Increased lymphangiogenesis in joints of mice with inflammatory arthritis

Arthritis Research and Therapy

Volumn 9, Issue 6, 2007, Pages

  Zhang, Qian ^a   Lu, Yan ^a   Proulx, Steven T ^a   Guo, Ruolin ^a   Yao, Zhenqiang ^a   Schwarz, Edward M ^a   Boyce, Brendan F ^a   Xing, Lianping ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ACTIN; CD11B ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PLACENTAL GROWTH FACTOR; TUMOR NECROSIS FACTOR; VASCULOTROPIN A; VASCULOTROPIN B; VASCULOTROPIN C; VASCULOTROPIN D; PRIMER DNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CELL; BONE MARROW CELL; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SEVERITY; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOHISTOCHEMISTRY; INFLAMMATORY DISEASE; LYMPH NODE; LYMPH VESSEL; LYMPHANGIOGENESIS; MALE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; OSTEOCLAST; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; SPLEEN CELL; STEM CELL; SYNOVITIS; SYNOVIUM; TRANSGENIC MOUSE; WESTERN BLOTTING; ADULT STEM CELL; ANIMAL; ARTHRITIS; C57BL MOUSE; CBA MOUSE; DNA MICROARRAY; GENE EXPRESSION; GENETICS; INFLAMMATION; JOINT; MOUSE; NONOBESE DIABETIC MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT STEM CELLS; ANIMALS; ARTHRITIS, EXPERIMENTAL; BASE SEQUENCE; DNA PRIMERS; FEMALE; GENE EXPRESSION; INFLAMMATION; JOINTS; LYMPHANGIOGENESIS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED NOD; MICE, TRANSGENIC; NF-KAPPA B; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOCLASTS; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 37249060635     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar2326     Document Type: Article

References (56)

1. Firestein GS Evolving concepts of rheumatoid arthritis Nature 2003, 423:356-361. 10.1038/nature01661 12748655
2. Maruotti N Cantatore FP Crivellato E Vacca A Ribatti D Angiogenesis in rheumatoid arthritis Histol Histopathol 2006, 21:557-566. 16493585
3. De Bandt M Ben Mahdi MH Ollivier V Grossin M Dupuis M Gaudry M Bohlen P Lipson KE Rice A Wu Y Blockade of vascular endothelial growth factor receptor I (VEGF-RI), but not VEGF-RII, suppresses joint destruction in the K/B × N model of rheumatoid arthritis J Immunol 2003, 171:4853-4859. 14568965
4. Oliver G Detmar M The rediscovery of the lymphatic system: Old and new insights into the development and biological function of the lymphatic vasculature Genes Dev 2002, 16:773-783. 10.1101/gad.975002 11937485
5. Podgrabinska S Braun P Velasco P Kloos B Pepper MS Skobe M Molecular characterization of lymphatic endothelial cells Proc Natl Acad Sci USA 2002, 99:16069-16074. 138566 12446836 10.1073/pnas.242401399
6. Kriehuber E Breiteneder-Geleff S Groeger M Soleiman A Schoppmann SF Stingl G Kerjaschki D Maurer D Isolation and characterization of dermal lymphatic and blood endothelial cells reveal stable and functionally specialized cell lineages J Exp Med 2001, 194:797-808. 10.1084/ jem.194.6.797 11560995
7. Mäkinen T Veikkola T Mustjoki S Karpanen T Catimel B Nice EC Wise L Mercer A Kowalski H Kerjaschki D Isolated lymphatic endothelial cells transduce growth, survival and migratory signals via the VEGF-C/D receptor VEGFR-3 EMBO J 2001, 20:4762-4773. 125596 11532940 10.1093/ emboj/20.17.4762
