Role of the vascular and lymphatic endothelium in the pathogenesis of inflammatory bowel disease: 'Brothers in arms'

Gut

Volumn 60, Issue 7, 2011, Pages 998-1008

  Danese, Silvio ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

BETA7 INTEGRIN; CCX 282B; CD18 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CCR ANTAGONIST; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MITOGEN ACTIVATED PROTEIN KINASE; MUCOSAL ADDRESSIN CELL ADHESION MOLECULE 1; NATALIZUMAB; PF 547659; PROTEIN ANTIBODY; RANTES; RHUMAB BETA 7; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; VEDOLIZUMAB; VERY LATE ACTIVATION ANTIGEN 4;

ANGIOGENESIS; ANTIGEN EXPRESSION; CELL ACTIVITY; CELL ADHESION; CELL FUNCTION; CELL HOMING; CELL INTERACTION; CROHN DISEASE; DISEASE COURSE; DISEASE SEVERITY; DRUG TARGETING; ENTERITIS; ENZYME ACTIVITY; ENZYME INHIBITION; EXTRAVASATION; HUMAN; INNATE IMMUNITY; LEUKOCYTE MIGRATION; LYMPH VESSEL ENDOTHELIUM; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; PATHOGENESIS; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; THROMBOCYTE FUNCTION; THROMBOEMBOLISM; TISSUE SPECIFICITY; VASCULAR ENDOTHELIUM;

BLOOD COAGULATION DISORDERS; ENDOTHELIUM, LYMPHATIC; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATORY BOWEL DISEASES; MICROCIRCULATION; NEOVASCULARIZATION, PATHOLOGIC;

EID: 79958227886     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gut.2010.207480     Document Type: Review

References (120)

1. Fiocchi C. Intestinal inflammation: a complex interplay of immune and nonimmune cell interactions. Am J Physiol 1997;273:G769-75.
2. Danese S, Fiocchi C. Etiopathogenesis of inflammatory bowel diseases. World J Gastroenterol 2006;12:4807-12. (Pubitemid 44323204)
3. Fiocchi C. From immune activation to gut tissue injury: the pieces of the puzzle are coming together. Gastroenterology 1999;117:1238-41. (Pubitemid 29512685)
4. Danese S. Inflammation and the mucosal microcirculation in inflammatory bowel disease: the ebb and flow. Curr Opin Gastroenterol 2007;23:384-9. (Pubitemid 46878949)
5. Danese S, Papa A, Saibeni S, et al. Inflammation and coagulation in inflammatory bowel disease: The clot thickens. Am J Gastroenterol 2007;102:174-6.
6. Carmeliet P. Angiogenesis in health and disease. Nat Med 2003;9:653-60. (Pubitemid 36749213)
7. Rieder F, Brenmoehl J, Leeb S, et al. Wound healing and fibrosis in intestinal disease. Gut 2007;56:130-9. (Pubitemid 46044899)
8. Andoh A, Bamba S, Brittan M, et al. Role of intestinal subepithelial myofibroblasts in inflammation and regenerative response in the gut. Pharmacol Ther 2007;114:94-106. (Pubitemid 46498158)
9. Danese S. Non-immune cells in inflammatory bowel disease: from victim to villain. Trends Immunol 2008;29:555-64.
10. Danese S, Dejana E, Fiocchi C. Immune regulation by microvascular endothelial cells: directing innate and adaptive immunity, coagulation, and inflammation. J Immunol 2007;178:6017-22. (Pubitemid 46717378)
11. Granger DN, Kubes P. The microcirculation and inflammation: modulation of leukocyte-endothelial cell adhesion. J Leukoc Biol 1994;55:662-75. (Pubitemid 24171735)
12. Hatoum OA, Miura H, Binion DG. The vascular contribution in the pathogenesis of inflammatory bowel disease. Am J Physiol Heart Circ Physiol 2003;285:H1791-6.
