Interleukin 6 promotes vasculogenesis of murine brain microvessel endothelial cells

Cytokine

Volumn 12, Issue 6, 2000, Pages 655-665

  Fee, Dominic ^a   Grzybicki, Dana ^b   Dobbs, Matthew ^c   Ihyer, Sudakhar ^a   Clotfelter, Justine ^a   MacVilay, Sinarack ^a   Hart, Michael N ^a   Sandor, Matyas ^a   Fabry, Zsuzsanna ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b DUQUESNE UNIVERSITY   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Brain injury; Cytokine; Development; Growth factor; Vascularization

Indexed keywords

INTERLEUKIN 6; MATRIGEL; MESSENGER RNA; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; BRAIN; BRAIN DEVELOPMENT; BRAIN INJURY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENDOTHELIUM CELL; IN SITU HYBRIDIZATION; MICROVASCULATURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALIA; MURINAE;

EID: 0033947016     PISSN: 10434666     EISSN: None     Source Type: Journal    
DOI: 10.1006/cyto.1999.0599     Document Type: Article

References (44)

1. Risau, W, 1997, Mechanisms of angiogenesis, Nature, 386, 671, 674.
2. Mustonen T, Alitalo K. Endothelial tyrosine kinases involved in vasculogenesis and angiogenesis. J Cell Biol. 129:1995;895.
3. Davis S, Aldrich TH, Jones PF, Acheson A, Compton DL, Jain V, Ryan TE, Bruno J, Radziejewski C, Maisonpierre PC, Yancopoulos GD. Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning [see comments]. Cell. 87:1996;1161-1169.
4. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, Sato TN, Yancopoulos GD. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis [see comments]. Cell. 87:1996;1171-1180.
5. Fukushi J, Morisaki T, Shono T, Nishie A, Torisu H, Ono M, Kuwano M. Novel biological functions of interleukin-4: formation of tube-like structures by vascular endothelial cells in vitro and angiogenesis in vivo [In Process Citation]. Biochem Biophs Res Commun. 250:1998;444-448.
6. Volpert OV, Fong T, Koch AE, Peterson JD, Waltenbaugh C, Tepper RI, Bouck NP. Inhibition of angiogenesis by interleukin 4. J Exp Med. 188:1998;1039-1046.
7. Petzelbauer P, Watson CA, Pfau SE, Pober JS. IL-8 and angiogenesis: evidence that human endothelial cells lack receptors and do not respond to IL-8 in vitro. Cytokine. 7:1995;267-272.
8. Frater-Schroder M, Risau W, Hallmann R, Gautschi P, Bohlen P. Tumor necrosis factor type alpha, a potent inhibitor of endothelial cell growth in vitro, is angiogenic in vivo. Proc Natl Acad Sci USA. 84:1987;5277-5281.
9. Folkman J, Klagsburn M. Angiogenic factors. Science. 235:1987;442-447.
10. Folkman J. Angiogenesis and its inhibitors. Important Adv Oncol. 1985;42-62.
11. Folkman J. Angiogenesis and angiogenesis inhibition: an overview. EXS. 79:1997;1-8.
12. Kumar R, Yoneda J, Bucana CD, Fidler IJ. Regulation of distinct steps of angiogenesis by different angiogenic molecules. Int J Oncol. 12:1998;749-757.
13. Motro B, Itin A, Sachs L, Keshet E. Pattern of interleukin 6 gene expression in vivo suggests a role for this cytokine in angiogenesis. Proc Natl Acad Sci USA. 87:1990;3092-3096.
14. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, Mucke L. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci USA. 90:1993;10061-10065.
15. Taga T, Kishimoto T. gp130 and the interleukin-6 family of cytokines. Ann Rev Immunol. 15:1997;797.
16. Campbell IL. Structural and functional impact of the transgenic expression of cytokines in the CNS. Ann NY Acad Sci. 840:1998;83-96.
17. Vallieres L, Rivest S. Regulation of the genes encoding interleukin-6, its receptor, and gp130 in the rat brain in response to the immune activator lipopolysaccharide and the proinflammatory cytokine interleukin-1beta. J Neurochem. 69:1997;1668-1683.
18. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, Kishimoto T, Zinkernagel R, Bluethmann H, Kohler G. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature. 368:1994;339-342.
19. Bernad A, Kopf M, Kulbacki R, Weich N, Koehler G, Gutierrez-Ramos JC. Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity. 1:1994;725-731.
20. Romano M, Sironi M, Toniatti C, Polentarutti N, Fruscella P, Ghezzi P, Faggioni R, Luini W, van Hinsbergh V, Sossani S, Bussolino F, Poli V, Ciliberto G, Mantovani A. Role of IL-6 and its soluble receptor in induction of chemokines and leukocyte recruitment. Immunity. 6:1997;315-325.
21. Klein MA, Moller JC, Jones LL, Bluethmann H, Kreutzberg GW, Raivich G. Impaired neuroglial activation in interleukin-6 deficient mice. Glia. 19:1997;227-233.
