Inflammatory lymphangiogenesis: Cellular mediators and functional implications

Angiogenesis

Volumn 17, Issue 2, 2014, Pages 373-381

  Tan, Kar Wai ^a   Chong, Shu Zhen ^a   Angeli, Véronique ^b  

^a AGENCY FOR SCIENCE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cell trafficking; Fibroblastic reticular cells; Inflammation; Lymph node; Lymphangiogenesis; Lymphocytes; Macrophages; Neutrophils

Indexed keywords

CD45 ANTIGEN; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR2; HYALURONIC ACID BINDING PROTEIN; HYALURONIC ACID RECEPTOR LYVE 1; IMMUNOGLOBULIN G; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; PODOPLANIN; SECONDARY LYMPHOID TISSUE CHEMOKINE; UNCLASSIFIED DRUG; VASCULOTROPIN A; VASCULOTROPIN D; AUTACOID;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CELL MIGRATION; CELL TRANSPORT; CELLULAR IMMUNITY; DENDRITIC CELL; DERMATITIS; DISEASE COURSE; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFLAMMATION; LYMPH FLOW; LYMPHANGIOGENESIS; LYMPHEDEMA; LYMPHOCYTE ACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; ANIMAL; BIOLOGICAL MODEL; METABOLISM; PATHOLOGY;

MAMMALIA;

ANIMALS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; LYMPHANGIOGENESIS; MODELS, BIOLOGICAL;

EID: 84898898541     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-014-9419-4     Document Type: Article

References (84)