13. Cines DB, Pollak ES, Buck CA, et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998;91:3527-761.
14. Deban L, Correale C, Vetrano S, et al. Multiple pathogenic roles of microvasculature in inflammatory bowel disease: a Jack of all trades. Am J Pathol 2008;172:1457-66. (Pubitemid 351793339)
15. Saharinen P, Tammela T, Karkkainen MJ, et al. Lymphatic vasculature: development, molecular regulation and role in tumor metastasis and inflammation. Trends Immunol 2004;25:387-95. (Pubitemid 38780956)
16. Van Kruiningen HJ, Colombel JF. The forgotten role of lymphangitis in Crohn's disease. Gut 2008;57:1-4.
17. Lawrence T, Gilroy DW. Chronic inflammation: a failure of resolution? Int J Exp Pathol 2007;88:85-94.
18. Ades EW, Candal FJ, Swerlick RA, et al. HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 1992;99:683-90. (Pubitemid 23002027)
19. Binion DG, West GA, Ina K, et al. Enhanced leukocyte binding by intestinal microvascular endothelial cells in inflammatory bowel disease. Gastroenterology 1997;112:1895-907. (Pubitemid 27240776)
20. Kvietys PR, Granger DN. Endothelial cell monolayers as a tool for studying microvascular pathophysiology. Am J Physiol 1997;273:G1189-99.
21. Aird WC, Edelberg JM, Weiler-Guettler H, et al. Vascular bed-specific expression of an endothelial cell gene is programmed by the tissue microenvironment. J Cell Biol 1997;138:1117-24. (Pubitemid 27386460)
22. Granger DN. Cell adhesion and migration. II. Leukocyte-endothelial cell adhesion in the digestive system. Am J Physiol 1997;273:G982-6.
23. Panes J, Granger DN. Leukocyte-endothelial cell interactions: molecular mechanisms and implications in gastrointestinal disease. Gastroenterology 1998;114:1066-90. (Pubitemid 28217575)
24. Danese S, Semeraro S, Marini M, et al. Adhesion molecules in inflammatory bowel disease: therapeutic implications for gut inflammation. Dig Liver Dis 2005;37:811-18. (Pubitemid 44356115)
25. Fiorino G, Correale C, Fries W, et al. Leukocyte traffic control: a novel therapeutic strategy for inflammatory bowel disease. Expert Rev Clin Immunol 2010;6:567-72.
26. Rivera-Nieves J, Gorfu G, Ley K. Leukocyte adhesion molecules in animal models of inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1715-35.
27. Stefanelli T, Malesci A, De La Rue SA, et al. Anti-adhesion molecule therapies in inflammatory bowel disease: touch and go. Autoimmun Rev 2008;7:364-9.
28. Papadakis KA, Prehn J, Moreno ST, et al. CCR9-positive lymphocytes and thymus-expressed chemokine distinguish small bowel from colonic Crohn's disease. Gastroenterology 2001;121:246-54. (Pubitemid 32729371)
29. Apostolaki M, Manoloukos M, Roulis M, et al. Role of beta7 integrin and the chemokine/chemokine receptor pair CCL25/CCR9 in modeled TNF-dependent Crohn's disease. Gastroenterology 2008;134:2025-35. (Pubitemid 351790742)
30. Rivera-Nieves J, Ho J, Bamias G, et al. Antibody blockade of CCL25/CCR9 ameliorates early but not late chronic murine ileitis. Gastroenterology 2006;131:1518-29. (Pubitemid 44708936)
31. Binion DG, West GA, Volk EE, et al. Acquired increase in leucocyte binding by intestinal microvascular endothelium in inflammatory bowel disease. Lancet 1998;352:1742-6. (Pubitemid 28534957)
32. Briskin M, Winsor-Hines D, Shyjan A, et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol 1997;151:97-110. (Pubitemid 27283962)
33. Rivera-Nieves J, Olson T, Bamias G, et al. L-selectin, alpha 4 beta 1, and alpha 4 beta 7 integrins participate in CD4+ T cell recruitment to chronically inflamed small intestine. J Immunol 2005;174:2343-52. (Pubitemid 40223984)
34. Danese S, Sans M, Scaldaferri F, et al. TNF-alpha blockade downregulates the CD40/CD40L pathway in the mucosal microcirculation: a novel anti-inflammatory mechanism of infliximab in Crohn's disease. J Immunol 2006;176:2617-24. (Pubitemid 43201714)
35. Sans M, Danese S, De La Motte C, et al. Enhanced recruitment of CX3CR1+ T cells by mucosal endothelial cellederived fractalkine in inflammatory bowel disease. Gastroenterology 2007;132:139-53. (Pubitemid 46108734)
36. Danese S, Sans M, Fiocchi C. The CD40/CD40L costimulatory pathway in inflammatory bowel disease. Gut 2004;53:1035-43. (Pubitemid 38824165)
37. Danese S, De La Motte C, Sturm A, et al. Platelets trigger a CD40-dependent inflammatory response in the microvasculature of inflammatory bowel disease patients. Gastroenterology 2003;124:1249-64. (Pubitemid 36531801)
38. Danese S, Katz J, Saibeni S, et al. Activated platelets are the source of elevated levels of soluble CD40 ligand in the circulation of inflammatory bowel disease patients. Gut 2003;10:1435-41.
