Aberrant mural cell recruitment to lymphatic vessels and impaired lymphatic drainage in a murine model of pulmonary fibrosis

Blood

Volumn 119, Issue 24, 2012, Pages 5931-5942

  Meinecke, Anna Katharina ^a   Nagy, Nadine ^b   D'Amico Lago, Gabriela ^c   Kirmse, Santina ^a   Klose, Ralph ^a   Schrödter, Katrin ^a   Zimmermann, Annika ^b   Helfrich, Iris ^a   Rundqvist, Helene ^d   Theegarten, Dirk ^e   Anhenn, Olaf ^e   Orian Rousseau, Véronique ^f   Johnson, Randall S ^g   Alitalo, Kari ^c   Fischer, Jens W ^b   Fandrey, Joachim ^a   Stockmann, Christian ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c UNIVERSITY OF HELSINKI   (Finland)

^d KAROLINSKA INSTITUTE   (Sweden)

^e UNIVERSITY OF DUISBURG ESSEN   (Germany)

^f KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^g SECTION OF MOLECULAR BIOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BIOLOGICAL MARKER; HYALURONIC ACID; PLATELET DERIVED GROWTH FACTOR B; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN PROX 1; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; ENDOTHELIUM CELL; FIBROBLAST; HISTOPATHOLOGY; HOMEOSTASIS; HUMAN; HUMAN TISSUE; LUNG FIBROSIS; LUNG PARENCHYMA; LYMPH VESSEL; LYMPHATIC DRAINAGE; MOUSE; MURAL CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY FAILURE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

EID: 84862491030     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-12-396895     Document Type: Article

References (43)