1. Alitalo K (2011) The lymphatic vasculature in disease. Nat Med 17:1371-1380
2. Kim H, Kataru RP, Koh GY (2012) Regulation and implications of inflammatory lymphangiogenesis. Trends Immunol 33:350-356
3. Kerjaschki D, Regele HM, Moosberger I, Nagy-Bojarski K, Watschinger B, Soleiman A, Birner P, Krieger S, Hovorka A, Silberhumer G, Laakkonen P, Petrova T, Langer B, Raab I (2004) Lymphatic neoangiogenesis in human kidney transplants is associated with immunologically active lymphocytic infiltrates. J Am Soc Nephrol 15:603-612
4. Kerjaschki D, Huttary N, Raab I, Regele H, Bojarski-Nagy K, Bartel G, Krober SM, Greinix H, Rosenmaier A, Karlhofer F, Wick N, Mazal PR (2006) Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants. Nat Med 12:230-234
5. Cursiefen C, Cao J, Chen L, Liu Y, Maruyama K, Jackson D, Kruse FE, Wiegand SJ, Dana MR, Streilein JW (2004) Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival. Invest Ophthalmol Vis Sci 45:2666-2673
6. Dietrich T, Onderka J, Bock F, Kruse FE, Vossmeyer D, Stragies R, Zahn G, Cursiefen C (2007) Inhibition of inflammatory lymphangiogenesis by integrin alpha5 blockade. Am J Pathol 171:361-372
7. Chen L, Hamrah P, Cursiefen C, Zhang Q, Pytowski B, Streilein JW, Dana MR (2004) Vascular endothelial growth factor receptor-3 mediates induction of corneal alloimmunity. Nat Med 10:813-815
8. Fogt F, Pascha TL, Zhang PJ, Gausas RE, Rahemtulla A, Zimmerman RL (2004) Proliferation of D2-40-expressing intestinal lymphatic vessels in the lamina propria in inflammatory bowel disease. Int J Mol Med 13:211-214
9. Kaiserling E, Krober S, Geleff S (2003) Lymphatic vessels in the colonic mucosa in ulcerative colitis. Lymphology 36:52-61
10. Pedica F, Ligorio C, Tonelli P, Bartolini S, Baccarini P (2008) Lymphangiogenesis in Crohn's disease: an immunohistochemical study using monoclonal antibody D2-40. Virchows Arch 452:57-63
11. Geleff S, Schoppmann SF, Oberhuber G (2003) Increase in podoplanin-expressing intestinal lymphatic vessels in inflammatory bowel disease. Virchows Arch 442:231-237
12. Zhang Q, Lu Y, Proulx ST, Guo R, Yao Z, Schwarz EM, Boyce BF, Xing L (2007) Increased lymphangiogenesis in joints of mice with inflammatory arthritis. Arthr Res Ther 9:R118
13. Xu H, Edwards J, Banerji S, Prevo R, Jackson DG, Athanasou NA (2003) Distribution of lymphatic vessels in normal and arthritic human synovial tissues. Ann Rheum Dis 62:1227-1229
14. Wilkinson LS, Edwards JC (1991) Demonstration of lymphatics in human synovial tissue. Rheumatol Int 11:151-155
15. Yao LC, Baluk P, Feng J, McDonald DM (2010) Steroid-resistant lymphatic remodeling in chronically inflamed mouse airways. Am J Pathol 176:1525-1541
16. Baluk P, Tammela T, Ator E, Lyubynska N, Achen MG, Hicklin DJ, Jeltsch M, Petrova TV, Pytowski B, Stacker SA, Yla-Herttuala S, Jackson DG, Alitalo K, McDonald DM (2005) Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation. J Clin Invest 115:247-257
17. Kunstfeld R, Hirakawa S, Hong YK, Schacht V, Lange-Asschenfeldt B, Velasco P, Lin C, Fiebiger E, Wei X, Wu Y, Hicklin D, Bohlen P, Detmar M (2004) Induction of cutaneous delayed-type hypersensitivity reactions in VEGF-A transgenic mice results in chronic skin inflammation associated with persistent lymphatic hyperplasia. Blood 104:1048-1057
18. Kajiya K, Kunstfeld R, Detmar M, Chung JH (2007) Reduction of lymphatic vessels in photodamaged human skin. J Dermatol Sci 47:241-243
