The pathogenic role of angiogenesis in rheumatoid arthritis

Angiogenesis

Volumn 18, Issue 4, 2015, Pages 433-448

  Elshabrawy, Hatem A ^a   Chen, Zhenlong ^a   Volin, Michael V ^b   Ravella, Shalini ^a   Virupannavar, Shanti ^a   Shahrara, Shiva ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b MIDWESTERN UNIVERSITY   (United States)

Author keywords

Angiogenesis; Chemokines; Cytokines; Growth factors; Matrix metalloproteinases and adhesion molecules; RA

Indexed keywords

B7 ANTIGEN; BRODALUMAB; CD11B ANTIGEN; CD14 ANTIGEN; CD209 ANTIGEN; CD64 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR7; DECTIN 1; FIBROBLAST GROWTH FACTOR 2; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYPOXIA INDUCIBLE FACTOR 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 13; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 8; IXEKIZUMAB; MILATUZUMAB; MONOCYTE CHEMOTACTIC PROTEIN 1; PLERIXAFOR; SECUKINUMAB; TREBANANIB; TUMOR NECROSIS FACTOR; UNINDEXED DRUG; VASCULOTROPIN; CYTOKINE;

ANGIOGENESIS; BONE MARROW CELL; CELL DIFFERENTIATION; ENDOTHELIUM CELL; EPITHELIUM CELL; FIBROBLAST; HUMAN; LEUKOCYTE MIGRATION; MACROPHAGE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PATHOGENESIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN TRANSPORT; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIUM; TH17 CELL; ANIMAL; CELL MOTION; METABOLISM; PATHOLOGY;

ANIMALS; ARTHRITIS, RHEUMATOID; CELL MOVEMENT; CYTOKINES; FIBROBLASTS; HUMANS; MACROPHAGES; NEOVASCULARIZATION, PATHOLOGIC; SYNOVIAL MEMBRANE;

EID: 84943354831     PISSN: 09696970     EISSN: 15737209     Source Type: Journal    
DOI: 10.1007/s10456-015-9477-2     Document Type: Review

References (189)

