Abstract
Human interferon-inducible protein 10 (IP-10), a member of the alpha chemokine family, inhibits bone marrow colony formation, has antitumor activity in vivo, is chemoattractant for human monocytes and T cells, and promotes T cell adhesion to endothelial cells. Here we report that IP-10 is a potent inhibitor of angiogenesis in vivo. IP-10 profoundly inhibited basic fibroblast growth factor-induced neovascularization of Matrigel (prepared by H. K. Kleinman) injected subcutaneously into athymic mice. In addition, IP-10, in a dose-dependent fashion, suppressed endothelial cell differentiation into tubular capillary structures in vitro. IP-10 had no effect on endothelial cell growth, attachment, and migration as assayed in vitro. These results document an important biological property of IP-10 and raise the possibility that IP-10 may participate in the regulation of angiogenesis during inflammation and tumorigenesis.
Full Text
The Full Text of this article is available as a PDF (1.6 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baggiolini M., Dahinden C. A. CC chemokines in allergic inflammation. Immunol Today. 1994 Mar;15(3):127–133. doi: 10.1016/0167-5699(94)90156-2. [DOI] [PubMed] [Google Scholar]
- Chopra H., Fligiel S. E., Hatfield J. S., Nelson K. K., Diglio C. A., Taylor J. D., Honn K. V. An in vivo study of the role of the tumor cell cytoskeleton in tumor cell-platelet-endothelial cell interactions. Cancer Res. 1990 Dec 1;50(23):7686–7696. [PubMed] [Google Scholar]
- Cid M. C., Grant D. S., Hoffman G. S., Auerbach R., Fauci A. S., Kleinman H. K. Identification of haptoglobin as an angiogenic factor in sera from patients with systemic vasculitis. J Clin Invest. 1993 Mar;91(3):977–985. doi: 10.1172/JCI116319. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cozzolino F., Torcia M., Aldinucci D., Ziche M., Almerigogna F., Bani D., Stern D. M. Interleukin 1 is an autocrine regulator of human endothelial cell growth. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6487–6491. doi: 10.1073/pnas.87.17.6487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ezekowitz R. A., Mulliken J. B., Folkman J. Interferon alfa-2a therapy for life-threatening hemangiomas of infancy. N Engl J Med. 1992 May 28;326(22):1456–1463. doi: 10.1056/NEJM199205283262203. [DOI] [PubMed] [Google Scholar]
- Farber J. M. HuMig: a new human member of the chemokine family of cytokines. Biochem Biophys Res Commun. 1993 Apr 15;192(1):223–230. doi: 10.1006/bbrc.1993.1403. [DOI] [PubMed] [Google Scholar]
- Folkman J., Shing Y. Angiogenesis. J Biol Chem. 1992 Jun 5;267(16):10931–10934. [PubMed] [Google Scholar]
- Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol. 1992 Apr;3(2):65–71. [PubMed] [Google Scholar]
- Friesel R., Komoriya A., Maciag T. Inhibition of endothelial cell proliferation by gamma-interferon. J Cell Biol. 1987 Mar;104(3):689–696. doi: 10.1083/jcb.104.3.689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Garlanda C., Parravicini C., Sironi M., De Rossi M., Wainstok de Calmanovici R., Carozzi F., Bussolino F., Colotta F., Mantovani A., Vecchi A. Progressive growth in immunodeficient mice and host cell recruitment by mouse endothelial cells transformed by polyoma middle-sized T antigen: implications for the pathogenesis of opportunistic vascular tumors. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7291–7295. doi: 10.1073/pnas.91.15.7291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Good D. J., Polverini P. J., Rastinejad F., Le Beau M. M., Lemons R. S., Frazier W. A., Bouck N. P. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci U S A. 1990 Sep;87(17):6624–6628. doi: 10.1073/pnas.87.17.6624. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grant D. S., Tashiro K., Segui-Real B., Yamada Y., Martin G. R., Kleinman H. K. Two different laminin domains mediate the differentiation of human endothelial cells into capillary-like structures in vitro. Cell. 1989 Sep 8;58(5):933–943. doi: 10.1016/0092-8674(89)90945-8. [DOI] [PubMed] [Google Scholar]
- Ingber D., Fujita T., Kishimoto S., Sudo K., Kanamaru T., Brem H., Folkman J. Synthetic analogues of fumagillin that inhibit angiogenesis and suppress tumour growth. Nature. 1990 Dec 6;348(6301):555–557. doi: 10.1038/348555a0. [DOI] [PubMed] [Google Scholar]