8. Hirakawa S Hong YK Harvey N Schacht V Matsuda K Libermann T Detmar M Identification of vascular lineage-specific genes by transcriptional profiling of isolated blood vascular and lymphatic endothelial cells Am J Pathol 2003, 162:575-586. 1851142 12547715
9. Cao R Eriksson A Kubo H Alitalo K Cao Y Thyberg J Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability Circ Res 2004, 94:664-670. 10.1161/01.RES.0000118600.91698.BB 14739162
10. Brown P Lymphatic system: Unlocking the drains Nature 2005, 436:456-458. 10.1038/436456a 16049446
11. Alitalo K Tammela T Petrova TV Lymphangiogenesis in development and human disease Nature 2005, 438:946-953. 10.1038/nature04480 16355212
12. Karkkainen MJ Haiko P Sainio K Partanen J Taipale J Petrova TV Jeltsch M Jackson DG Talikka M Rauvala H Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins Nat Immunol 2004, 5:74-80. 10.1038/ni1013 14634646
13. Lee J Gray A Yuan J Luoh SM Avraham H Wood WI Vascular endothelial growth factor-related protein: A ligand and specific activator of the tyrosine kinase receptor Flt4 Proc Natl Acad Sci USA 1996, 93:1988-1992. 39896 8700872 10.1073/pnas.93.5.1988
14. Kerjaschki D Huttary N Raab I Regele H Bojarski-Nagy K Bartel G Kröber SM Greinix H Rosenmaier A Karlhofer F Lymphatic endothelial progenitor cells contribute to de novo lymphangiogenesis in human renal transplants Nat Med 2006, 12:230-234. 10.1038/nm1340 16415878
15. Maruyama K Ii M Cursiefen C Jackson DG Keino H Tomita M Van Rooijen N Takenaka H D'Amore PA Stein-Streilein J Inflammation-induced lymphangiogenesis in the cornea arises from CD11b-positive macrophages J Clin Invest 2005, 115:2363-2372. 1193872 16138190 10.1172/JCI23874
16. Hamrah P Chen L Zhang Q Dana MR Novel expression of vascular endothelial growth factor receptor (VEGFR)-3 and VEGF-C on corneal dendritic cells Am J Pathol 2003, 163:57-68. 1868166 12819011
17. Baluk P Tammela T Ator E Lyubynska N Achen MG Hicklin DJ Jeltsch M Petrova TV Pytowski B Stacker SA Pathogenesis of persistent lymphatic vessel hyperplasia in chronic airway inflammation J Clin Invest 2005, 115:247-257. 544601 15668734 10.1172/JCI200522037
18. Chilov D Kukk E Taira S Jeltsch M Kaukonen J Palotie A Joukov V Alitalo K Genomic organization of human and mouse genes for vascular endothelial growth factor C J Biol Chem 1997, 272:25176-25183. 10.1074/ jbc.272.40.25176 9312130
19. Ristimäki A Narko K Enholm B Joukov V Alitalo K Proinflammatory cytokines regulate expression of the lymphatic endothelial mitogen vascular endothelial growth factor-C J Biol Chem 1998, 273:8413-8418. 10.1074/jbc.273.14.8413 9525952
20. Li P Schwarz EM O'Keefe RJ Ma L Looney RJ Ritchlin CT Boyce BF Xing L Systemic tumor necrosis factor alpha mediates an increase in peripheral CD11bhigh osteoclast precursors in tumor necrosis factor alpha-transgenic mice Arthritis Rheum 2004, 50:265-276. 10.1002/ art.11419 14730625
21. Kim N Kadono Y Takami M Lee J Lee SH Okada F Kim JH Kobayashi T Odgren PR Nakano H Osteoclast differentiation independent of the TRANCE-RANK-TRAF6 axis J Exp Med 2005, 202:589-595. 10.1084/jem.20050978 16147974
22. Xing L Schwarz EM Boyce BF Osteoclast precursors, RANKL/RANK, and immunology Immunol Rev 2005, 208:19-29. 10.1111/j.0105-2896.2005.00336.x 16313338
