Critical role of VEGF-C/VEGFR-3 signaling in innate and adaptive immune responses in experimental obliterative bronchiolitis

American Journal of Pathology

Volumn 181, Issue 5, 2012, Pages 1607-1620

  Krebs, Rainer ^a   Tikkanen, Jussi M ^a   Ropponen, Jussi O ^a,b   Jeltsch, Michael ^a   Jokinen, Janne J ^a,b   Ylä Herttuala, Seppo ^c   Nykänen, Antti I ^a   Lemström, Karl B ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSPORIN A; VASCULOTROPIN C; VASCULOTROPIN RECEPTOR 3;

ADAPTIVE IMMUNITY; ALLOIMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRONCHIOLITIS OBLITERANS; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DOSE RESPONSE; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; LUNG TRANSPLANTATION; LYMPHANGIOGENESIS; MALE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH17 CELL;

ADAPTIVE IMMUNITY; ANIMALS; BRONCHIOLITIS OBLITERANS; CHEMOTAXIS; CYCLOSPORINE; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; EPITHELIAL CELLS; EPITHELIUM; GRAFT REJECTION; IMMUNITY, INNATE; IMMUNOGLOBULINS; INFLAMMATION; LYMPHANGIOGENESIS; MACROPHAGES; NEUTROPHILS; RATS; SIGNAL TRANSDUCTION; TH17 CELLS; TRACHEA; TRANSPLANTATION, HOMOLOGOUS; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR C; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-3;

EID: 84868109832     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.07.021     Document Type: Article

References (46)