- Kleinman H. K., McGarvey M. L., Hassell J. R., Star V. L., Cannon F. B., Laurie G. W., Martin G. R. Basement membrane complexes with biological activity. Biochemistry. 1986 Jan 28;25(2):312–318. doi: 10.1021/bi00350a005. [DOI] [PubMed] [Google Scholar]
- Koch A. E., Polverini P. J., Kunkel S. L., Harlow L. A., DiPietro L. A., Elner V. M., Elner S. G., Strieter R. M. Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science. 1992 Dec 11;258(5089):1798–1801. doi: 10.1126/science.1281554. [DOI] [PubMed] [Google Scholar]
- Luster A. D., Leder P. IP-10, a -C-X-C- chemokine, elicits a potent thymus-dependent antitumor response in vivo. J Exp Med. 1993 Sep 1;178(3):1057–1065. doi: 10.1084/jem.178.3.1057. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luster A. D., Ravetch J. V. Biochemical characterization of a gamma interferon-inducible cytokine (IP-10). J Exp Med. 1987 Oct 1;166(4):1084–1097. doi: 10.1084/jem.166.4.1084. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Luster A. D., Unkeless J. C., Ravetch J. V. Gamma-interferon transcriptionally regulates an early-response gene containing homology to platelet proteins. Nature. 1985 Jun 20;315(6021):672–676. doi: 10.1038/315672a0. [DOI] [PubMed] [Google Scholar]
- Maione T. E., Gray G. S., Petro J., Hunt A. J., Donner A. L., Bauer S. I., Carson H. F., Sharpe R. J. Inhibition of angiogenesis by recombinant human platelet factor-4 and related peptides. Science. 1990 Jan 5;247(4938):77–79. doi: 10.1126/science.1688470. [DOI] [PubMed] [Google Scholar]
- Müller G., Behrens J., Nussbaumer U., Böhlen P., Birchmeier W. Inhibitory action of transforming growth factor beta on endothelial cells. Proc Natl Acad Sci U S A. 1987 Aug;84(16):5600–5604. doi: 10.1073/pnas.84.16.5600. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Passaniti A., Taylor R. M., Pili R., Guo Y., Long P. V., Haney J. A., Pauly R. R., Grant D. S., Martin G. R. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Invest. 1992 Oct;67(4):519–528. [PubMed] [Google Scholar]
- Pepper M. S., Sappino A. P., Montesano R., Orci L., Vassalli J. D. Plasminogen activator inhibitor-1 is induced in migrating endothelial cells. J Cell Physiol. 1992 Oct;153(1):129–139. doi: 10.1002/jcp.1041530117. [DOI] [PubMed] [Google Scholar]
- Sarris A. H., Broxmeyer H. E., Wirthmueller U., Karasavvas N., Cooper S., Lu L., Krueger J., Ravetch J. V. Human interferon-inducible protein 10: expression and purification of recombinant protein demonstrate inhibition of early human hematopoietic progenitors. J Exp Med. 1993 Sep 1;178(3):1127–1132. doi: 10.1084/jem.178.3.1127. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith D. R., Polverini P. J., Kunkel S. L., Orringer M. B., Whyte R. I., Burdick M. D., Wilke C. A., Strieter R. M. Inhibition of interleukin 8 attenuates angiogenesis in bronchogenic carcinoma. J Exp Med. 1994 May 1;179(5):1409–1415. doi: 10.1084/jem.179.5.1409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takigawa M., Nishida Y., Suzuki F., Kishi J., Yamashita K., Hayakawa T. Induction of angiogenesis in chick yolk-sac membrane by polyamines and its inhibition by tissue inhibitors of metalloproteinases (TIMP and TIMP-2). Biochem Biophys Res Commun. 1990 Sep 28;171(3):1264–1271. doi: 10.1016/0006-291x(90)90822-5. [DOI] [PubMed] [Google Scholar]
- Taub D. D., Lloyd A. R., Conlon K., Wang J. M., Ortaldo J. R., Harada A., Matsushima K., Kelvin D. J., Oppenheim J. J. Recombinant human interferon-inducible protein 10 is a chemoattractant for human monocytes and T lymphocytes and promotes T cell adhesion to endothelial cells. J Exp Med. 1993 Jun 1;177(6):1809–1814. doi: 10.1084/jem.177.6.1809. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Taylor S., Folkman J. Protamine is an inhibitor of angiogenesis. Nature. 1982 May 27;297(5864):307–312. doi: 10.1038/297307a0. [DOI] [PubMed] [Google Scholar]
- Tosato G., Sgadari C., Taga K., Jones K. D., Pike S. E., Rosenberg A., Sechler J. M., Magrath I. T., Love L. A., Bhatia K. Regression of experimental Burkitt's lymphoma induced by Epstein-Barr virus-immortalized human B cells. Blood. 1994 Feb 1;83(3):776–784. [PubMed] [Google Scholar]
- Vanguri P., Farber J. M. Identification of CRG-2. An interferon-inducible mRNA predicted to encode a murine monokine. J Biol Chem. 1990 Sep 5;265(25):15049–15057. [PubMed] [Google Scholar]