1. Szekanecz Z, Koch AE (2008) Vascular involvement in rheumatic diseases: ‘vascular rheumatology’. Arthritis Res Ther 10(5):224
2. Szekanecz Z, Koch AE (2007) Mechanisms of disease: angiogenesis in inflammatory diseases. Nat Clin Pract Rheumatol 3(11):635–643
3. Folkman J, Klagsbrun M (1987) Angiogenic factors. Science 235(4787):442–447
4. Lainer-Carr D, Brahn E (2007) Angiogenesis inhibition as a therapeutic approach for inflammatory synovitis. Nat Clin Pract Rheumatol 3(8):434–442
5. Koch AE (1998) Angiogenesis: implications for rheumatoid arthritis. Arthritis Rheum 41(6):951–962
6. Veale DJ, Fearon U (2006) Inhibition of angiogenic pathways in rheumatoid arthritis: potential for therapeutic targeting. Best Pract Res Clin Rheumatol 20(5):941–947
7. Szekanecz Z, Koch AE (2001) Chemokines and angiogenesis. Curr Opin Rheumatol 13(3):202–208
8. Auerbach W, Auerbach R (1994) Angiogenesis inhibition: a review. Pharmacol Ther 63(3):265–311
9. Koch AE, Distler O (2007) Vasculopathy and disordered angiogenesis in selected rheumatic diseases: rheumatoid arthritis and systemic sclerosis. Arthritis Res Ther 9(Suppl 2):S3
10. Chua RA, Arbiser JL (2009) The role of angiogenesis in the pathogenesis of psoriasis. Autoimmunity 42(7):574–579
11. Di Stefano R, Felice F, Balbarini A (2009) Angiogenesis as risk factor for plaque vulnerability. Curr Pharm Des 15(10):1095–1106
12. Kushner EJ, Bautch VL (2013) Building blood vessels in development and disease. Curr Opin Hematol 20(3):231–236
13. Szekanecz Z, Koch AE (2005) Endothelial cells in inflammation and angiogenesis. Curr Drug Targets Inflamm Allergy 4(3):319–323
14. Folkman J, Brem H (1992) Angiogenesis and inflammation. In: Gallin JI, Goldstein IM, Snyderman R (eds) Inflammation: basic principles and clinical correlates, 2nd edn. Raven Press, New York, pp 821–839
15. Folkman J (1997) Angiogenesis and angiogenesis inhibition: an overview. EXS 79:1–8
16. Folkman J, Shing Y (1992) Angiogenesis. J Biol Chem 267(16):10931–10934
17. Haringman JJ, Gerlag DM, Zwinderman AH, Smeets TJ, Kraan MC, Baeten D, McInnes IB, Bresnihan B, Tak PP (2005) Synovial tissue macrophages: a sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 64(6):834–838
18. Tak PP, Breedveld FC (1997) Analysis of serial synovial biopsies as a screening method for predicting the effects of therapeutic interventions. J Clin Rheumatol 3(4):186
19. Tak PP, Bresnihan B (2000) The pathogenesis and prevention of joint damage in rheumatoid arthritis: advances from synovial biopsy and tissue analysis. Arthritis Rheum 43(12):2619–2633
20. Mulherin D, Fitzgerald O, Bresnihan B (1996) Synovial tissue macrophage populations and articular damage in rheumatoid arthritis. Arthritis Rheum 39(1):115–124
21. Firestein GS (1996) Invasive fibroblast-like synoviocytes in rheumatoid arthritis. Passive responders or transformed aggressors? Arthritis Rheum 39(11):1781–1790
22. Gautier EL, Shay T, Miller J, Greter M, Jakubzick C, Ivanov S, Helft J, Chow A, Elpek KG, Gordonov S, Mazloom AR, Ma’ayan A, Chua WJ, Hansen TH, Turley SJ, Merad M, Randolph GJ (2012) Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat Immunol 13(11):1118–1128
23. Davies LC, Jenkins SJ, Allen JE, Taylor PR (2013) Tissue-resident macrophages. Nat Immunol 14(10):986–995
24. Tamoutounour S, Henri S, Lelouard H, de Bovis B, de Haar C, van der Woude CJ, Woltman AM, Reyal Y, Bonnet D, Sichien D, Bain CC, Mowat AM, Reis e Sousa C, Poulin LF, Malissen B, Guilliams M (2012) CD64 distinguishes macrophages from dendritic cells in the gut and reveals the Th1-inducing role of mesenteric lymph node macrophages during colitis. Eur J Immunol 42(12):3150–3166
25. Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW, Frampton J, Liu KJ, Geissmann F (2012) A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science 336(6077):86–90