19. Sugaya M, Kuwano Y, Suga H, Miyagaki T, Ohmatsu H, Kadono T, Okochi H, Blauvelt A, Tamaki K, Sato S (2012) Lymphatic dysfunction impairs antigen-specific immunization, but augments tissue swelling following contact with allergens. J Invest Dermatol 132:667-676
20. Tammela T, Alitalo K (2010) Lymphangiogenesis: molecular mechanisms and future promise. Cell 140:460-476
21. Cursiefen C, Maruyama K, Bock F, Saban D, Sadrai Z, Lawler J, Dana R, Masli S (2011) Thrombospondin 1 inhibits inflammatory lymphangiogenesis by CD36 ligation on monocytes. J Exp Med 208:1083-1092
22. Kataru RP, Jung K, Jang C, Yang H, Schwendener RA, Baik JE, Han SH, Alitalo K, Koh GY (2009) Critical role of CD11b + macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 113:5650-5659
23. Maruyama K, Ii M, Cursiefen C, Jackson DG, Keino H, Tomita M, Van Rooijen N, Takenaka H, D'Amore PA, Stein-Streilein J, Losordo DW, Streilein JW (2005) Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages. J Clin Invest 115:2363-2372
24. Cursiefen C, Chen L, Borges LP, Jackson D, Cao J, Radziejewski C, D'Amore PA, Dana MR, Wiegand SJ, Streilein JW (2004) VEGF-A stimulates lymphangiogenesis and hemangiogenesis in inflammatory neovascularization via macrophage recruitment. J Clin Invest 113:1040-1050
25. Kang S, Lee SP, Kim KE, Kim HZ, Memet S, Koh GY (2009) Toll-like receptor 4 in lymphatic endothelial cells contributes to LPS-induced lymphangiogenesis by chemotactic recruitment of macrophages. Blood 113:2605-2613
26. Kim KE, Koh YJ, Jeon BH, Jang C, Han J, Kataru RP, Schwendener RA, Kim JM, Koh GY (2009) Role of CD11b+ macrophages in intraperitoneal lipopolysaccharide-induced aberrant lymphangiogenesis and lymphatic function in the diaphragm. Am J Pathol 175:1733-1745
27. Kubota Y, Takubo K, Shimizu T, Ohno H, Kishi K, Shibuya M, Saya H, Suda T (2009) M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med 206:1089-1102
28. Muniz LR, Pacer ME, Lira SA, Furtado GC (2011) A critical role for dendritic cells in the formation of lymphatic vessels within tertiary lymphoid structures. J Immunol 187:828-834
29. Hamrah P, Chen L, Zhang Q, Dana MR (2003) Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells. Am J Pathol 163:57-68
30. Kanao T, Miyachi Y (2006) Lymphangiogenesis promotes lens destruction and subsequent lens regeneration in the newt eyeball, and both processes can be accelerated by transplantation of dendritic cells. Dev Biol 290:118-124
31. Angeli V, Ginhoux F, Llodra J, Quemeneur L, Frenette PS, Skobe M, Jessberger R, Merad M, Randolph GJ (2006) B cell-driven lymphangiogenesis in inflamed lymph nodes enhances dendritic cell mobilization. Immunity 24:203-215
32. Liao S, Ruddle NH (2006) Synchrony of high endothelial venules and lymphatic vessels revealed by immunization. J Immunol 177:3369-3379
33. Shrestha B, Hashiguchi T, Ito T, Miura N, Takenouchi K, Oyama Y, Kawahara K, Tancharoen S, Ki IY, Arimura N, Yoshinaga N, Noma S, Shrestha C, Nitanda T, Kitajima S, Arimura K, Sato M, Sakamoto T, Maruyama I (2010) B cell-derived vascular endothelial growth factor A promotes lymphangiogenesis and high endothelial venule expansion in lymph nodes. J Immunol 184:4819-4826
34. Tan KW, Chong SZ, Wong FH, Evrard M, Tan SM, Keeble J, Kemeny DM, Ng LG, Abastado JP, Angeli V (2013) Neutrophils contribute to inflammatory lymphangiogenesis by increasing VEGF-A bioavailability and secreting VEGF-D. Blood 122:3666-3677
35. Furtado GC, Marinkovic T, Martin AP, Garin A, Hoch B, Hubner W, Chen BK, Genden E, Skobe M, Lira SA (2007) Lymphotoxin beta receptor signaling is required for inflammatory lymphangiogenesis in the thyroid. Proc Natl Acad Sci USA 104:5026-5031
