Transforming growth factor beta 1-induced changes in cell migration, proliferation, and angiogenesis in the chicken chorioallantoic membrane.
Open accessAbstract
Application of TGF beta 1 (10-100 ng) to the chicken chorioallantoic membrane (CAM) for 72 h resulted in a dose-dependent, gross angiogenic response. The vascular effects induced by TGF beta 1 were qualitatively different than those induced by maximal doses of basic FGF (bFGF) (500 ng). While TGF beta 1 induced the formation of large blood vessels by 72 h, bFGF induced primarily small blood vessels. Histologic analysis revealed that TGF beta 1 stimulated pleiotropic cellular responses in the CAM. Increases in fibroblast and epithelial cell density in the area of TGF beta 1 delivery were observed as early as 4 h after TGF beta 1 treatment. By 8 h, these cell types also demonstrated altered morphology and marked inhibition of proliferation as evidenced by 3H-thymidine labeling. Thus, the TGF beta 1-stimulated accumulation of these cell types was the result of cellular chemotaxis from peripheral areas into the area of TGF beta 1 delivery. Microscopic angiogenesis in the form of capillary sprouts and increased endothelial cell density first became evident at 16 h. By 24 h, capillary cords appeared within the mesenchyme of the CAM, extending towards the point of TGF beta 1 delivery. 3H-thymidine labeling revealed that the growth of these capillary cords was due to endothelial cell proliferation. Finally, perivascular mononuclear inflammation did not become evident until 48 h of treatment, and its presence correlated spatially and temporally with the gross and histological remodelling of newly formed capillary cords into larger blood vessels. In summary, these data suggest that, in the chicken CAM, TGF beta 1 initiates a sequence of cellular responses that results in growth inhibition, cellular accumulation through migration, and microvascular angiogenesis.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
TGF-β secreted by endothelial cells promotes recruitment of perivascular pericytes and myofibroblasts that support functional vascular integrity.
“Additionally, TGF-β secreted by endothelial cells promotes recruitment of perivascular pericytes and myofibroblasts that support functional vascular integrity273”
From TGFβ biology in cancer progression and immunotherapy (2021) · cites this paper as [273]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Roberts, A. B., Sporn, M. B., Assoian, R. K., Smith, J. M., Roche, N. S., Wakefield, L. M., Heine, U., Liotta, L. A., Falanga, V., & Kehrl, J. H. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.12.4167 · Cited by 2,867 · see citing works
Ignotz, R. A., & Massagué, J. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)35666-1 · Cited by 2,492 · see citing works
Kehrl, J. H., Wakefield, L. M., Roberts, A. B., Jakowlew, S. B., Álvarez‐Mon, M., Derynck, R., Sporn, M. B., & Fauci, A. S. (1986) · The Journal of Experimental Medicine · doi:10.1084/jem.163.5.1037 · Cited by 1,581 · see citing works
The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum.
(1975) · PubMed Central · Cited by 1,437 · see citing works
Ausprunk, D. H., & Folkman, J. (1977) · Microvascular Research · doi:10.1016/0026-2862(77)90141-8 · Cited by 1,290 · see citing works
Transforming growth factor type beta induces monocyte chemotaxis and growth factor production.
Wahl, S. M., Hunt, D. A., Wakefield, L. M., McCartney-Francis, N. L., Wahl, L. M., Roberts, A. B., & Sporn, M. B. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.16.5788 · Cited by 1,273 · see citing works
Folkman, J. (1985) · Advances in cancer research · doi:10.1016/s0065-230x(08)60946-x · Cited by 1,071 · see citing works
Expression and secretion of type beta transforming growth factor by activated human macrophages.
Assoian, R. K., Fleurdelys, B. E., Stevenson, H. C., Miller, P. J., Madtes, D. K., Raines, E. W., Ross, R., & Sporn, M. B. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.17.6020 · Cited by 958 · see citing works
Accelerated Healing of Incisional Wounds in Rats Induced by Transforming Growth Factor-β
Mustoe, T. A., Pierce, G. F., Thomason, A., Gramates, P. H., Sporn, M. B., & Deuel, T. F. (1987) · Science · doi:10.1126/science.2442813 · Cited by 930 · see citing works
Roberts, A. B., Anzano, M. A., Lamb, L. C., Smith, J. M., & Sporn, M. B. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.9.5339 · Cited by 919 · see citing works
Activated macrophages induce vascular proliferation
Polverini, P. J., Cotran, R. S., Gimbrone, M. A., & Unanue, E. R. (1977) · Nature · doi:10.1038/269804a0 · Cited by 805 · see citing works
Stimulation of the chemotactic migration of human fibroblasts by transforming growth factor beta.