26. Bain CC, Scott CL, Uronen-Hansson H, Gudjonsson S, Jansson O, Grip O, Guilliams M, Malissen B, Agace WW, Mowat AM (2013) Resident and pro-inflammatory macrophages in the colon represent alternative context-dependent fates of the same Ly6Chi monocyte precursors. Mucosal Immunol 6(3):498–510
27. Jojic V, Shay T, Sylvia K, Zuk O, Sun X, Kang J, Regev A, Koller D, Best AJ, Knell J, Goldrath A, Joic V, Cohen N, Brennan P, Brenner M, Kim F, Rao TN, Wagers A, Heng T, Ericson J, Rothamel K, Ortiz-Lopez A, Mathis D, Benoist C, Bezman NA, Sun JC, Min-Oo G, Kim CC, Lanier LL, Miller J, Brown B, Merad M, Gautier EL, Jakubzick C, Randolph GJ, Monach P, Blair DA, Dustin ML, Shinton SA, Hardy RR, Laidlaw D, Collins J, Gazit R, Rossi DJ, Malhotra N, Kreslavsky T, Fletcher A, Elpek K, Bellemarte-Pelletier A, Malhotra D, Turley S (2013) Identification of transcriptional regulators in the mouse immune system. Nat Immunol 14(6):633–643
28. Epelman S, Lavine KJ, Randolph GJ (2014) Origin and functions of tissue macrophages. Immunity 41(1):21–35
29. Jakubzick C, Gautier EL, Gibbings SL, Sojka DK, Schlitzer A, Johnson TE, Ivanov S, Duan Q, Bala S, Condon T, van Rooijen N, Grainger JR, Belkaid Y, Ma’ayan A, Riches DW, Yokoyama WM, Ginhoux F, Henson PM, Randolph GJ (2013) Minimal differentiation of classical monocytes as they survey steady-state tissues and transport antigen to lymph nodes. Immunity 39(3):599–610
30. Mills CD (1991) Molecular basis of “suppressor” macrophages. Arginine metabolism via the nitric oxide synthetase pathway. J Immunol 146(8):2719–2723
31. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M (2004) The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25(12):677–686
32. Krausgruber T, Blazek K, Smallie T, Alzabin S, Lockstone H, Sahgal N, Hussell T, Feldmann M, Udalova IA (2011) IRF5 promotes inflammatory macrophage polarization and TH1–TH17 responses. Nat Immunol 12(3):231–238
33. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A (2002) Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23(11):549–555
34. Konisti S, Kiriakidis S, Paleolog EM (2012) Hypoxia—a key regulator of angiogenesis and inflammation in rheumatoid arthritis. Nat Rev Rheumatol 8(3):153–162
35. Neumann E, Lefevre S, Zimmermann B, Gay S, Muller-Ladner U (2010) Rheumatoid arthritis progression mediated by activated synovial fibroblasts. Trends Mol Med 16(10):458–468
36. Bartok B, Firestein GS (2010) Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 233(1):233–255
37. Pap T, Meinecke I, Muller-Ladner U, Gay S (2005) Are fibroblasts involved in joint destruction? Ann Rheum Dis 64(Suppl 4):iv52–iv54
38. Huber LC, Distler O, Tarner I, Gay RE, Gay S, Pap T (2006) Synovial fibroblasts: key players in rheumatoid arthritis. Rheumatology 45(6):669–675
39. Niedermeier M, Pap T, Korb A (2010) Therapeutic opportunities in fibroblasts in inflammatory arthritis. Best Pract Res Clin Rheumatol 24(4):527–540
40. Fava RA, Olsen NJ, Spencer-Green G, Yeo KT, Yeo TK, Berse B, Jackman RW, Senger DR, Dvorak HF, Brown LF (1994) Vascular permeability factor/endothelial growth factor (VPF/VEGF): accumulation and expression in human synovial fluids and rheumatoid synovial tissue. J Exp Med 180:341–346
41. Szekanecz Z, Koch AE (2007) Macrophages and their products in rheumatoid arthritis. Curr Opin Rheumatol 19(3):289–295
42. Koch AE, Harlow LA, Haines GK, Amento EP, Unemori EN, Wong WL, Pope RM, Ferrara N (1994) Vascular endothelial growth factor. A cytokine modulating endothelial function in rheumatoid arthritis. J Immunol 152(8):4149–4156
43. Brouwer E, Gouw AS, Posthumus MD, van Leeuwen MA, Boerboom AL, Bijzet J, Bos R, Limburg PC, Kallenberg CG, Westra J (2009) Hypoxia inducible factor-1-alpha (HIF-1alpha) is related to both angiogenesis and inflammation in rheumatoid arthritis. Clin Exp Rheumatol 27(6):945–951
44. Marrelli A, Cipriani P, Liakouli V, Carubbi F, Perricone C, Perricone R, Giacomelli R (2011) Angiogenesis in rheumatoid arthritis: a disease specific process or a common response to chronic inflammation? Autoimmun Rev 10(10):595–598