23. Kouskoff V Korganow AS Duchatelle V Degott C Benoist C Mathis D Organ-specific disease provoked by systemic autoimmunity Cell 1996, 87:811-822. 10.1016/S0092-8674(00)81989-3 8945509
24. Takeshita S Kaji K Kudo A Identification and characterization of the new osteoclast progenitor with macrophage phenotypes being able to differentiate into mature osteoclasts J Bone Miner Res 2000, 15:1477-1488. 10.1359/jbmr.2000.15.8.1477 10934646
25. Zhang Q Badell IR Schwarz EM Boulukos KE Yao Z Boyce BF Xing L Tumor necrosis factor prevents alendronate-induced osteoclast apoptosis in vivo by stimulating Bcl-xL expression through Ets-2 Arthritis Rheum 2005, 52:2708-2718. 10.1002/art.21236 16142752
26. Brühl H Cihak J Schneider MA Plachý J Rupp T Wenzel I Shakarami M Milz S Ellwart JW Stangassinger M Dual role of CCR2 during initiation and progression of collagen-induced arthritis: Evidence for regulatory activity of CCR2+ T cells J Immunol 2004, 172:890-898. 14707060
27. Kamata K Kamijo S Nakajima A Koyanagi A Kurosawa H Yagita H Okumura K Involvement of TNF-like weak inducer of apoptosis in the pathogenesis of collagen-induced arthritis J Immunol 2006, 177:6433-6439. 17056575
28. Yao Z Li P Zhang Q Schwarz EM Keng P Arbini A Boyce BF Xing L Tumor necrosis factor-{alpha} increases circulating osteoclast precursor numbers by promoting their proliferation and differentiation in the bone marrow through up-regulation of c-Fms expression J Biol Chem 2006, 281:11846-11855. 10.1074/jbc.M512624200 16461346
29. Boyce BF Bone biopsy and histomorphometry in metabolic bone disease New Techniques in Metabolic Bone Disease London: Butterworths Stevenson JC 1990, 110:131.
30. Feng JQ Xing L Zhang JH Zhao M Horn D Chan J Boyce BF Harris SE Mundy GR Chen D NF-kappaB specifically activates BMP-2 gene expression in growth plate chondrocytes in vivo and in a chondrocyte cell line in vitro J Biol Chem 2003, 278:29130-29135. 10.1074/jbc.M212296200 12759356
31. Proulx TS Kwok E Beck CA Shealy D Ritchlin CT Awad HA Boyce BF Xing L Schwarz EM Longitudinal assessment of synovial, lymph node, and bone volumes in inflammatory arthritis in mice using in vivo MRI and micro-CT Arthritis Rheum 18050199
32. Ritchlin CT Haas-Smith SA Li P Hicks DG Schwarz EM Mechanisms of TNF-alpha- and RANKL-mediated osteoclastogenesis and bone resorption in psoriatic arthritis J Clin Invest 2003, 111:821-831. 153764 12639988 10.1172/JCI200316069
33. Xing L Schwarz EM Circulating osteoclast precursors: A mechanism and a marker of erosive arthritis Curr Rheumatol Rev 2005, 1:21-28. 10.2174/ 1573397052954127
34. Battegay EJ Raines EW Colbert T Ross R TNF-alpha stimulation of fibroblast proliferation. Dependence on platelet-derived growth factor (PDGF) secretion and alteration of PDGF receptor expression J Immunol 1995, 154:6040-6047. 7751646
35. Su JL Yang PC Shih JY Yang CY Wei LH Hsieh CY Chou CH Jeng YM Wang MY Chang KJ The VEGF-C/Flt-4 axis promotes invasion and metastasis of cancer cells Cancer Cell 2006, 9:209-223. 10.1016/j.ccr.2006.02.018 16530705
36. Roy H Bhardwaj S Yla-Herttuala S Biology of vascular endothelial growth factors FEBS Lett 2006, 580:2879-2887. 10.1016/j.febslet.2006.03.087 16631753
37. Yao Z Xing L Qin C Schwarz EM Boyce BF Osteoclast precursors induce their differentiation to osteoclasts by interacting with bone matrix and secreting cytokines JBMR 2006, 21(Suppl 2):S262.