1. Olson AL, Swigris JJ, Lezotte DC, Norris JM, Wilson CG, Brown KK. Mortality from pulmonary fibrosis increased in the United States from 1992 to 2003. Am J Respir Crit Care Med. 2007;176(3):277-284. (Pubitemid 47195878)
2. Selman M, Pardo A. Role of epithelial cells in idiopathic pulmonary fibrosis: from innocent targets to serial killers. Proc Am Thorac Soc. 2006;3(4):364-372. (Pubitemid 43845414)
3. El-Chemaly S, Malide D, Zudaire E, et al. Abnormal lymphangiogenesis in idiopathic pulmonary fibrosis with insights into cellular and molecular mechanisms. Proc Natl Acad Sci U S A. 2009;106(10):3958-3963.
4. Ebina M, Shibata N, Ohta H, et al. The disappearance of subpleural and interlobular lymphatics in idiopathic pulmonary fibrosis. Lymphat Res Biol. 2010;8(4):199-207.
5. Petrova TV, Karpanen T, Norrmen C, et al. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat Med. 2004;10(9):974-981. (Pubitemid 39273739)
6. Aukland K, Reed RK. Interstitial-lymphatic mechanisms in the control of extracellular fluid volume. Physiol Rev. 1993;73(1):1-78. (Pubitemid 23065433)
7. Reed RK, Laurent TC, Taylor AE. Hyaluronan in prenodal lymph from skin: changes with lymph flow. Am J Physiol. 1990;259(4 Pt 2):H1097-H1100. (Pubitemid 20352308)
8. Schirger A, Harrison EG Jr, Janes JM. Idiopathic lymphedema. Review of 131 cases. JAMA. 1962;182:14-22.
9. Rockson SG. Lymphedema. Am J Med. 2001;110(4):288-295. (Pubitemid 32187290)
10. Wagner EM, Blosser S, Mitzner W. Bronchial vascular contribution to lung lymph flow. J Appl Physiol. 1998;85(6):2190-2195. (Pubitemid 28558075)
11. Traber DL, Lentz CW, Traber LD, Herndon DN. Lymph and blood flow responses in central airways. Am Rev Respir Dis. 1992;146(5 Pt 2):S15-S18.
12. Lauweryns JM, Baert JH. Alveolar clearance and the role of the pulmonary lymphatics. Am Rev Respir Dis. 1977;115(4):625-683. (Pubitemid 8074576)
13. Stockmann C, Kerdiles Y, Nomaksteinsky M, et al. Loss of myeloid cell-derived vascular endothelial growth factor accelerates fibrosis. Proc Natl Acad Sci U S A. 2010;107(9):4329-4334.
14. Oliver G, Alitalo K. The lymphatic vasculature: recent progress and paradigms. Annu Rev Cell Dev Biol. 2005;21:457-483. (Pubitemid 41740643)
15. Gordon EJ, Gale NW, Harvey NL. Expression of the hyaluronan receptor LYVE-1 is not restricted to the lymphatic vasculature; LYVE-1 is also expressed on embryonic blood vessels. Dev Dyn. 2008;237(7):1901-1909. (Pubitemid 351962466)
16. Foo SS, Turner CJ, Adams S, et al. Ephrin-B2 controls cell motility and adhesion during blood-vessel- wall assembly. Cell. 2006;124(1):161-173. (Pubitemid 43069317)
17. Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C. Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development. 1999;126(14):3047-3055. (Pubitemid 29378170)
18. Shimoda H, Bernas MJ, Witte MH, Gale NW, Yancopoulos GD, Kato S. Abnormal recruitment of periendothelial cells to lymphatic capillaries in digestive organs of angiopoietin-2-deficient mice. Cell Tissue Res. 2007;328(2):329-337. (Pubitemid 46452201)
19. Lindahl P, Johansson BR, Leveen P, Betsholtz C. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science. 1997;277(5323):242- 245. (Pubitemid 27446080)
20. Kovalenko M, Ronnstrand L, Heldin CH, et al. Phosphorylation site-specific inhibition of plateletderived growth factor beta-receptor autophosphorylation by the receptor blocking tyrphostin AG1296. Biochemistry. 1997;36(21):6260-6269. (Pubitemid 27231382)
21. Dumont DJ, Jussila L, Taipale J, et al. Cardiovascular failure in mouse embryos deficient in VEGF receptor-3. Science. 1998;282(5390):946-949. (Pubitemid 28507528)
22. Tager AM, LaCamera P, Shea BS, et al. The lysophosphatidic acid receptor LPA1 links pulmonary fibrosis to lung injury by mediating fibroblast recruitment and vascular leak. Nat Med. 2008;14(1):45-54.
23. Webber J, Jenkins RH, Meran S, Phillips A, Steadman R. Modulation of TGFbeta1-dependent myofibroblast differentiation by hyaluronan. Am J Pathol. 2009;175(1):148-160.
24. Webber J, Meran S, Steadman R, Phillips A. Hyaluronan orchestrates transforming growth factor-beta1- dependent maintenance of myofibroblast phenotype. J Biol Chem. 2009;284(14):9083-9092.
25. Meran S, Thomas D, Stephens P, et al. Involvement of hyaluronan in regulation of fibroblast phenotype. J Biol Chem. 2007;282(35):25687-25697. (Pubitemid 47372811)
26. Meran S, Thomas DW, Stephens P, et al. Hyaluronan facilitates transforming growth factor-beta1- mediated fibroblast proliferation. J Biol Chem. 2008;283(10):6530-6545.
27. Li Y, Jiang D, Liang J, et al. Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44. J Exp Med. 2011;208(7):1459-1471.
28. Gale NW, Prevo R, Espinosa J, et al. Normal lymphatic development and function in mice deficient for the lymphatic hyaluronan receptor LYVE-1. Mol Cell Biol. 2007;27(2):595-604. (Pubitemid 46080127)
29. Teder P, Vandivier RW, Jiang D, et al. Resolution of lung inflammation by CD44. Science. 2002;296(5565):155-158. (Pubitemid 34280077)
30. Ebina M, Shimizukawa M, Shibata N, et al. Heterogeneous increase in CD34-positive alveolar capillaries in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med. 2004;169(11):1203-1208. (Pubitemid 38680397)
31. Ryan TJ, De Berker D. The interstitium, the connective tissue environment of the lymphatic, and angiogenesis in human skin. Clin Dermatol. 1995;13(5):451-458. (Pubitemid 26073915)
32. Piller NB. Lymphoedema, macrophages and benzopyrones. Lymphology. 1980;13(3):109-119. (Pubitemid 10003829)
33. Piller NB. Macrophage and tissue changes in the developmental phases of secondary lymphoedema and during conservative therapy with benzopyrone. Arch Histol Cytol. 1990;53 Suppl:209-218.
34. McKee CM, Penno MB, Cowman M, et al. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest. 1996;98(10):2403-2413. (Pubitemid 26394217)
35. Lauer ME, Erzurum SC, Mukhopadhyay D, et al. Differentiated murine airway epithelial cells synthesize a leukocyte-adhesive hyaluronan matrix in response to endoplasmic reticulum stress. J Biol Chem. 2008;283(38):26283-26296.
36. Lauer ME, Fulop C, Mukhopadhyay D, Comhair S, Erzurum SC, Hascall VC. Airway smooth muscle cells synthesize hyaluronan cable structures independent of inter-alpha-inhibitor heavy chain attachment. J Biol Chem. 2009;284(8):5313- 5323.
37. Kovacs EJ, Van Stedum S, Neuman JE. Selective induction of PDGF gene expression in peritoneal macrophages by interleukin-2. Immunobiology. 1994;190(3):263-274. (Pubitemid 24145644)
38. Morisaki N, Koyama N, Kawano M, et al. Human macrophages modulate the phenotype of cultured rabbit aortic smooth muscle cells through secretion of platelet-derived growth factor. Eur J Clin Invest. 1992;22(7):461-468.
39. Lindroos PM, Coin PG, Badgett A, Morgan DL, Bonner JC. Alveolar macrophages stimulated with titanium dioxide, chrysotile asbestos, and residual oil fly ash upregulate the PDGF receptoralpha on lung fibroblasts through an IL-1betadependent mechanism. Am J Respir Cell Mol Biol. 1997;16(3):283-292. (Pubitemid 127497451)
40. Aono Y, Nishioka Y, Inayama M, et al. Imatinib as a novel antifibrotic agent in bleomycin-induced pulmonary fibrosis in mice. Am J Respir Crit Care Med. 2005;171(11):1279-1285. (Pubitemid 40740736)
41. Daniels CE, Wilkes MC, Edens M, et al. Imatinib mesylate inhibits the profibrogenic activity of TGF-beta and prevents bleomycin-mediated lung fibrosis. J Clin Invest. 2004;114(9):1308-1316. (Pubitemid 40385302)
42. Levitzki A, Mishani E. Tyrphostins and other tyrosine kinase inhibitors. Annu Rev Biochem. 2006;75:93-109. (Pubitemid 44118027)
43. Richeldi L, Costabel U, Selman M, et al. Efficacy of a tyrosine kinase inhibitor in idiopathic pulmonary fibrosis. N Engl J Med. 2011;365(12):1079- 1087.