogenesis, ISSN 0969-6970, E-ISSN 1573-7209, Vol. 21, no 3, p. 425-532Article, review/survey (Refereed)
    Abstract [en]

    The formation of new blood vessels, or angiogenesis, is a complex process that plays important roles in growth and development, tissue and organ regeneration, as well as numerous pathological conditions. Angiogenesis undergoes multiple discrete steps that can be individually evaluated and quantified by a large number of bioassays. These independent assessments hold advantages but also have limitations. This article describes in vivo, ex vivo, and in vitro bioassays that are available for the evaluation of angiogenesis and highlights critical aspects that are relevant for their execution and proper interpretation. As such, this collaborative work is the first edition of consensus guidelines on angiogenesis bioassays to serve for current and future reference.

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