1. J.D. Christie, L.B. Edwards, A.Y. Kucheryavaya, P. Aurora, F. Dobbels, R. Kirk, A.O. Rahmel, J. Stehlik, M.I. Hertz The Registry of the International Society for Heart and Lung Transplantation: twenty-seventh official adult lung and heart-lung transplant report-2010 J Heart Lung Transplant 29 2010 1104 1118
2. S. Stewart, M.C. Fishbein, G.I. Snell, G.J. Berry, A. Boehler, M.M. Burke, A. Glanville, F.K. Gould, C. Magro, C.C. Marboe, K.D. McNeil, E.F. Reed, N.L. Reinsmoen, J.P. Scott, S.M. Studer, H.D. Tazelaar, J.L. Wallwork, G. Westall, M.R. Zamora, A. Zeevi, S.A. Yousem Revision of the 1996 working formulation for the standardization of nomenclature in the diagnosis of lung rejection J Heart Lung Transplant 26 2007 1229 1242 (Pubitemid 350256994)
3. T. Lawrence, D.A. Willoughby, D.W. Gilroy Anti-inflammatory lipid mediators and insights into the resolution of inflammation Nat Rev Immunol 2 2002 787 795 (Pubitemid 37328718)
4. K. Alitalo, T. Tammela, T.V. Petrova Lymphangiogenesis in development and human disease Nature 438 2005 946 953 (Pubitemid 43093960)
5. S. El-Chemaly, S.J. Levine, J. Moss Lymphatics in lung disease Ann NY Acad Sci 1131 2008 195 202 (Pubitemid 351758514)
6. M.J. Karkkainen, P. Haiko, K. Sainio, J. Partanen, J. Taipale, T.V. Petrova, M. Jeltsch, D.G. Jackson, M. Talikka, H. Rauvala, C. Betsholtz, K. Alitalo Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins Nat Immunol 5 2004 74 80 (Pubitemid 38081471)
7. V. Joukov, K. Pajusola, A. Kaipainen, D. Chilov, I. Lahtinen, E. Kukk, O. Saksela, N. Kalkkinen, K. Alitalo A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases [Erratum appeared in EMBO J 1996, 15:1751] EMBO J 15 1996 290 298 (Pubitemid 26029207)
8. A. Ristimäki, K. Narko, B. Enholm, V. Joukov, K. Alitalo Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C J Biol Chem 273 1998 8413 8418 (Pubitemid 28168903)
9. C. Cursiefen, L. Chen, L.P. Borges, D. Jackson, J. Cao, C. Radziejewski, P.A. D'Amore, M.R. Dana, S.J. Wiegand, J.W. Streilein VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment J Clin Invest 113 2004 1040 1050 (Pubitemid 38544126)
10. R. Förster, A.C. Davalos-Misslitz, A. Rot CCR7 and its ligands: balancing immunity and tolerance Nat Rev Immunol 8 2008 362 371 (Pubitemid 351595218)
11. K. Hirota, H. Yoshitomi, M. Hashimoto, S. Maeda, S. Teradaira, N. Sugimoto, T. Yamaguchi, T. Nomura, H. Ito, T. Nakamura, N. Sakaguchi, S. Sakaguchi Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model J Exp Med 204 2007 2803 2812 (Pubitemid 350179551)
12. D.R. Greaves, W. Wang, D.J. Dairaghi, M.C. Dieu, B. Saint-Vis, K. Franz-Bacon, D. Rossi, C. Caux, T. McClanahan, S. Gordon, A. Zlotnik, T.J. Schall CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3alpha and is highly expressed in human dendritic cells J Exp Med 186 1997 837 844 (Pubitemid 27407345)
13. P. Baluk, T. Tammela, E. Ator, N. Lyubynska, M.G. Achen, D.J. Hicklin, M. Jeltsch, T.V. Petrova, B. Pytowski, S.A. Stacker, S. Ylä-Herttuala, D.G. Jackson, K. Alitalo, D.M. McDonald Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation J Clin Invest 115 2005 247 257 (Pubitemid 40385467)
14. D. Kerjaschki, H.M. Regele, I. Moosberger, K. Nagy-Bojarski, B. Watschinger, A. Soleiman, P. Birner, S. Krieger, A. Hovorka, G. Silberhumer, P. Laakkonen, T. Petrova, B. Langer, I. Raab Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates J Am Soc Nephrol 15 2004 603 612 (Pubitemid 38294790)
15. R. Huggenberger, S. Ullmann, S.T. Proulx, B. Pytowski, K. Alitalo, M. Detmar Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation J Exp Med 207 2010 2255 2269
16. P.K. Koskinen, E.A. Kallio, R. Krebs, K.B. Lemström A dose-dependent inhibitory effect of cyclosporine A on obliterative bronchiolitis of rat tracheal allografts Am J Respir Crit Care Med 155 1997 303 312 (Pubitemid 27053181)