Postlethwaite, A. E., Keski-Oja, J., Moses, H. L., & Kang, A. H. (1987) · The Journal of experimental medicine · doi:10.1084/jem.165.1.251 · Cited by 777 · see citing works
Self-citationRole of transforming growth factor-beta in the development of the mouse embryo.
Heine, U., Munoz, E. F., Flanders, K. C., Ellingsworth, L. R., Lam, H. Y., Thompson, N. L., Roberts, A. B., & Sporn, M. B. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.6.2861 · Cited by 739 · see citing works
Folkman, J., Langer, R., Linhardt, R. J., Haudenschild, C. C., & Taylor, S. (1983) · Science · doi:10.1126/science.6192498 · Cited by 619 · see citing works
Pierce, G. F., Mustoe, T. A., Lingelbach, J., Masakowski, V. R., Griffin, G. L., Senior, R. M., & Deuel, T. F. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.1.429 · Cited by 591 · see citing works
Protamine is an inhibitor of angiogenesis
Taylor, S., & Folkman, J. (1982) · Nature · doi:10.1038/297307a0 · Cited by 580 · see citing works
Madri, J. A., Pratt, B. M., & Tucker, A. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.106.4.1375 · Cited by 570 · see citing works
Assoian, R. K., & Sporn, M. B. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.4.1217 · Cited by 545 · see citing works
Leof, E. B., Proper, J. A., Goustin, A. S., Shipley, G. D., DiCorleto, P. E., & Moses, H. L. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.8.2453 · Cited by 529 · see citing works
Self-citationTransforming growth factor production by chemically transformed cells.
Moses, H. L., Branum, E. L., Proper, J. A., & Robinson, R. A. (1981) · PubMed · Cited by 497 · see citing works
Self-citationMignatti, P., Tsuboi, R., Robbins, E. S., & Rifkin, D. B. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.2.671 · Cited by 453 · see citing works
A simple procedure for the long-term cultivation of chicken embryos
Auerbach, R., Kubai, L., Knighton, D. R., et al. (1974) · Developmental Biology · doi:10.1016/0012-1606(74)90316-9 · Cited by 443 · see citing works
Fine, A., & Goldstein, R. H. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)61441-3 · Cited by 395 · see citing works
Transforming growth factors and the regulation of cell proliferation
Lyons, R. M., & Moses, H. L. (1990) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1990.tb15327.x · Cited by 382 · see citing works
Self-citationSaksela, O., Moscatelli, D., & Rifkin, D. B. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.2.957 · Cited by 371 · see citing works
Serum contains a platelet-derived transforming growth factor.
Childs, C. B., Proper, J. A., Tucker, R. F., & Moses, H. L. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.17.5312 · Cited by 330 · see citing works
Self-citationInhibitory action of transforming growth factor beta on endothelial cells.
Müller, G., Behrens, J., Nussbaumer, U., Böhlen, P., & Birchmeier, W. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.16.5600 · Cited by 320 · see citing works
Baird, A., & Durkin, T. (1986) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(86)90305-0 · Cited by 308 · see citing works
Transforming growth factor-beta inhibits endothelial cell proliferation
Fràter‐Schröder, M., Müller, G. I., Birchmeier, W., & Böhlen, P. (1986) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(86)91209-x · Cited by 307 · see citing works
Pierce, G. F., Mustoe, T. A., Lingelbach, J., Masakowski, V. R., Gramates, P. H., & Deuel, T. F. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.7.2229 · Cited by 301 · see citing works
Production of transforming growth factor beta by human peripheral blood monocytes and neutrophils
Grotendorst, G. R., Smale, G., & Pencev, D. (1989) · Journal of Cellular Physiology · doi:10.1002/jcp.1041400226 · Cited by 262 · see citing works
Corpus Luteum Angiogenic Factor Is Related to Fibroblast Growth Factor*
Gospodarowicz, D., CHENG, J., Lui, G. M., et al. (1985) · Endocrinology · doi:10.1210/endo-117-6-2383 · Cited by 259 · see citing works
Promotion of wound repair in old mice by local injection of macrophages.