22. Yoshida K, Taga T, Saito M, Suematsu S, Kumanogoh A, Tanaka T, Fujiwara H, Hirata M, Yamagami T, Nakahata T, Hirabayashi T, Yoneda Y, Tanaka K, Wang WZ, Mori C, Shiota K, Yoshida N, Kishimoto T. Targeted disruption of gp130, a common signal transducer for the interleukin 6 family of cytokines, leads to myocardial and hematological disorders. Proc Natl Acad Sci USA. 93:1996;407-411.
23. Betz UAK, Bloch W, van den Broek M, Yoshida K, Taga T, Kishimoto T, Addicks K, Rajewsky K, Muller W. Postnatally induced inactivation of gp130 in mice results in neurological, cardiac, hematopoietic, immunological, hepatic, and pulmonary defects [In Process Citation]. J Exp Med. 188:1998;1955-1965.
24. Iruela-Arispe ML, Dvorak HF. Angiogenesis: a dynamic balance of stimulators and inhibitors. Thromb Haemost. 78:1997;672-677.
25. Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem. 271:1996.
26. Loganadane LD, Berge N, Legrand C, Fauvel-Lafeve F. Endothelial cell proliferation regulated by cytokines modulates thrombospondin-1 secretion into the subendothelium. Cytokine. 9:1997;740-746.
27. Giraudo E, Arese M, Toniatti C, Strasly M, Primo L, Mantovani A, Ciliberto G, Bussolini F. IL-6 is an in vitro and in vivo autocrine growth factor for middle T antigen-transformed endothelial cells. J Immunol. 157:1996;2618-2623.
28. Takashima S, Klagsbrun M. Inhibition of endothelial cell growth by macrophage-like U-937 cell-derived oncostatin M, leukemia inhibitory factor, and transforming growth factor beta1. J Biol Chem. 271:1996;24901-24906.
29. Auerbach R. Vascular endothelial cell differentiation: organ-specificity and selective affinities as the basis for developing anti-cancer strategies. Int J Radiat Biol. 60:1991;1-10.
30. Zhao B, Schwartz JP. Involvement of cytokines in normal CNS development and neurological diseases: recent progress and perspectives. J Neurosci Res. 52:1998;7-16.
31. Mendel I, Katz A, Kozak N, Ben-Nun A, Revel M. Interleukin-6 functions in autoimmune encephalomyelitis: a study in gene-targeted mice. Eur J Immunol. 28:1998;1727-1737.
32. Okuda Y, Sakoda S, Bernard CC, Fujimura H, Saeki Y, Kishimoto T, Yanagihara T. IL-6-deficient mice are resistant to the induction of experimental autoimmune encephalomyelitis provoked by myelin oligodendrocyte glycoprotein. Int Immunol. 10:1998;703-708.
33. Eugster HP, Frei K, Kopf M, Lassmann H, Fontana A. IL-6-deficient mice resist myelin oligodendrocyte glycoprotein-induced autoimmune encephalomyelitis. Eur J Immunol. 28:1998;2178-2187.
34. DeBault KJ, Henriquez M, Hart MN, Cancilla PA. Cerebral microvessel derived cells in tissue culture. II. Establishment, identification, and preliminary characterization of an endothelial cell line. In Vitro. 17:1981;480-485.
35. DeBault KE, Cancilla PA. Some properties of isolated endothelial cells in culture. Adv Exp Med Biol. 131:1980;69-78.
36. Moore SA, Spector AA, Hart MN. Eicosanoid metabolism in cerebromicrovascular endothelium. Am J Physiol. 254:1988;C37.
37. Sahagun G, Moore SA, Fabry Z, Schelper RL, Hart MN. Purification of murine endothelial cell cultures by flow cytometry using fluorescein-labeled griffonia simplicifolia agglutinin. Am J Pathol. 134:1989;1227-1232.
38. Hart MN, VanDyk LF, Moore SA, Shasby M, Cancilla PA. Differential opening of the brain endothelial barrier following neutralization of the endothelial luminal anionic charge in vitro. J Neuropathol Exp Neurol. 46:1987;141-147.
39. DeBault LE, Cancilla PA. γ-glutamyl transpeptidase in isolated brain endothelial cells: induction by glial cells in vitro. Science. 207:1980;652-655.
40. Robinson RA, Teneyck CJ, Hart MN. Growth control in cerebral microvessel-derived endothelial cells. Brain Res. 384:1986;114-120.
41. Moore SA, Yoder E, Spector AA. Role of the blood-brain barrier in the formation of long-chain omega-3 and omega-6 fatty acids from essential fatty acid precursors. J Neurochem. 55:1990;391-402.
42. Fabry Z, Fitzsimmons KM, Herlein JA, Moninger TO, Dobbs MB, Hart MN. Production of the cytokines interleukin 1 and 6 by murine brain microvessel endothelium and smooth muscle pericytes. J Neuroimmunol. 47:1993;23-34.
43. Sambrook J, Fritsch EF, Mariatis T. Molecular Cloning. A Laboratory Manual. 1989;Cold Spring Harbor Laboratory Press, Plainview, New York.
44. Gamble JR, Matthias LJ, Meyer G, Kaur P, Russ G, Faull R, Berndt MC, Vadas MA. Regulation of in vitro capillary tube formation by anti-integrin antibodies. J Cell Biol. 121:1993;931-943.