17. J.M. Tikkanen, E.A. Kallio, C.A. Bruggeman, P.K. Koskinen, K.B. Lemström Prevention of cytomegalovirus infection-enhanced experimental obliterative bronchiolitis by antiviral prophylaxis or immunosuppression in rat tracheal allografts Am J Respir Crit Care Med 164 2001 672 679 (Pubitemid 32801676)
18. R. Krebs, J.M. Tikkanen, A.I. Nykänen, J. Wood, M. Jeltsch, S. Ylä-Herttuala, P.K. Koskinen, K.B. LemströM Dual role of vascular endothelial growth factor in experimental obliterative bronchiolitis Am J Respir Crit Care Med 171 2005 1421 1429 (Pubitemid 40800516)
19. M.O. Hiltunen, M.P. Turunen, A.M. Turunen, T.T. Rissanen, M. Laitinen, V.M. Kosma, S. Ylä-Herttuala Biodistribution of adenoviral vector to nontarget tissues after local in vivo gene transfer to arterial wall using intravascular and periadventitial gene delivery methods FASEB J 14 2000 2230 2236
20. A.M. Duijvestijn, H. van Goor, F. Klatter, G.D. Majoor, E. van Bussel, P.J. van Breda Vriesman Antibodies defining rat endothelial cells: rECA-1, a pan-endothelial cell-specific monoclonal antibody Lab Invest 66 1992 459 466
21. S. Banerji, J. Ni, S.X. Wang, S. Clasper, J. Su, R. Tammi, M. Jones, D.G. Jackson LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan J Cell Biol 144 1999 789 801 (Pubitemid 29234556)
22. M.B. King, A.C. Pedtke, H.L. Levrey-Hadden, M.I. Hertz Obliterative airway disease progresses in heterotopic airway allografts without persistent alloimmune stimulus Transplantation 74 2002 557 562 (Pubitemid 34977689)
23. B. DiGiovine, J.P. Lynch 3rd, F.J. Martinez, A. Flint, R.I. Whyte, M.D. Iannettoni, D.A. Arenberg, M.D. Burdick, M.C. Glass, C.A. Wilke, S.B. Morris, S.L. Kunkel, R.M. Strieter Bronchoalveolar lavage neutrophilia is associated with obliterative bronchiolitis after lung transplantation: role of IL-8 J Immunol 157 1996 4194 4202 (Pubitemid 126449334)
24. G.M. Verleden, B.M. Vanaudenaerde, L.J. Dupont, D.E. Van Raemdonck Azithromycin reduces airway neutrophilia and interleukin-8 in patients with bronchiolitis obliterans syndrome Am J Respir Crit Care Med 174 2006 566 570 (Pubitemid 44330550)
25. A.I. Nykänen, H. Sandelin, R. Krebs, M.A. Keränen, R. Tuuminen, T. Kärpänen, Y. Wu, B. Pytowski, P.K. Koskinen, S. Ylä-Herttuala, K. Alitalo, K.B. Lemström Targeting lymphatic vessel activation and CCL21 production by vascular endothelial growth factor receptor-3 inhibition has novel immunomodulatory and antiarteriosclerotic effects in cardiac allografts Circulation 121 2010 1413 1422
26. K.C. Meyer, D.R. Nunley, J.H. Dauber, A.T. Iacono, R.J. Keenan, R.D. Cornwell, R.B. Love Neutrophils, unopposed neutrophil elastase, and alpha1-antiprotease defenses following human lung transplantation Am J Respir Crit Care Med 164 2001 97 102 (Pubitemid 33151305)
27. J.A. De Andrade, J.P. Crow, L. Viera, C.B. Alexander, R.K. Young, D.C. McGiffin, G.L. Zorn, S. Zhu, S. Matalon, R.M. Jackson Protein nitration, metabolites of reactive nitrogen species, and inflammation in lung allografts Am J Respir Crit Care Med 161 2000 2035 2042 (Pubitemid 30418148)
28. K. Watanabe, K. Konishi, M. Fujioka, S. Kinoshita, H. Nakagawa The neutrophil chemoattractant produced by the rat kidney epithelioid cell line NRK-52E is a protein related to the KC/gro protein J Biol Chem 264 1989 19559 19563 (Pubitemid 20008058)
29. K. Hieshima, T. Imai, G. Opdenakker, J. Van Damme, J. Kusuda, H. Tei, Y. Sakaki, K. Takatsuki, R. Miura, O. Yoshie, H. Nomiyama Molecular cloning of a novel human CC chemokine liver and activation-regulated chemokine (LARC) expressed in liver Chemotactic activity for lymphocytes and gene localization on chromosome 2 J Biol Chem 272 1997 5846 5853 (Pubitemid 27102418)
30. S. Yamashiro, J.M. Wang, D. Yang, W.H. Gong, H. Kamohara, T. Yoshimura Expression of CCR6 and CD83 by cytokine-activated human neutrophils Blood 96 2000 3958 3963
