Endothelial cells recruit macrophages and contribute to a fibrotic milieu in bleomycin lung injury

American Journal of Respiratory Cell and Molecular Biology

Volumn 49, Issue 6, 2013, Pages 1093-1101

  Leach, Heather G ^a   Chrobak, Izabela ^a   Han, Rong ^a   Trojanowska, Maria ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Bleomycin; Endothelial cells; Idiopathic pulmonary fibrosis; Pulmonary fibrosis; Systemic sclerosis

Indexed keywords

ANAPHYLATOXIN; BLEOMYCIN; CALVASCULIN; CCL CHEMOKINE; COMPLEMENT COMPONENT C3A RECEPTOR; COMPLEMENT COMPONENT C5A RECEPTOR; COMPLEMENT RECEPTOR; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; LEUKEMIA INHIBITORY FACTOR; MACROPHAGE ELASTASE; ONCOSTATIN M; OSTEOPONTIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN; SELECTIN; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL INJURY; CELL SELECTION; CONTROLLED STUDY; DISEASE COURSE; ENDOTHELIUM CELL; ENDOTHELIUM INJURY; GENE EXPRESSION; INFLAMMATORY CELL; LUNG FIBROSIS; LUNG INJURY; MACROPHAGE; MALE; MOUSE; NONHUMAN; PATHOGENESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

ANIMALS; BLEOMYCIN; CHEMOKINES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; INFLAMMATION MEDIATORS; LUNG INJURY; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PULMONARY FIBROSIS; SCLERODERMA, SYSTEMIC; SELECTINS; UP-REGULATION;

EID: 84890043130     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2013-0152OC     Document Type: Article

References (50)