39. Danese S, De La Motte C, Reyes BM, et al. Cutting edge: T cells trigger CD40-dependent platelet activation and granular RANTES release: a novel pathway for immune response amplification. J Immunol 2004;172:2011-15. (Pubitemid 38182345)
40. Vogel JD, West GA, Danese S, et al. CD40-mediated immune-nonimmune cell interactions induce mucosal fibroblast chemokines leading to T-cell transmigration. Gastroenterology 2004;126:63-80. (Pubitemid 38040725)
41. Vowinkel T, Anthoni C, Wood KC, et al. CD40-CD40 Ligand mediates the recruitment of leukocytes and platelets in the inflamed murine colon. Gastroenterology 2007;132:955-65. (Pubitemid 46440860)
42. Krieglstein CF, Cerwinka WH, Laroux FS, et al. Regulation of murine intestinal inflammation by reactive metabolites of oxygen and nitrogen: divergent roles of superoxide and nitric oxide. J Exp Med 2001;194:1207-18. (Pubitemid 33055040)
43. Binion DG, Rafiee P, Ramanujam KS, et al. Deficient iNOS in inflammatory bowel disease intestinal microvascular endothelial cells results in increased leukocyte adhesion. Free Radic Biol Med 2000;29:881-8.
44. Binion DG, Fu S, Ramanujam KS, et al. iNOS expression in human intestinal microvascular endothelial cells inhibits leukocyte adhesion. Am J Physiol 1998;275:G592-603.
45. Horowitz S, Binion DG, Nelson V, et al. Increased arginase activity and endothelial dysfunction in human inflammatory bowel disease. Am J Physiol 2007;292:G1323-36.
46. Danese S, Sgambato A, Papa A, et al. Homocysteine triggers mucosal microvascular activation in inflammatory bowel disease. Am J Gastroenterol 2005;100:886-95. (Pubitemid 40592384)
47. Scaldaferri F, Sans M, Vetrano S, et al. The role of MAPK in governing lymphocyte adhesion to and migration across the microvasculature in inflammatory bowel disease. Eur J Immunol 2009;39:290-300.
48. Scaldaferri F, Correale C, Gasbarrini A, et al. Molecular signaling blockade as a new approach to inhibit leukocyte-endothelial interactions for inflammatory bowel disease treatment. Cell Adh Migr 2009;3:296-9.
49. Hommes D, van den Blink B, Plasse T, et al. Inhibition of stress-activated MAP kinases induces clinical improvement in moderate to severe Crohn's disease. Gastroenterology 2002;122:7-14. (Pubitemid 34049188)
50. Jackson JR, Seed MP, Kircher CH, et al. The codependence of angiogenesis and chronic inflammation. FASEB J 1997;11:457-65. (Pubitemid 27259987)
51. Koutroubakis IE, Tsiolakidou G, Karmiris K, et al. Role of angiogenesis in inflammatory bowel disease. Inflamm Bowel Dis 2006;12:515-23.
52. Chidlow JH Jr, Shukla D, Grisham MB, et al. Pathogenic angiogenesis in IBD and experimental colitis: new ideas and therapeutic avenues. Am J Physiol Gastrointest Liver Physiol 2007;293:G5-18.
53. Rutella S, Vetrano S, Correale C, et al. Enhanced platelet adhesion induces angiogenesis in intestinal inflammation and inflammatory bowel disease microvasculature. J Cell Mol Med 2011;15:625-34.
54. Milkiewicz M, Brown MD, Egginton S, et al. Association between shear stress, angiogenesis, and VEGF in skeletal muscles in vivo. Microcirculation 2001;8:229-41. (Pubitemid 33598129)
55. Cane G, Moal VL, Pages G, et al. Up-regulation of intestinal vascular endothelial growth factor by Afa/Dr diffusely adhering Escherichia coli. PLoS One 2007;2:e1359.