Danon, D., Kowatch, M. A., & Roth, G. S. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.6.2018 · Cited by 257 · see citing works
Roberts, A. B., Flanders, K. C., Kondaiah, P., THOMPSON, N. L., Obberghen‐Schilling, E. V., Wakefield, L. M., Rossi, P., Crombrugghe, B. D., Heine, U., & Sporn, M. B. (1988) · Elsevier eBooks · doi:10.1016/b978-0-12-571144-9.50010-7 · Cited by 254 · see citing works
Effects of growth factors in vivo. I. Cell ingrowth into porous subcutaneous chambers.
Sprugel, K. H., McPherson, J. M., Clowes, A. W., & Ross, R. (1987) · PubMed Central · Cited by 235 · see citing works
Angiogenesis is stimulated by a tumor‐derived endothelial cell growth factor
Shing, Y., Folkman, J., Haudenschild, C. C., Lund, D. P., Crum, R. M., & Klagsbrun, M. (1985) · Journal of Cellular Biochemistry · doi:10.1002/jcb.240290402 · Cited by 203 · see citing works
Expression of transforming growth factor β2 RNA during murine embryogenesis
Pelton, R. W., Nomura, S., Moses, H. L., & Hogan, B. L. M. (1989) · Development · doi:10.1242/dev.106.4.759 · Cited by 200 · see citing works
Self-citationShipley, G. D., Tucker, R. F., & Moses, H. L. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.12.4147 · Cited by 191 · see citing works
Self-citationThe Reversal of an Adriamycin® Induced Healing Impairment with Chemoattractants and Growth Factors
Lawrence, W., Sporn, M. B., Gorschboth, C. M., Norton, J. A., & Grotendorst, G. R. (1986) · Annals of Surgery · doi:10.1097/00000658-198602000-00006 · Cited by 176 · see citing works
Nickoloff, B. J., Mitra, R. S., Riser, B. L., Dixit, V. M., & Varani, J. (1988) · PubMed Central · Cited by 162 · see citing works
Transforming growth factor β levels in rat wound chambers
Cromack, D. T., Sporn, M. B., Roberts, A. B., Merino, M. J., Dart, L. L., & Norton, J. A. (1987) · Journal of Surgical Research · doi:10.1016/0022-4804(87)90005-9 · Cited by 159 · see citing works
Soma, Y., & Grotendorst, G. R. (1989) · Journal of Cellular Physiology · doi:10.1002/jcp.1041400209 · Cited by 152 · see citing works
Tucker, R. F., Volkenant, M. E., Branum, E. L., et al. (1983) · PubMed · Cited by 131 · see citing works
Pircher, R., Lawrence, D. A., & Jullien, P. (1984) · PubMed · Cited by 112 · see citing works
Proper, J. A., Bjornson, C. L., & Moses, H. L. (1982) · Journal of Cellular Physiology · doi:10.1002/jcp.1041100210 · Cited by 109 · see citing works
Self-citationInduction of Neovascularization by Activated Human Monocytes
Koch, A. E., Polverini, P. J., & Leibovich, S. J. (1986) · Journal of Leukocyte Biology · doi:10.1002/jlb.39.2.233 · Cited by 104 · see citing works
Shipley, G. D., Childs, C. B., Volkenant, M. E., et al. (1984) · PubMed · Cited by 95 · see citing works
What is the role of endothelial cells in angiogenesis?
Folkman, J. (1984) · PubMed · Cited by 81 · see citing works
Beauchamp, R. D., Lyons, R. M., Yang, E. Y., et al. (1990) · Pancreas · doi:10.1097/00006676-199007000-00001 · Cited by 74 · see citing works
Self-citationPlouët, J., & Gospodarowicz, D. (1989) · Journal of Cellular Physiology · doi:10.1002/jcp.1041410221 · Cited by 73 · see citing works
An evaluation of methods to quantitate the chick chorioallantoic membrane assay in angiogenesis.
Mt, V., Cf, S., Burger, P. C., et al. (1985) · PubMed · Cited by 59 · see citing works
Leukocytes and experimental corneal vascularization.