45. Hu F, Mu R, Zhu J, Shi L, Li Y, Liu X, Shao W, Li G, Li M, Su Y, Cohen PL, Qiu X, Li Z (2014) Hypoxia and hypoxia-inducible factor-1alpha provoke toll-like receptor signalling-induced inflammation in rheumatoid arthritis. Ann Rheum Dis 73(5):928–936
46. Lu J, Kasama T, Kobayashi K, Yoda Y, Shiozawa F, Hanyuda M, Negishi M, Ide H, Adachi M (2000) Vascular endothelial growth factor expression and regulation of murine collagen-induced arthritis. J Immunol 164(11):5922–5927
47. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS (2003) HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112(5):645–657
48. Shahrara S, Volin MV, Connors MA, Haines GK, Koch AE (2002) Differential expression of the angiogenic Tie receptor family in arthritic and normal synovial tissue. Arthritis Res 4(3):201–208
49. Fearon U, Griosios K, Fraser A, Reece R, Emery P, Jones PF, Veale DJ (2003) Angiopoietins, growth factors, and vascular morphology in early arthritis. J Rheumatol 30(2):260–268
50. Gravallese EM, Pettit AR, Lee R, Madore R, Manning C, Tsay A, Gaspar J, Goldring MB, Goldring SR, Oettgen P (2003) Angiopoietin-1 is expressed in the synovium of patients with rheumatoid arthritis and is induced by tumour necrosis factor alpha. Ann Rheum Dis 62(2):100–107
51. Clavel G, Bessis N, Boissier MC (2003) Recent data on the role for angiogenesis in rheumatoid arthritis. Joint Bone Spine 70(5):321–326
52. Daly C, Eichten A, Castanaro C, Pasnikowski E, Adler A, Lalani AS, Papadopoulos N, Kyle AH, Minchinton AI, Yancopoulos GD, Thurston G (2013) Angiopoietin-2 functions as a Tie2 agonist in tumor models, where it limits the effects of VEGF inhibition. Cancer Res 73(1):108–118
53. Chen Y, Donnelly E, Kobayashi H, Debusk LM, Lin PC (2005) Gene therapy targeting the Tie2 function ameliorates collagen-induced arthritis and protects against bone destruction. Arthritis Rheum 52(5):1585–1594
54. Honorati MC, Neri S, Cattini L, Facchini A (2006) Interleukin-17, a regulator of angiogenic factor release by synovial fibroblasts. Osteoarthr Cartil 14(4):345–352
55. Shibuya H, Yoshitomi H, Murata K, Kobayashi S, Furu M, Ishikawa M, Fujii T, Ito H, Matsuda S (2015) TNFalpha, PDGF, and TGFbeta synergistically induce synovial lining hyperplasia via inducible PI3Kdelta. Mod Rheumatol 25(1):72–78
56. Koyama K, Hatsushika K, Ando T, Sakuma M, Wako M, Kato R, Haro H, Sugiyama H, Hamada Y, Ogawa H, Nakao A (2007) Imatinib mesylate both prevents and treats the arthritis induced by type II collagen antibody in mice. Mod Rheumatol 17(4):306–310
57. Kokkonen H, Soderstrom I, Rocklov J, Hallmans G, Lejon K, Rantapaa Dahlqvist S (2010) Up-regulation of cytokines and chemokines predates the onset of rheumatoid arthritis. Arthritis Rheum 62(2):383–391
58. Leibovich SJ, Polverini PJ, Shepard HM, Wiseman DM, Shively V, Nuseir N (1987) Macrophage-induced angiogenesis is mediated by tumour necrosis factor-alpha. Nature 329(6140):630–632
59. Strunk J, Bundke E, Lange U (2006) Anti-TNF-alpha antibody Infliximab and glucocorticoids reduce serum vascular endothelial growth factor levels in patients with rheumatoid arthritis: a pilot study. Rheumatol Int 26(3):252–256
60. Markham T, Mullan R, Golden-Mason L, Rogers S, Bresnihan B, Fitzgerald O, Fearon U, Veale DJ (2006) Resolution of endothelial activation and down-regulation of Tie2 receptor in psoriatic skin after infliximab therapy. J Am Acad Dermatol 54(6):1003–1012
61. Lubberts E (2010) Th17 cytokines and arthritis. Semin Immunopathol 32(1):43–53
62. Pickens SR, Volin MV, Mandelin AM II, Kolls JK, Pope RM, Shahrara S (2010) IL-17 contributes to angiogenesis in rheumatoid arthritis. J Immunol 184(6):3233–3241
63. Pickens SR, Chamberlain ND, Volin MV, Gonzalez M, Pope RM, Mandelin AM II, Kolls JK, Shahrara S (2011) Anti-CXCL5 therapy ameliorates IL-17-induced arthritis by decreasing joint vascularization. Angiogen 14(4):443–455