36. Kataru RP, Kim H, Jang C, Choi DK, Koh BI, Kim M, Gollamudi S, Kim YK, Lee SH, Koh GY (2011) T lymphocytes negatively regulate lymph node lymphatic vessel formation. Immunity 34:96-107
37. Halin C, Tobler NE, Vigl B, Brown LF, Detmar M (2007) VEGF-A produced by chronically inflamed tissue induces lymphangiogenesis in draining lymph nodes. Blood 110:3158-3167
38. Wuest TR, Carr DJ (2010) VEGF-A expression by HSV-1-infected cells drives corneal lymphangiogenesis. J Exp Med 207:101-115
39. Chyou S, Ekland EH, Carpenter AC, Tzeng TC, Tian S, Michaud M, Madri JA, Lu TT (2008) Fibroblast-type reticular stromal cells regulate the lymph node vasculature. J Immunol 181:3887-3896
40. Tan KW, Yeo KP, Wong FH, Lim HY, Khoo KL, Abastado JP, Angeli V (2012) Expansion of cortical and medullary sinuses restrains lymph node hypertrophy during prolonged inflammation. J Immunol 188:4065-4080
41. Grigorova IL, Panteleev M, Cyster JG (2010) Lymph node cortical sinus organization and relationship to lymphocyte egress dynamics and antigen exposure. Proc Natl Acad Sci USA 107:20447-20452
42. Weber M, Hauschild R, Schwarz J, Moussion C, de Vries I, Legler DF, Luther SA, Bollenbach T, Sixt M (2013) Interstitial dendritic cell guidance by haptotactic chemokine gradients. Science 339:328-332
43. Pflicke H, Sixt M (2009) Preformed portals facilitate dendritic cell entry into afferent lymphatic vessels. J Exp Med 206:2925-2935
44. Lammermann T, Bader BL, Monkley SJ, Worbs T, Wedlich-Soldner R, Hirsch K, Keller M, Forster R, Critchley DR, Fassler R, Sixt M (2008) Rapid leukocyte migration by integrin-independent flowing and squeezing. Nature 453:51-55
45. Acton SE, Astarita JL, Malhotra D, Lukacs-Kornek V, Franz B, Hess PR, Jakus Z, Kuligowski M, Fletcher AL, Elpek KG, Bellemare-Pelletier A, Sceats L, Reynoso ED, Gonzalez SF, Graham DB, Chang J, Peters A, Woodruff M, Kim YA, Swat W, Morita T, Kuchroo V, Carroll MC, Kahn ML, Wucherpfennig KW, Turley SJ (2012) Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 37:276-289
46. Salmi M, Koskinen K, Henttinen T, Elima K, Jalkanen S (2004) CLEVER-1 mediates lymphocyte transmigration through vascular and lymphatic endothelium. Blood 104:3849-3857
47. Braun A, Worbs T, Moschovakis GL, Halle S, Hoffmann K, Bolter J, Munk A, Forster R (2011) Afferent lymph-derived T cells and DCs use different chemokine receptor CCR7-dependent routes for entry into the lymph node and intranodal migration. Nat Immunol 12:879-887
48. Debes GF, Arnold CN, Young AJ, Krautwald S, Lipp M, Hay JB, Butcher EC (2005) Chemokine receptor CCR7 required for T lymphocyte exit from peripheral tissues. Nat Immunol 6:889-894
49. Bromley SK, Yan S, Tomura M, Kanagawa O, Luster AD (2013) Recirculating memory T cells are a unique subset of CD4 + T cells with a distinct phenotype and migratory pattern. J Immunol 190:970-976
50. Bromley SK, Thomas SY, Luster AD (2005) Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat Immunol 6:895-901
51. Tomura M, Honda T, Tanizaki H, Otsuka A, Egawa G, Tokura Y, Waldmann H, Hori S, Cyster JG, Watanabe T, Miyachi Y, Kanagawa O, Kabashima K (2010) Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J Clin Invest 120:883-893
52. Johnson LA, Jackson DG (2010) Inflammation-induced secretion of CCL21 in lymphatic endothelium is a key regulator of integrin-mediated dendritic cell transmigration. Int Immunol 22:839