38. Zhang YH Heulsmann A Tondravi MM Mukherjee A Abu-Amer Y Tumor necrosis factor-alpha (TNF) stimulates RANKL-induced osteoclastogenesis via coupling of TNF type 1 receptor and RANK signaling pathways J Biol Chem 2001, 276:563-568. 10.1074/jbc.M008198200 11032840
39. Tsai PW Shiah SG Lin MT Wu CW Kuo ML Up-regulation of vascular endothelial growth factor C in breast cancer cells by heregulin-beta 1. A critical role of p38/nuclear factor-kappa B signaling pathway J Biol Chem 2003, 278:5750-5759. 10.1074/jbc.M204863200 12471041
40. Tammela T Enholm B Alitalo K Paavonen K The biology of vascular endothelial growth factors Cardiovasc Res 2005, 65:550-563. 10.1016/ j.cardiores.2004.12.002 15664381
41. Yin G Liu W An P Li P Ding I Planelles V Schwarz EM Min W Endostatin gene transfer inhibits joint angiogenesis and pannus formation in inflammatory arthritis Mol Ther 2002, 5(5 Pt 1):547-554. 10.1006/ mthe.2002.0590 11991745
42. Olszewski WL Pazdur J Kubasiewicz E Zaleska M Cooke CJ Miller NE Lymph draining from foot joints in rheumatoid arthritis provides insight into local cytokine and chemokine production and transport to lymph nodes Arthritis Rheum 2001, 44:541-549. 10.1002/ 1529-0131(200103)44:3<541::AID-ANR102>3.0.CO;2-6 11263768
43. Huh YM Kim S Suh JS Song H Song K Shin KH The role of popliteal lymph nodes in differentiating rheumatoid arthritis from osteoarthritis by using CE 3D FSPGR MR imaging: Relationship of the inflamed synovial volume Korean J Radiol 2005, 6:117-124. 15968151
44. Goldman J Le TX Skobe M Swartz MA Overexpression of VEGF-C causes transient lymphatic hyperplasia but not increased lymphangiogenesis in regenerating skin Circ Res 2005, 96:1193-1199. 10.1161/ 01.RES.0000168918.27576.78 15890974
45. Wauke K Nagashima M Ishiwata T Asano G Yoshino S Expression and localization of vascular endothelial growth factor-C in rheumatoid arthritis synovial tissue J Rheumatol 2002, 29:34-38. 11824968
46. Cha HS Bae EK Koh JH Chai JY Jeon CH Ahn KS Kim J Koh EM Tumor necrosis factor-alpha induces vascular endothelial growth factor-C expression in rheumatoid synoviocytes J Rheumatol 2007, 34:16-19. 17216674
47. Kerjaschki D Lymphatic neoangiogenesis in renal transplants: A driving force of chronic rejection? J Nephrol 2006, 19:403-406. 17048196
48. Tammali R Ramana KV Srivastava SK Aldose reductase regulates TNF-alpha-induced PGE2 production in human colon cancer cells Cancer Lett 2007, 252:299-306. 10.1016/j.canlet.2007.01.001 17300864
49. Timoshenko AV Chakraborty C Wagner GF Lala PK COX-2-mediated stimulation of the lymphangiogenic factor VEGF-C in human breast cancer Br J Cancer 2006, 94:1154-1163. 10.1038/sj.bjc.6603067 16570043
50. Silverman MD Haas CS Rad AM Arbab AS Koch AE The role of vascular cell adhesion molecule 1/very late activation antigen 4 in endothelial progenitor cell recruitment to rheumatoid arthritis synovium Arthritis Rheum 2007, 56:1817-1826. 10.1002/art.22706 17530710
51. Bashyam H Vessel-widening by VEGF J Exp Med 2007, 204:1240. 10.1084/ jem.2046iti4
52. Braverman IM Yen A Microcirculation in psoriatic skin J Invest Dermatol 1974, 62:493-502. 10.1111/1523-1747.ep12681007 4823589
53. Ryan TJ Microcirculation in psoriasis: Blood vessels, lymphatics and tissue fluid Pharmacol Ther 1980, 10:27-64. 10.1016/0163-7258(80)90008-X 6996005
54. Kovi J Duong HD Hoang CT Ultrastructure of intestinal lymphatics in Crohn's disease Am J Clin Pathol 1981, 76:385-394. 6117198
55. Cursiefen C Cao J Chen L Liu Y Maruyama K Jackson D Kruse FE Wiegand SJ Dana MR Streilein JW Inhibition of hemangiogenesis and lymphangiogenesis after normal-risk corneal transplantation by neutralizing VEGF promotes graft survival Invest Ophthalmol Vis Sci 2004, 45:2666-2673. 10.1167/ iovs.03-1380 15277490
56. Kajiya K Detmar M An important role of lymphatic vessels in the control of UVB-induced edema formation and inflammation J Invest Dermatol 2006, 126:919-921. 10.1038/sj.jid.5700126 16470183