56. Im E, Choi YJ, Kim CH, et al. The angiogenic effect of probiotic Bacillus polyfermenticus on human intestinal microvascular endothelial cells is mediated by IL-8. Am J Physiol Gastrointest Liver Physiol 2009;297:G999-1008.
57. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med 2000;6:389-95. (Pubitemid 30208155)
58. Majno G. Chronic inflammation: links with angiogenesis and wound healing. Am J Pathol 1998;153:1035-9. (Pubitemid 28465827)
59. Danese S, Sans M, De La Motte C, et al. Angiogenesis as a novel component of inflammatory bowel disease pathogenesis. Gastroenterology 2006;130:2060-73. (Pubitemid 43816964)
60. Bardin N, Reumaux D, Geboes K, et al. Increased expression of CD146, a new marker of the endothelial junction in active inflammatory bowel disease. Inflamm Bowel Dis 2006;12:16-21. (Pubitemid 43032446)
61. Saito S, Tsuno NH, Sunami E, et al. Expression of platelet-derived endothelial cell growth factor in inflammatory bowel disease. J Gastroenterol 2003;38:229-37. (Pubitemid 36527125)
62. Kanazawa S, Tsunoda T, Onuma E, et al. VEGF, basic-FGF, and TGF-beta in Crohn's disease and ulcerative colitis: a novel mechanism of chronic intestinal inflammation. Am J Gastroenterol 2001;96:227-8.
63. Bousvaros A, Zurakowski D, Fishman SJ, et al. Serum basic fibroblast growth factor in pediatric Crohn's disease. Implications for wound healing. Dig Dis Sci 1997;42:378-86. (Pubitemid 27112987)
64. Koutroubakis IE, Xidakis C, Karmiris K, et al. Potential role of soluble angiopoietin-2 and Tie-2 in patients with inflammatory bowel disease. Eur J Clin Invest 2006;36:127-32.
65. Ferrante M, Pierik M, Henckaerts L, et al. The role of vascular endothelial growth factor (VEGF) in inflammatory bowel disease. Inflamm Bowel Dis 2006;12:870-8. (Pubitemid 44352714)
66. Ganta VC, Cromer W, Mills GL, et al. Angiopoietin-2 in experimental colitis. Inflamm Bowel Dis 2010;16:1029-39.
67. Oikonomou KA, Kapsoritakis AN, Kapsoritaki AI, et al. Angiogenin, angiopoietin-1, angiopoietin-2, and endostatin serum levels in inflammatory bowel disease. Inflamm Bowel Dis 2011;17:963-70.
68. Im E, Rhee SH, Park YS, et al. Corticotropin-releasing hormone family of peptides regulates intestinal angiogenesis. Gastroenterology 2010;138:2457-67. 2467.e1-5.
69. Koon HW, Zhao D, Xu H, et al. Substance P-mediated expression of the pro-angiogenic factor CCN1 modulates the course of colitis. Am J Pathol 2008;173:400-10.
70. Danese S, Scaldaferri F, Vetrano S, et al. Critical role of the CD40-CD40 ligand pathway in governing mucosal inflammation-driven angiogenesis in inflammatory bowel disease. Gut 2007;56:1248-56. (Pubitemid 47300427)
71. Goebel S, Huang M, Davis WC, et al. VEGF-A stimulation of leukocyte adhesion to colonic microvascular endothelium: implications for inflammatory bowel disease. Am J Physiol 2006;290:G648-54.
72. Chidlow JH Jr, Langston W, Greer JJ, et al. Differential angiogenic regulation of experimental colitis. Am J Pathol 2006;169:2014-30. (Pubitemid 351181962)
73. Danese S, Sans M, Spencer DM, et al. Angiogenesis blockade as a new therapeutic approach to experimental colitis. Gut 2007;56:855-62. (Pubitemid 46854204)
74. Scaldaferri F, Vetrano S, Sans M, et al. VEGF-A links angiogenesis and inflammation in inflammatory bowel disease pathogenesis. Gastroenterology 2009;136:585-95.
75. Tolstanova G, Khomenko T, Deng X, et al. Neutralizing antivascular endothelial growth factor (VEGF) antibody reduces severity of experimental ulcerative colitis in rats: direct evidence for the pathogenic role of VEGF. J Pharmacol Exp Ther 2009;328:749-57.
76. Chidlow JH Jr, Greer JJ, Anthoni C, et al. Endothelial caveolin-1 regulates pathologic angiogenesis in a mouse model of colitis. Gastroenterology 2009;136:575-84.