Eliason, J. A. (1978) · PubMed · Cited by 48 · see citing works
Sorrentino, V., & Bandyopadhyay, S. (1989) · PubMed · Cited by 41 · see citing works
Production of growth factors (PDGF & TGF-beta) at the site of tissue repair.
Gr, G., Ca, G., & Gilman, T. (1988) · PubMed · Cited by 35 · see citing works
Bergh, J. C. S. (1988) · PubMed · Cited by 34 · see citing works
Gf, P., Mustoe, T., & Deuel, T. (1988) · PubMed · Cited by 13 · see citing works
Sholley, M. M., & Cotran, R. S. (1978) · PubMed · Cited by 9 · see citing works
Biological effects of transforming growth factors
Moses, H. L., Keski‐Oja, J., Lyons, R. M., et al. (1989) · Springer eBooks · doi:10.1007/978-3-662-11054-6_13 · Cited by 5 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
TGF-β Signaling in Tumor Suppression and Cancer Progression
Derynck, R., Akhurst, R. J., & Balmain, A. (2001) · Nature Genetics · doi:10.1038/ng1001-117 · Cited by 2,275 · see citing works
Cyclooxygenase regulates angiogenesis induced by colon cancer cells
Tsujii, M., Kawano, S., Tsuji, S., Sawaoka, H., Hori, M., & DuBois, R. N. (1998) · Cell · doi:10.1016/s0092-8674(00)81433-6 · Cited by 2,272 · see citing works
Tonnesen, M. G., Feng, X., & Clark, R. A. F. (2000) · Journal of Investigative Dermatology Symposium Proceedings · doi:10.1046/j.1087-0024.2000.00014.x · Cited by 1,463 · see citing works
TGFβ biology in cancer progression and immunotherapy
Derynck, R., Turley, S. J., & Akhurst, R. J. (2021) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0403-1 · Cited by 944 · see citing works
Mechanisms of normal and tumor-derived angiogenesis
Papetti, M., & Herman, I. M. (2002) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00389.2001 · Cited by 809 · see citing works
Broekelmann, T. J., Limper, A. H., Colby, T. V., & McDonald, J. A. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.15.6642 · Cited by 794 · see citing works
Angiogenesis in wound repair: Angiogenic growth factors and the extracellular matrix
Li, J., Zhang, Y., & Kirsner, R. S. (2003) · Microscopy Research and Technique · doi:10.1002/jemt.10249 · Cited by 740 · see citing works
Lu, Y., Azad, N., Wang, L., Iyer, A. K. V., Castranova, V., Jiang, B.-H., & Rojanasakul, Y. (2010) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2009-0002oc · Cited by 138 · see citing works
- Authors
- Yang, E. Y., & Moses, H. L.
- Affiliations
- Vanderbilt University (US)
- ORCID
- Venue
- The Journal of cell biology
- Publisher
- Rockefeller University Press
- Published
- 1990-08-01
- Volume
- 111
- Issue
- 2
- Pages
- 731-741
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC2116177
- OpenAlex
- W2041708400
- Cited by
- 464
- References
- 58
- Citations by year
- 2025: 2 · 2024: 3 · 2023: 3 · 2022: 8 · 2021: 6 · 2020: 8 · 2019: 7 · 2018: 5 · 2017: 13 · 2016: 7 · 2015: 9 · 2014: 11 · 2013: 8 · 2012: 9
- FWCI
- 8.69
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r35ca042572-14)
- National Cancer Institute (CA42572)
- National Institute of General Medical Sciences (T32GM007347)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Hepatology › Liver physiology and pathology
- Keywords
- TGF-β1, angiogenesis, chorioallantoic membrane, cell migration, cell proliferation, basic fibroblast growth factor, endothelial cell proliferation, fibroblast accumulation, chemotaxis, capillary sprouting, perivascular inflammation, vascular remodeling, chick embryo
- MeSH terms
- Allantois, Animals, Cell Division, Cell Movement, Chick Embryo, Chorion, Extraembryonic Membranes, Fibroblast Growth Factors, Kinetics, Neovascularization, Pathologic, Recombinant Proteins, Time Factors, Transforming Growth Factors, Macromolecular Substances
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review