53. Tal O, Lim HY, Gurevich I, Milo I, Shipony Z, Ng LG, Angeli V, Shakhar G (2011) DC mobilization from the skin requires docking to immobilized CCL21 on lymphatic endothelium and intralymphatic crawling. J Exp Med 208:2141-2153
54. Johnson LA, Clasper S, Holt AP, Lalor PF, Baban D, Jackson DG (2006) An inflammation-induced mechanism for leukocyte transmigration across lymphatic vessel endothelium. J Exp Med 203:2763-2777
55. Vigl B, Aebischer D, Nitschke M, Iolyeva M, Rothlin T, Antsiferova O, Halin C (2011) Tissue inflammation modulates gene expression of lymphatic endothelial cells and dendritic cell migration in a stimulus-dependent manner. Blood 118:205-215
56. Lee KM, McKimmie CS, Gilchrist DS, Pallas KJ, Nibbs RJ, Garside P, McDonald V, Jenkins C, Ransohoff R, Liu L, Milling S, Cerovic V, Graham GJ (2011) D6 facilitates cellular migration and fluid flow to lymph nodes by suppressing lymphatic congestion. Blood 118:6220-6229
57. McKimmie CS, Singh MD, Hewit K, Lopez-Franco O, Le Brocq M, Rose-John S, Lee KM, Baker AH, Wheat R, Blackbourn DJ, Nibbs RJ, Graham GJ (2013) An analysis of the function and expression of D6 on lymphatic endothelial cells. Blood 121:3768-3777
58. Grigorova IL, Schwab SR, Phan TG, Pham TH, Okada T, Cyster JG (2009) Cortical sinus probing, S1P1-dependent entry and flow-based capture of egressing T cells. Nat Immunol 10:58-65
59. Pham TH, Okada T, Matloubian M, Lo CG, Cyster JG (2008) S1P1 receptor signaling overrides retention mediated by G alpha i-coupled receptors to promote T cell egress. Immunity 28:122-133
60. Schwab SR, Cyster JG (2007) Finding a way out: lymphocyte egress from lymphoid organs. Nat Immunol 8:1295-1301
61. Pham TH, Baluk P, Xu Y, Grigorova I, Bankovich AJ, Pappu R, Coughlin SR, McDonald DM, Schwab SR, Cyster JG (2010) Lymphatic endothelial cell sphingosine kinase activity is required for lymphocyte egress and lymphatic patterning. J Exp Med 207:17-27
62. Lee JW, Epardaud M, Sun J, Becker JE, Cheng AC, Yonekura AR, Heath JK, Turley SJ (2007) Peripheral antigen display by lymph node stroma promotes T cell tolerance to intestinal self. Nat Immunol 8:181-190
63. Gardner JM, Devoss JJ, Friedman RS, Wong DJ, Tan YX, Zhou X, Johannes KP, Su MA, Chang HY, Krummel MF, Anderson MS (2008) Deletional tolerance mediated by extrathymic Aire-expressing cells. Science 321:843-847
64. Nichols LA, Chen Y, Colella TA, Bennett CL, Clausen BE, Engelhard VH (2007) Deletional self-tolerance to a melanocyte/melanoma antigen derived from tyrosinase is mediated by a radio-resistant cell in peripheral and mesenteric lymph nodes. J Immunol 179:993-1003
65. Cohen JN, Guidi CJ, Tewalt EF, Qiao H, Rouhani SJ, Ruddell A, Farr AG, Tung KS, Engelhard VH (2010) Lymph node-resident lymphatic endothelial cells mediate peripheral tolerance via Aire-independent direct antigen presentation. J Exp Med 207:681-688
66. Tewalt EF, Cohen JN, Rouhani SJ, Guidi CJ, Qiao H, Fahl SP, Conaway MR, Bender TP, Tung KS, Vella AT, Adler AJ, Chen L, Engelhard VH (2012) Lymphatic endothelial cells induce tolerance via PD-L1 and lack of costimulation leading to high-level PD-1 expression on CD8 T cells. Blood 120:4772-4782
67. Fletcher AL, Lukacs-Kornek V, Reynoso ED, Pinner SE, Bellemare-Pelletier A, Curry MS, Collier AR, Boyd RL, Turley SJ (2010) Lymph node fibroblastic reticular cells directly present peripheral tissue antigen under steady-state and inflammatory conditions. J Exp Med 207:689-697
68. Lukacs-Kornek V, Malhotra D, Fletcher AL, Acton SE, Elpek KG, Tayalia P, Collier AR, Turley SJ (2011) Regulated release of nitric oxide by nonhematopoietic stroma controls expansion of the activated T cell pool in lymph nodes. Nat Immunol 12:1096-1104