77. Punekar S, Zak S, Kalter VG, et al. Thrombospondin 1 and its mimetic peptide ABT-510 decrease angiogenesis and inflammation in a murine model of inflammatory bowel disease. Pathobiology 2008;75:9-21. (Pubitemid 351365633)
78. Danese S. Negative regulators of angiogenesis in inflammatory bowel disease: thrombospondin in the spotlight. Pathobiology 2008;75:22-4. (Pubitemid 351365634)
79. Adenis A, Vanseymortier L, Foissey D, et al. Bevacizumab and postponed suture leakages after surgery for ulcerative colitis and rectal cancer. Gut 2007;56:734. (Pubitemid 46662946)
80. Loriot Y, Boudou-Rouquette P, Billemont B, et al. Acute exacerbation of hemorrhagic rectocolitis during antiangiogenic therapy with sunitinib and sorafenib. Ann Oncol 2008;19:1975.
81. Hindryckx P, Waeytens A, Laukens D, et al. Absence of placental growth factor blocks dextran sodium sulfate-induced colonic mucosal angiogenesis, increases mucosal hypoxia and aggravates acute colonic injury. Lab Invest 2010;90:566-76.
82. Esmon CT. Interactions between the innate immune and blood coagulation systems. Trends Immunol 2004;25:536-42. (Pubitemid 39208352)
83. Danese S, De La Motte C, Fiocchi C. Platelets in Inflammatory bowel disease: clinical, pathological and therapeutical implications. Am J Gastroenterol 2004;99:938-45. (Pubitemid 39090227)
84. Sankey EA, Dhillon AP, Anthony A, et al. Early mucosal changes in Crohn's disease. Gut 1993;34:375-81. (Pubitemid 23080265)
85. Thompson NP, Wakefield AJ, Pounder RE. Inherited disorders of coagulation appear to protect against inflammatory bowel disease. Gastroenterology 1995;108:1011-15.
86. Dhillon AP, Anthony A, Sim R, et al. Mucosal capillary thrombi in rectal biopsies. Histopathology 1992;21:127-33.
87. Mori M, Salter JW, Vowinkel T, et al. Molecular determinants of the prothrombogenic phenotype assumed by inflamed colonic venules. Am J Physiol 2005;288:G920-6.
88. Vowinkel T, Wood KC, Stokes KY, et al. Mechanisms of platelet and leukocyte recruitment in experimental colitis. Am J Physiol 2007;293:G1054-60.
89. Strukova S. Blood coagulation-dependent inflammation. Coagulation-dependent inflammation and inflammation-dependent thrombosis. Front Biosci 2006;11:59-80.
90. Danese S, Vetrano S, Zhang L, et al. The protein C pathway in tissue inflammation and injury: pathogenic role and therapeutic implications. Blood 2010;115:1121-30.
91. Lust M, Vulcano M, Danese S. The protein C pathway in inflammatory bowel disease: the missing link between inflammation and coagulation. Trends Mol Med 2008;14:237-44.
92. Scaldaferri F, Sans M, Vetrano S, et al. Crucial role of the protein C pathway in governing microvascular inflammation in inflammatory bowel disease. J Clin Invest 2007;117:1951-60. (Pubitemid 47036329)
93. Faioni EM, Ferrero S, Fontana G, et al. Expression of endothelial protein C receptor and thrombomodulin in the intestinal tissue of patients with inflammatory bowel disease. Crit Care Med 2004;32:S266-70.
94. Yoshida H, Russell J, Stokes KY, et al. Role of the protein C pathway in the extraintestinal thrombosis associated with murine colitis. Gastroenterology 2008;135:882-8.