1. Varga JA, Trojanowska M. Fibrosis in systemic sclerosis. Rheum Dis Clin North Am 2008;34:115-143.
2. Pattanaik D, Brown M, Postlethwaite AE. Vascular involvement in systemic sclerosis (scleroderma). J Inflamm Res 2011;4:105-125.
3. Manetti M, Guiducci S, Ibba-Manneschi L, Matucci-Cerinic M. Mechanisms in the loss of capillaries in systemic sclerosis: angiogenesis versus vasculogenesis. J Cell Mol Med 2010;14:1241-1254.
4. Harrison JH Jr, Lazo JS. High dose continuous infusion of bleomycin in mice: a new model for drug-induced pulmonary fibrosis. J Pharmacol Exp Ther 1987;243:1185-1194.
5. Mungunsukh O, Griffin AJ, Lee YH, Day RM. Bleomycin induces the extrinsic apoptotic pathway in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 2010;298:L696-L703.
6. Adamson IY. Pulmonary toxicity of bleomycin. Environ Health Perspect 1976;16:119-126.
7. Phan SH, Gharaee-Kermani M, Wolber F, Ryan US. Stimulation of rat endothelial cell transforming growth factor-beta production by bleomycin. J Clin Invest 1991;87:148-154.
8. Yin Q, Nan HY, Zhang WH, Yan LF, Cui GB, Huang XF, Wei JG. Pulmonary microvascular endothelial cells from bleomycin-induced rats promote the transformation and collagen synthesis of fibroblasts. J Cell Physiol 2011;226:2091-2102.
9. Hashimoto N, Phan SH, Imaizumi K, Matsuo M, Nakashima H, Kawabe T, Shimokata K, Hasegawa Y. Endothelial-mesenchymal transition in bleomycin-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2010;43:161-172.
10. Fichtner F, Koslowski R, Augstein A, Hempel U, Rohlecke C, Kasper M. Bleomycin induces IL-8 and ICAM-1 expression in microvascular pulmonary endothelial cells. Exp Toxicol Pathol 2004;55:497-503.
11. Miyamoto H, Sugawara I, Azuma A, Saito Y, Kohno N, Kudoh S. Differential secretion of cytokines and adhesion molecules by HUVEC stimulated with low concentrations of bleomycin. Cell Immunol 2002;219:73-81.
12. Sato N, Suzuki Y, Nishio K, Suzuki K, Naoki K, Takeshita K, Kudo H, Miyao N, Tsumura H, Serizawa H, et al. Roles of ICAM-1 for abnormal leukocyte recruitment in the microcirculation of bleomycin-induced fibrotic lung injury. Am J Respir Crit Care Med 2000;161:1681-1688.
13. Azuma A, Takahashi S, Nose M, Araki K, Araki M, Takahashi T, Hirose M, Kawashima H, Miyasaka M, Kudoh S. Role of E-selectin in bleomycin induced lung fibrosis in mice. Thorax 2000;55:147-152.
14. Serrano-Mollar A, Closa D, Cortijo J, Morcillo EJ, Prats N, Gironella M, Panes J, Rosello-Catafau J, Bulbena O. P-selectin upregulation in bleomycin induced lung injury in rats: effect of N-acetyl-L-cysteine. Thorax 2002;57:629-634.
15. Wynn TA, Barron L. Macrophages: master regulators of inflammation and fibrosis. Semin Liver Dis 2010;30:245-257.
16. Laskin DL, Sunil VR, Gardner CR, Laskin JD. Macrophages and tissue injury: agents of defense or destruction? Annu Rev Pharmacol Toxicol 2011;51:267-288.
17. Cleret A, Quesnel-Hellmann A, Mathieu J, Vidal D, Tournier JN. Resident CD11c1 lung cells are impaired by anthrax toxins after spore infection. J Infect Dis 2006;194:86-94.
18. Rydell-Tormanen K, Andreasson K, Hesselstrand R, Risteli J, Heinegard D, Saxne T, Westergren-Thorsson G. Extracellular matrix alterations and acute inflammation: developing in parallel during early induction of pulmonary fibrosis. Lab Invest 2012;92:917-925.
19. Bandinelli F, Del Rosso A, Gabrielli A, Giacomelli R, Bartoli F, Guiducci S, Matucci Cerinic M. CCL2, CCL3 and CCL5 chemokines in systemic sclerosis: the correlation with SSc clinical features and the effect of prostaglandin E1 treatment. Clin Exp Rheumatol 2012;30 (Suppl. 71) S44-S49.
20. Ho MK, Springer TA. Tissue distribution, structural characterization, and biosynthesis of Mac-3, a macrophage surface glycoprotein exhibiting molecular weight heterogeneity. J Biol Chem 1983;258:636-642.
21. Magro CM, Waldman WJ, Knight DA, Allen JN, Nadasdy T, Frambach GE, Ross P, Marsh CB. Idiopathic pulmonary fibrosis related to endothelial injury and antiendothelial cell antibodies. Hum Immunol 2006;67:284-297.
22. Kahaleh MB, Osborn I, Le Roy EC. Increased Factor VIII/von Willebrand factor antigen and von Willebrand factor activity in scleroderma and in Raynaud's phenomenon. Ann Intern Med 1981;94:482-484.
23. Manetti M, Guiducci S, Romano E, Bellando-Randone S, Conforti ML, Ibba-Manneschi L, Matucci-Cerinic M. Increased serum levels and tissue expression of matrix metalloproteinase-12 in patients with systemic sclerosis: correlation with severity of skin and pulmonary fibrosis and vascular damage. Ann Rheum Dis 2012;71:1064-1072.
24. Dixit N, Simon SI. Chemokines, selectins and intracellular calcium flux: temporal and spatial cues for leukocyte arrest. Front Immunol 2012;3:188.
25. Codullo V, Baldwin HM, Singh MD, Fraser AR, Wilson C, Gilmour A, Hueber AJ, Bonino C, McInnes IB, Montecucco C, et al. An investigation of the inflammatory cytokine and chemokine network in systemic sclerosis. Ann Rheum Dis 2011;70:1115-1121.