69. Siegert S, Huang HY, Yang CY, Scarpellino L, Carrie L, Essex S, Nelson PJ, Heikenwalder M, Acha-Orbea H, Buckley CD, Marsland BJ, Zehn D, Luther SA (2011) Fibroblastic reticular cells from lymph nodes attenuate T cell expansion by producing nitric oxide. PLoS ONE 6:e27618
70. Khan O, Headley M, Gerard A, Wei W, Liu L, Krummel MF (2011) Regulation of T cell priming by lymphoid stroma. PLoS ONE 6:e26138
71. Podgrabinska S, Kamalu O, Mayer L, Shimaoka M, Snoeck H, Randolph GJ, Skobe M (2009) Inflamed lymphatic endothelium suppresses dendritic cell maturation and function via Mac-1/ICAM-1-dependent mechanism. J Immunol 183:1767-1779
72. Kajiya K, Hirakawa S, Detmar M (2006) Vascular endothelial growth factor-A mediates ultraviolet B-induced impairment of lymphatic vessel function. Am J Pathol 169:1496-1503
73. Shi VY, Bao L, Chan LS (2012) Inflammation-driven dermal lymphangiogenesis in atopic dermatitis is associated with CD11b + macrophage recruitment and VEGF-C up-regulation in the IL-4-transgenic mouse model. Microcirculation 19:567-579
74. Bachmann BO, Luetjen-Drecoll E, Bock F, Wiegand SJ, Hos D, Dana R, Kruse FE, Cursiefen C (2009) Transient postoperative vascular endothelial growth factor (VEGF)-neutralisation improves graft survival in corneas with partly regressed inflammatory neovascularisation. Br J Ophthalmol 93:1075-1080
75. Bachmann BO, Bock F, Wiegand SJ, Maruyama K, Dana MR, Kruse FE, Luetjen-Drecoll E, Cursiefen C (2008) Promotion of graft survival by vascular endothelial growth factor a neutralization after high-risk corneal transplantation. Arch Ophthalmol 126:71-77
76. Dietrich T, Bock F, Yuen D, Hos D, Bachmann BO, Zahn G, Wiegand S, Chen L, Cursiefen C (2010) Cutting edge: lymphatic vessels, not blood vessels, primarily mediate immune rejections after transplantation. J Immunol 184:535-539
77. Kajiya K, Sawane M, Huggenberger R, Detmar M (2009) Activation of the VEGFR-3 pathway by VEGF-C attenuates UVB-induced edema formation and skin inflammation by promoting lymphangiogenesis. J Invest Dermatol 129:1292-1298
78. Huggenberger R, Ullmann S, Proulx ST, Pytowski B, Alitalo K, Detmar M (2010) Stimulation of lymphangiogenesis via VEGFR-3 inhibits chronic skin inflammation. J Exp Med 207:2255
79. Huggenberger R, Siddiqui SS, Brander D, Ullmann S, Zimmermann K, Antsiferova M, Werner S, Alitalo K, Detmar M (2011) An important role of lymphatic vessel activation in limiting acute inflammation. Blood 117:4667-4678
80. Guo R, Zhou Q, Proulx ST, Wood R, Ji RC, Ritchlin CT, Pytowski B, Zhu Z, Wang YJ, Schwarz EM, Xing L (2009) Inhibition of lymphangiogenesis and lymphatic drainage via vascular endothelial growth factor receptor 3 blockade increases the severity of inflammation in a mouse model of chronic inflammatory arthritis. Arthr Rheum 60:2666-2676
81. Polzer K, Baeten D, Soleiman A, Distler J, Gerlag DM, Tak PP, Schett G, Zwerina J (2008) Tumour necrosis factor blockade increases lymphangiogenesis in murine and human arthritic joints. Ann Rheum Dis 67:1610-1616
82. Proulx ST, Kwok E, You Z, Beck CA, Shealy DJ, Ritchlin CT, Boyce BF, Xing L, Schwarz EM (2007) MRI and quantification of draining lymph node function in inflammatory arthritis. Ann N Y Acad Sci 1117:106-123
83. Drayton DL, Liao S, Mounzer RH, Ruddle NH (2006) Lymphoid organ development: from ontogeny to neogenesis. Nat Immunol 7:344-353
84. Aloisi F, Pujol-Borrell R (2006) Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 6:205-217