31. C.Y. Kao, F. Huang, Y. Chen, P. Thai, S. Wachi, C. Kim, L. Tam, R. Wu Up-regulation of CC chemokine ligand 20 expression in human airway epithelium by IL-17 through a JAK-independent but MEK/NF-kappaB-dependent signaling pathway J Immunol 175 2005 6676 6685 (Pubitemid 41598911)
32. B.M. Vanaudenaerde, S.I. DE Vleeschauwer, R. Vos, I. Meyts, D.M. Bullens, V. Reynders, W.A. Wuyts, D.E. Van Raemdonck, L.J. Dupont, G.M. Verleden The role of the IL23/IL17 axis in bronchiolitis obliterans syndrome after lung transplantation Am J Transplant 8 2008 1911 1920
33. Y.S. Kim, S.W. Hong, J.P. Choi, T.S. Shin, H.G. Moon, E.J. Choi, S.G. Jeon, S.Y. Oh, Y.S. Gho, Z. Zhu, Y.K. Kim Vascular endothelial growth factor is a key mediator in the development of T cell priming and its polarization to type 1 and type 17 T helper cells in the airways J Immunol 183 2009 5113 5120
34. D.J. Cua, C.M. Tato Innate IL-17-producing cells: the sentinels of the immune system [Erratum appeared in Nat Rev Immunol 2010, 10:following 489, and in Nat Rev Immunol 2010, 10:611] Nat Rev Immunol 10 2010 479 489
35. S.D. Hurst, T. Muchamuel, D.M. Gorman, J.M. Gilbert, T. Clifford, S. Kwan, S. Menon, B. Seymour, C. Jackson, T.T. Kung, J.K. Brieland, S.M. Zurawski, R.W. Chapman, G. Zurawski, R.L. Coffman New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25 J Immunol 169 2002 443 453 (Pubitemid 34686166)
36. M.S. Mulligan, M.L. Jones, A.A. Vaporciyan, M.C. Howard, P.A. Ward Protective effects of IL-4 and IL-10 against immune complex-induced lung injury J Immunol 151 1993 5666 5674 (Pubitemid 23332376)
37. K. Nakagome, M. Dohi, K. Okunishi, R. Tanaka, J. Miyazaki, K. Yamamoto In vivo IL-10 gene delivery attenuates bleomycin induced pulmonary fibrosis by inhibiting the production and activation of TGF-beta in the lung Thorax 61 2006 886 894 (Pubitemid 44570310)
38. A. El-Gamel, E. Sim, P. Hasleton, J. Hutchinson, N. Yonan, J. Egan, C. Campbell, A. Rahman, S. Sheldon, A. Deiraniya, I.V. Hutchinson Transforming growth factor beta (TGF-beta) and obliterative bronchiolitis following pulmonary transplantation J Heart Lung Transplant 18 1999 828 837 (Pubitemid 29469442)
39. R.M. Aris, S. Walsh, W. Chalermskulrat, V. Hathwar, I.P. Neuringer Growth factor upregulation during obliterative bronchiolitis in the mouse model Am J Respir Crit Care Med 166 2002 417 422 (Pubitemid 34864437)
40. A.M. Ramirez, Z. Shen, J.D. Ritzenthaler, J. Roman Myofibroblast transdifferentiation in obliterative bronchiolitis: tgf-beta signaling through smad3-dependent and -independent pathways Am J Transplant 6 2006 2080 2088 (Pubitemid 44199542)
41. A.M. Ramirez, S. Takagawa, M. Sekosan, H.A. Jaffe, J. Varga, J. Roman Smad3 deficiency ameliorates experimental obliterative bronchiolitis in a heterotopic tracheal transplantation model Am J Pathol 165 2004 1223 1232 (Pubitemid 39297728)
42. L. Chen, P. Hamrah, C. Cursiefen, Q. Zhang, B. Pytowski, J.W. Streilein, M.R. Dana Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity Nat Med 10 2004 813 815 (Pubitemid 39070853)
43. D. Kerjaschki, N. Huttary, I. Raab, H. Regele, K. Bojarski-Nagy, G. Bartel, S.M. Krober, H. Greinix, A. Rosenmaier, F. Karlhofer, N. Wick, P.R. Mazal Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants Nat Med 12 2006 230 234 (Pubitemid 43214751)
44. L.A. Johnson, S. Clasper, A.P. Holt, P.F. Lalor, D. Baban, D.G. Jackson An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium J Exp Med 203 2006 2763 2777 (Pubitemid 44833351)
45. S. Podgrabinska, O. Kamalu, L. Mayer, M. Shimaoka, H. Snoeck, G.J. Randolph, M. Skobe Inflamed lymphatic endothelium suppresses dendritic cell maturation and function via Mac-1/ICAM-1-dependent mechanism J Immunol 183 2009 1767 1779
46. R.M. Kulkarni, J.M. Greenberg, A.L. Akeson NFATc1 regulates lymphatic endothelial development Mech Dev 126 2009 350 365