26. Hasegawa M, Sato S, Takehara K. Augmented production of chemokines (monocyte chemotactic protein-1 (MCP-1), macrophage inflammatory protein-1alpha (MIP-1alpha) and MIP-1beta) in patients with systemic sclerosis: MCP-1 and MIP-1alpha may be involved in the development of pulmonary fibrosis. Clin Exp Immunol 1999;117:159-165.
27. Wynn TA. Fibrotic disease and the T (h) 1/T (h) 2 paradigm. Nat Rev Immunol 2004;4:583-594.
28. Liang J, Jung Y, Tighe RM, Xie T, Liu N, Leonard M, Gunn MD, Jiang D, Noble PW. A macrophage subpopulation recruited by CC chemokine ligand-2 clears apoptotic cells in noninfectious lung injury. Am J Physiol Lung Cell Mol Physiol 2012;302:L933-L940.
29. Laudes IJ, Chu JC, Huber-Lang M, Guo RF, Riedemann NC, Sarma JV, Mahdi F, Murphy HS, Speyer C, Lu KT, et al. Expression and function of C5a receptor in mouse microvascular endothelial cells. J Immunol 2002;169:5962-5970.
30. Karmiol S, Remick DG, Kunkel SL, Phan SH. Regulation of rat pulmonary endothelial cell interleukin-6 production by bleomycin: effects of cellular fatty acid composition. Am J Respir Cell Mol Biol 1993;9:628-636.
31. Day RM, Yang Y, Suzuki YJ, Stevens J, Pathi R, Perlmutter A, Fanburg BL, Lanzillo JJ. Bleomycin upregulates gene expression of angiotensin-converting enzyme via mitogen-activated protein kinase and early growth response 1 transcription factor. Am J Respir Cell Mol Biol 2001;25:613-619.
32. Blann AD, Illingworth K, Jayson MI. Mechanisms of endothelial cell damage in systemic sclerosis and Raynaud's phenomenon. J Rheumatol 1993;20:1325-1330.
33. Lip GY, Blann A. Von Willebrand factor: a marker of endothelial dysfunction in vascular disorders? Cardiovasc Res 1997;34:255-265.
34. Guiducci S, Giacomelli R, Cerinic MM. Vascular complications of scleroderma. Autoimmun Rev 2007;6:520-523.
35. Park SH, Saleh D, Giaid A, Michel RP. Increased endothelin-1 in bleomycin-induced pulmonary fibrosis and the effect of an endothelin receptor antagonist. Am J Respir Crit Care Med 1997;156:600-608.
36. Asano Y, Stawski L, Hant F, Highland K, Silver R, Szalai G, Watson DK, Trojanowska M. Endothelial FLI1 deficiency impairs vascular homeostasis: a role in scleroderma vasculopathy. Am J Pathol 2010;176:1983-1998.
37. Barnes TC, Anderson ME, Moots RJ. The many faces of interleukin-6: the role of IL-6 in inflammation, vasculopathy, and fibrosis in systemic sclerosis. Int J Rheumatol 2011;2011:721608.
38. Yao L, Pan J, Setiadi H, Patel KD, McEver RP. Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J Exp Med 1996;184:81-92.
39. Atamas SP, White B. Cytokine regulation of pulmonary fibrosis in scleroderma. Cytokine Growth Factor Rev 2003;14:537-550.
40. Addis-Lieser E, Kohl J, Chiaramonte MG. Opposing regulatory roles of complement factor 5 in the development of bleomycin-induced pulmonary fibrosis. J Immunol 2005;175:1894-1902.
41. Phan SH, Thrall RS. Inhibition of bleomycin-induced pulmonary fibrosis by cobra venom factor. Am J Pathol 1982;107:25-28.
42. Sprott H, Muller-Ladner U, Distler O, Gay RE, Barnum SR, Landthaler M, Scholmerich J, Lang B, Gay S. Detection of activated complement complex C5b-9 and complement receptor C5a in skin biopsies of patients with systemic sclerosis (scleroderma). J Rheumatol 2000;27:402-404.
43. Benbassat C, Schlesinger M, Luderschmidt C, Valentini G, Tirri G, Shoenfeld Y. The complement system and systemic sclerosis. Immunol Res 1993;12:312-316.
44. Nuver J, De Haas EC, Van Zweeden M, Gietema JA, Meijer C. Vascular damage in testicular cancer patients: a study on endothelial activation by bleomycin and cisplatin in vitro. Oncol Rep 2010;23:247-253.
45. Sisson TH, Simon RH. The plasminogen activation system in lung disease. Curr Drug Targets 2007;8:1016-1029.
46. Pardo A, Gibson K, Cisneros J, Richards TJ, Yang Y, Becerril C, Yousem S, Herrera I, Ruiz V, Selman M, et al. Up-regulation and profibrotic role of osteopontin in human idiopathic pulmonary fibrosis. PLoS Med 2005;2:e251.
47. Wu M, Schneider DJ, Mayes MD, Assassi S, Arnett FC, Tan FK, Blackburn MR, Agarwal SK. Osteopontin in systemic sclerosis and its role in dermal fibrosis. J Invest Dermatol 2012;132:1605-1614.
48. Berman JS, Serlin D, Li X, Whitley G, Hayes J, Rishikof DC, Ricupero DA, Liaw L, Goetschkes M, O'Regan AW. Altered bleomycin-induced lung fibrosis in osteopontin-deficient mice. Am J Physiol Lung Cell Mol Physiol 2004;286:L1311-L1318.
49. Hernnas J, Nettelbladt O, Bjermer L, Sarnstrand B, Malmstrom A, Hallgren R. Alveolar accumulation of fibronectin and hyaluronan precedes bleomycin-induced pulmonary fibrosis in the rat. Eur Respir J 1992;5:404-410.
50. Magnusson MK, Mosher DF. Fibronectin: structure, assembly, and cardiovascular implications. Arterioscler Thromb Vasc Biol 1998;18:1363-1370.