Pericytes in the mature chorioallantoic membrane capillary plexus contain desmin and α-smooth muscle actin: Relevance for non-sprouting angiogenesis

Histochemistry and Cell Biology

Volumn 130, Issue 5, 2008, Pages 1027-1040

  Kurz, Haymo ^a   Fehr, Janis ^b   Nitschke, Roland ^b   Burkhardt, Hans ^b  

^a PARACELSUS MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Smooth muscle actin; Avian embryo; Cell classification; Desmin; Endothelium; Leukocyte; Lymphatics; Multichannel imaging; Pericyte; Sambucus nigra agglutinin; Vascular smooth muscle cell; YoPro 1

Indexed keywords

AGGLUTININ; ALPHA SMOOTH MUSCLE ACTIN; CYTOSKELETON PROTEIN; DESMIN; DNA;

ANGIOGENESIS; ARTICLE; CAPILLARY; CELL LABELING; CELL MATURATION; CELL TYPE; CHICKEN; CHORIOALLANTOIS; FLUOROCHROME STAINING; IMMUNOHISTOCHEMISTRY; NONHUMAN; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SAMBUCUS NIGRA;

ACTINS; ANIMALS; CAPILLARIES; CELL NUCLEUS; CHICK EMBRYO; CHICKENS; CHORIOALLANTOIC MEMBRANE; DESMIN; DNA; FLUORESCENT ANTIBODY TECHNIQUE; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES;

AVES; SAMBUCUS NIGRA;

EID: 54049100317     PISSN: 09486143     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00418-008-0478-8     Document Type: Article

References (64)