95. Anthoni C, Russell J, Wood KC, et al. Tissue factor: a mediator of inflammatory cell recruitment, tissue injury, and thrombus formation in experimental colitis. J Exp Med 2007;204:1595-601. (Pubitemid 47048026)
96. Iwasaki A, Medzhitov R. Toll-like receptor control of the adaptive immune responses. Nat Immunol 2004;5:987-95. (Pubitemid 41057715)
97. Andonegui G, Bonder CS, Green F, et al. Endothelium-derived Toll-like receptor-4 is the key molecule in LPS-induced neutrophil sequestration into lungs. J Clin Invest 2003;111:1011-20. (Pubitemid 36397477)
98. Ogawa H, Rafiee P, Heidemann J, et al. Mechanisms of endotoxin tolerance in human intestinal microvascular endothelial cells. J Immunol 2003;170:5956-64. (Pubitemid 36682575)
99. Faure E, Thomas L, Xu H, et al. Bacterial lipopolysaccharide and IFN-gamma induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kappa B activation. J Immunol 2001;166:2018-24. (Pubitemid 32114690)
100. Maaser C, Heidemann J, von Eiff C, et al. Human intestinal microvascular endothelial cells express Toll-like receptor 5: a binding partner for bacterial flagellin. J Immunol 2004;172:5056-62. (Pubitemid 38456433)
101. Heidemann J, Ruther C, Kebschull M, et al. Expression of IL-12-related molecules in human intestinal microvascular endothelial cells is regulated by TLR3. Am J Physiol Gastrointest Liver Physiol 2007;293:G1315-24.
102. Inohara N, Nunez G. NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 2003;3:371-82. (Pubitemid 37323197)
103. Scaldaferri F, Phillips M, Rhee M, et al. Tolerization of intestinal mesenchymal and endothelial cells to bacterial products and TNF-á: a novel mechanism to sustain and amplify gut inflammation. Gastroenterology 2009;136:T1691.
104. Heidemann J, Domschke W, Kucharzik T, et al. Intestinal microvascular endothelium and innate immunity in inflammatory bowel disease: a second line of defense? Infect Immun 2006;74:5425-32.
105. Alitalo K, Tammela T, Petrova TV. Lymphangiogenesis in development and human disease. Nature 2005;438:946-53. (Pubitemid 43093960)
106. Kataru RP, Jung K, Jang C, et al. Critical role of CD11b+ macrophages and VEGF in inflammatory lymphangiogenesis, antigen clearance, and inflammation resolution. Blood 2009;113:5650-9.
107. Angeli V, Randolph GJ. Inflammation, lymphatic function, and dendritic cell migration. Lymphat Res Biol 2006;4:217-28. (Pubitemid 46493659)
108. Aloisi F, Pujol-Borrell R. Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 2006;6:205-17. (Pubitemid 43290990)
109. Kalima TV. Experimental lymphatic obstruction in the ileum. Ann Chir Gynaecol Fenn 1970;59:187-201.
110. Kalima TV, Saloniemi H, Rahko T. Experimental regional enteritis in pigs. Scand J Gastroenterol 1976;11:353-62.
111. Vetrano S, Borroni EM, Sarukhan A, et al. The lymphatic system controls intestinal inflammation and inflammation-associated colon cancer through the chemokine decoy receptor D6. Gut 2009;59:197-206.
112. Mouta C, Heroult M. Inflammatory triggers of lymphangiogenesis. Lymphat Res Biol 2003;1:201-18.
113. Alitalo K, Carmeliet P. Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell 2002;1:219-27. (Pubitemid 41039145)
114. Fogt F, Pascha TL, Zhang PJ, et al. Proliferation of D2-40-expressing intestinal lymphatic vessels in the lamina propria in inflammatory bowel disease. Int J Mol Med 2004;13:211-14.
115. Wu TF, MacNaughton WK, von der Weid PY. Lymphatic vessel contractile activity and intestinal inflammation. Mem Inst Oswaldo Cruz 2005;100(Suppl 1):107-10. (Pubitemid 40685448)
116. Geleff S, Schoppmann SF, Oberhuber G. Increase in podoplanin-expressing intestinal lymphatic vessels in inflammatory bowel disease. Virchows Arch 2003;442:231-7. (Pubitemid 36399216)
117. Wu TF, Carati CJ, MacNaughton WK, et al. Contractile activity of lymphatic vessels is altered in the TNBS model of guinea pig ileitis. Am J Physiol Gastrointest Liver Physiol 2006;291:G566-74.
118. Correale C, Vetrano S, Tognoli F, et al. Lymphoneogenesis: a new component in inflammatory bowel disease pathogenesis. Gastroenterology 2008;134:A656.
119. Podgrabinska S, Braun P, Velasco P, et al. Molecular characterization of lymphatic endothelial cells. Proc Natl Acad Sci U S A 2002;99:16069-74. (Pubitemid 35462750)
120. Amatschek S, Kriehuber E, Bauer W, et al. Blood and lymphatic endothelial cell-specific differentiation programs are stringently controlled by the tissue environment. Blood 2007;109:4777-85. (Pubitemid 46827771)