1. HG Augustin 2001 Tubes, branches, and pillars: the many ways of forming a new vasculature Circ Res 89 645 647
2. K Bartha H Rieger 2006 Vascular network remodeling via vessel cooption, regression and growth in tumors J Theor Biol 241 903 918
3. AM Boriek Y Capetanaki W Hwang T Officer M Badshah J Rodarte JG Tidball 2001 Desmin integrates the three-dimensional mechanical properties of muscles Am J Physiol Cell Physiol 280 C46 C52
4. PH Burri 1992 Intussusceptive microvascular growth, a new mechanism of capillary network formation EXS 61 32 39
5. PH Burri R Hlushchuk V Djonov 2004 Intussusceptive angiogenesis: its emergence, its characteristics, and its significance Dev Dyn 231 474 488
6. PH Burri MR Tarek 1990 A novel mechanism of capillary growth in the rat pulmonary microcirculation Anat Rec 228 35 45
7. JH Caduff LC Fischer PH Burri 1986 Scanning electron microscope study of the developing microvasculature in the postnatal rat lung Anat Rec 216 154 164
8. Y Capetanaki RJ Bloch A Kouloumenta M Mavroidis S Psarras 2007 Muscle intermediate filaments and their links to membranes and membranous organelles Exp Cell Res 313 2063 2076
9. T Chan-Ling MP Page T Gardiner L Baxter E Rosinova S Hughes 2004 Desmin ensheathment ratio as an indicator of vessel stability: evidence in normal development and in retinopathy of prematurity Am J Pathol 165 1301 1313
10. PH Cossmann PS Eggli B Christ H Kurz 1997 Mesoderm-derived cells proliferate in the embryonic central nervous system: confocal microscopy and three-dimensional visualization Histochem Cell Biol 107 205 213
11. PH Cossmann PS Eggli H Kurz 2000 Three-dimensional analysis of DNA replication foci: a comparative study on species and cell type in situ Histochem Cell Biol 113 195 295
12. V Djonov O Baum PH Burri 2003 Vascular remodeling by intussusceptive angiogenesis Cell Tissue Res 314 107 117
13. V Djonov M Schmid SA Tschanz PH Burri 2000 Intussusceptive angiogenesis: its role in embryonic vascular network formation Circ Res 86 286 292
14. VG Djonov AB Galli PH Burri 2000 Intussusceptive arborization contributes to vascular tree formation in the chick chorio-allantoic membrane Anat Embryol (Berl) 202 347 357
15. VG Djonov H Kurz PH Burri 2002 Optimality in the developing vascular system: branching remodeling by means of intussusception as an efficient adaptation mechanism Dev Dyn 224 391 402
16. E Ehler G Karlhuber HC Bauer A Draeger 1995 Heterogeneity of smooth muscle-associated proteins in mammalian brain microvasculature Cell Tissue Res 279 393 403
17. J Fehr H Burkhardt 2006 Phase based 3D texture features Lect Not Comp Sci 4174 263 272
18. J Fehr O Ronneberger H Kurz H Burkhardt 2005 Self-learning segmentation and classification of cell nuclei in 3D volumetric data using voxel-wise gray scale invariants Lect Not Comp Sci 3663 377 384
19. MG Gabrielli JV Cox G Materazzi G Menghi 2004 Cell type-specific and developmentally regulated expression of the AE1 anion exchanger in the chicken chorioallantoic membrane Histochem Cell Biol 121 189 199
20. MG Gabrielli G Materazzi AM Bondi G Menghi 2003 Developmental expression of glycocomponents in the chick chorioallantoic membrane Anat Embryol (Berl) 207 63 71
21. R Gödde H Kurz 2001 Structural and biophysical simulation of angiogenesis and vascular remodeling Dev Dyn 220 387 401
22. M Hagedorn M Balke A Schmidt W Bloch H Kurz S Javerzat B Rousseau J Wilting A Bikfalvi 2004 VEGF coordinates interaction of pericytes and endothelial cells during vasculogenesis and experimental angiogenesis Dev Dyn 230 23 33
23. Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A, Bikfalvi A (2005) Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci USA 102:1643-1648
24. R Hlushchuk O Baum G Gruber J Wood V Djonov 2007 The synergistic action of a VEGF-receptor tyrosine-kinase inhibitor and a sensitizing PDGF-receptor blocker depends upon the stage of vascular maturation Microcirculation 14 813 825
25. I Izawa M Inagaki 2006 Regulatory mechanisms and functions of intermediate filaments: a study using site- and phosphorylation state-specific antibodies Cancer Sci 97 167 174
26. J Korn B Christ H Kurz 2002 Neuroectodermal origin of brain pericytes and vascular smooth muscle cells J Comp Neurol 442 78 88
27. H Kurz S Ambrosy J Wilting D Marmé B Christ 1995 Proliferation pattern of capillary endothelial cells in chorioallantoic membrane development indicates local growth control, which is counteracted by vascular endothelial growth factor application Dev Dyn 203 174 186
28. H Kurz PH Burri VG Djonov 2003 Angiogenesis and vascular remodeling by intussusception: from form to function News Physiol Sci 18 65 70
29. H Kurz J Fehr R Nitschke H Burkhardt 2007 Two types of pericytes in the chorioallantoic membrane capillary plexus? Ann Anat 103 18
30. H Kurz J Fehr S Winnik M Moser O Ronneberger H Burkhardt 2005 Dynamics of vascular cells in their social context: quantitative 3-D-analysis of vasculargrowth and remodeling and new insights into mechanisms of angiogenesis Ann Anat 100 74
31. H Kurz T Gärtner PS Eggli B Christ 1996 First blood vessels in the avian neural tube are formed by a combination of dorsal angioblast immigration and ventral sprouting of endothelial cells Dev Biol 173 133 147
32. H Kurz J Korn PS Eggli R Huang B Christ 2001 Embryonic CNS angiogenesis does not involve blood-borne endothelial progenitors J Comp Neurol 436 263 274
33. H Kurz J Korn M Papoutsi B Christ G Wieczorek U Nuber 2004 Plasticity of grafted murine bone marrow stromal, trophoblast stem, and human melanoma cells and their interactions with avian chorioallantoic membrane (CAM) vasculature Ann Anat 99 43
34. H Kurz D Lauer M Papoutsi B Christ J Wilting 2002 Pericytes in experimental MDA-MB231 tumor angiogenesis Histochem Cell Biol 117 527 534
35. H Kurz J Wilting K Sandau B Christ 1998 Automated evaluation of angiogenic effects mediated by VEGF and PlGF homo- and heterodimers Microvasc Res 55 92 102
36. E Larger M Marre P Corvol JM Gasc 2004 Hyperglycemia-induced defects in angiogenesis in the chicken chorioallantoic membrane model Diabetes 53 752 761
37. L Loufrani D Henrion 2008 Role of the cytoskeleton in flow (shear stress)-induced dilation and remodeling in resistance arteries Med Biol Eng Comput 46 451 460
38. C Lugassy HK Kleinman SE Vernon DR Welch RL Barnhill 2007 C16 laminin peptide increases angiotropic extravascular migration of human melanoma cells in a shell-less chick chorioallantoic membrane assay Br J Dermatol 157 780 782
39. K Matschke L Da Silva-Azevedo R Hlushchuk V Djonov O Baum 2006 Annexins as cell-type-specific markers in the developing chicken chorionallantoic membrane Cell Tissue Res 323 395 404
40. DM McDonald PL Choyke 2003 Imaging of angiogenesis: from microscope to clinic Nat Med 9 713 725
41. V Nehls D Drenckhahn 1991 Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin J Cell Biol 113 147 154
42. B Nico MG Ennas E Crivellato A Frontino D Mangieri M De Giorgis L Roncali D Ribatti 2004 Desmin-positive pericytes in the chick embryo chorioallantoic membrane in response to fibroblast growth factor-2 Microvasc Res 68 13 19
43. WS Noble 2006 What is a support vector machine? Nat Biotechnol 24 1565 1567
44. M Oates R Chen M Duncan JA Hunt 2007 The angiogenic potential of three-dimensional open porous synthetic matrix materials Biomaterials 28 3679 3686
45. SJ Oh H Kurz B Christ J Wilting 1998 Platelet-derived growth factor-B induces transformation of fibrocytes into spindle-shaped myofibroblasts in vivo Histochem Cell Biol 109 349 357
46. M Papoutsi H Kurz C Schächtele D Marmé B Christ F Pröls J Wilting 2000 Induction of the blood-brain barrier marker neurothelin/HT7 in endothelial cells by a variety of tumors in chick embryos Histochem Cell Biol 113 105 113
47. P Parsons-Wingerter TL McKay D Leontiev MB Vickerman TK Condrich PE Dicorleto 2006 Lymphangiogenesis by blind-ended vessel sprouting is concurrent with hemangiogenesis by vascular splitting Anat Rec A Discov Mol Cell Evol Biol 288 233 247
48. S Patan 1998 TIE1 and TIE2 receptor tyrosine kinases inversely regulate embryonic angiogenesis by the mechanism of intussusceptive microvascular growth Microvasc Res 56 1 21
49. S Patan B Haenni PH Burri 1993 Evidence for intussusceptive capillary growth in the chicken chorio-allantoic membrane (CAM) Anat Embryol (Berl) 187 121 130
50. S Patan B Haenni PH Burri 1996 Implementation of intussusceptive microvascular growth in the chicken chorioallantoic membrane (CAM): 1. pillar formation by folding of the capillary wall Microvasc Res 51 80 98
51. M Pekny EB Lane 2007 Intermediate filaments and stress Exp Cell Res 313 2244 2254
52. E Ralston Z Lu N Biscocho E Soumaka M Mavroidis C Prats T Lomo Y Capetanaki T Ploug 2006 Blood vessels and desmin control the positioning of nuclei in skeletal muscle fibers J Cell Physiol 209 874 882
53. D Ribatti B Nico A Vacca L Roncali PH Burri V Djonov 2001 Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo Anat Rec 264 317 324
54. O Ronneberger J Fehr H Burkhardt 2005 Voxel-wise gray scale invariants for simultaneous segmentation and classification Lect Not Comp Sci 3663 85 92
55. K Sandau H Kurz 1994 Modelling of vascular growth processes: a stochastic biophysical approach to embryonic angiogenesis J Microsc 175 Pt 3 205 213
56. P Schlatter MF Konig LM Karlsson PH Burri 1997 Quantitative study of intussusceptive capillary growth in the chorioallantoic membrane (CAM) of the chicken embryo Microvasc Res 54 65 73
57. J Schulz T Schmidt O Ronneberger H Burkhardt T Pasternak A Dovzhenko K Palme 2006 Fast scalar and vectorial grayscale based invariant features for 3D cell nuclei localization and classification Lect Not Comp Sci 4174 182 191
58. D Szczerba G Szekely 2005 Computational model of flow-tissue interactions in intussusceptive angiogenesis J Theor Biol 234 87 97
59. D Szczerba G Szekely H Kurz 2006 A multiphysics model of capillary growth and remodeling Lect Not Comp Sci 3992 86 93
60. DD Tang 2008 Intermediate filaments in smooth muscle Am J Physiol Cell Physiol 294 C869 C878
61. J Wilting R Birkenhäger A Eichmann H Kurz G Martiny-Baron D Marmé JE McCarthy B Christ HA Weich 1996 VEGF121 induces proliferation of vascular endothelial cells and expression of flk-1 without affecting lymphatic vessels of chorioallantoic membrane Dev Biol 176 76 85
62. J Wilting B Christ M Bokeloh HA Weich 1993 In vivo effects of vascular endothelial growth factor on the chicken chorioallantoic membrane Cell Tissue Res 274 163 172
63. S Winters-Hilt A Yelundur C McChesney M Landry 2006 Support Vector Machine Implementations for Classification & Clustering BMC Bioinformatics 7 Suppl 2 S4
64. G Zwadlo-Klarwasser K Gorlitz B Hafemann D Klee B Klosterhalfen 2001 The chorioallantoic membrane of the chick embryo as a simple model for the study of the angiogenic and inflammatory response to biomaterials J Mater Sci Mater Med 12 195 199