64. Chen DY, Chen YM, Chen HH, Hsieh CW, Lin CC, Lan JL (2011) Increasing levels of circulating Th17 cells and interleukin-17 in rheumatoid arthritis patients with an inadequate response to anti-TNF-alpha therapy. Arthritis Res Ther 13(4):R126
65. Shu Q, Amin MA, Ruth JH, Campbell PL, Koch AE (2012) Suppression of endothelial cell activity by inhibition of TNFalpha. Arthritis Res Ther 14(2):R88
66. Choe JY, Lee SJ, Park SH, Kim SK (2012) Tacrolimus (FK506) inhibits interleukin-1beta-induced angiopoietin-1, Tie-2 receptor, and vascular endothelial growth factor through down-regulation of JNK and p38 pathway in human rheumatoid fibroblast-like synoviocytes. Joint Bone Spine 79(2):137–143
67. Pickens SR, Chamberlain ND, Volin MV, Pope RM, Mandelin AM II, Shahrara S (2011) Characterization of CCL19 and CCL21 in rheumatoid arthritis. Arthritis Rheum 63(4):914–922
68. Isozaki T, Arbab AS, Haas CS, Amin MA, Arendt MD, Koch AE, Ruth JH (2013) Evidence that CXCL16 is a potent mediator of angiogenesis and is involved in endothelial progenitor cell chemotaxis: studies in mice with K/BxN serum-induced arthritis. Arthritis Rheum 65(7):1736–1746
69. Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y (2003) IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA 100(10):5986–5990
70. Badolato R, Oppenheim JJ (1996) Role of cytokines, acute-phase proteins, and chemokines in the progression of rheumatoid arthritis. Semin Arthritis Rheum 26(2):526–538
71. Gabay C (2006) Interleukin-6 and chronic inflammation. Arthritis Res Ther 8(Suppl 2):S3
72. Blue ML, Conrad P, Webb DL, Sarr T, Macaro M (1993) Interacting monocytes and synoviocytes induce adhesion molecules by a cytokine-regulated process. Lymphokine Cytokine Res 12(4):213–218
73. Nakahara H, Song J, Sugimoto M, Hagihara K, Kishimoto T, Yoshizaki K, Nishimoto N (2003) Anti-interleukin-6 receptor antibody therapy reduces vascular endothelial growth factor production in rheumatoid arthritis. Arthritis Rheum 48(6):1521–1529
74. Kayakabe K, Kuroiwa T, Sakurai N, Ikeuchi H, Kadiombo AT, Sakairi T, Matsumoto T, Maeshima A, Hiromura K, Nojima Y (2012) Interleukin-6 promotes destabilized angiogenesis by modulating angiopoietin expression in rheumatoid arthritis. Rheumatology 51(9):1571–1579
75. Ogami K, Yamaguchi R, Imoto S, Tamada Y, Araki H, Print C, Miyano S (2012) Computational gene network analysis reveals TNF-induced angiogenesis. BMC Syst Biol 6(Suppl 2):S12
76. Chen Z, Kim SJ, Essani AB, Volin MV, Vila OM, Swedler W, Arami S, Volkov S, Sardin LV, Sweiss N, Shahrara S (2014) Characterising the expression and function of CCL28 and its corresponding receptor, CCR10, in RA pathogenesis. Ann Rheum Dis. doi:10.1136/annrheumdis-2013-204530
77. Shetty A, Hanson R, Korsten P, Shawagfeh M, Arami S, Volkov S, Vila O, Swedler W, Shunaigat AN, Smadi S, Sawaqed R, Perkins D, Shahrara S, Sweiss NJ (2014) Tocilizumab in the treatment of rheumatoid arthritis and beyond. Drug Des Dev Ther 8:349–364
78. Huang Q, Ma Y, Adebayo A, Pope RM (2007) Increased macrophage activation mediated through toll-like receptors in rheumatoid arthritis. Arthritis Rheum 56(7):2192–2201
79. Koch AE, Kunkel SL, Burrows JC, Evanoff HL, Haines GK, Pope RM, Strieter RM (1991) Synovial tissue macrophage as a source of the chemotactic cytokine IL-8. J Immunol 147(7):2187–2195
80. Cho ML, Ju JH, Kim HR, Oh HJ, Kang CM, Jhun JY, Lee SY, Park MK, Min JK, Park SH, Lee SH, Kim HY (2007) Toll-like receptor 2 ligand mediates the upregulation of angiogenic factor, vascular endothelial growth factor and interleukin-8/CXCL8 in human rheumatoid synovial fibroblasts. Immunol Lett 108(2):121–128
81. Koch AE, Polverini PJ, Kunkel SL, Harlow LA, DiPietro LA, Elner VM, Elner SG, Strieter RM (1992) Interleukin-8 as a macrophage-derived mediator of angiogenesis. Science 258(5089):1798–1801
82. Mehta VB, Hart J, Wewers MD (2001) ATP-stimulated release of interleukin (IL)-1beta and IL-18 requires priming by lipopolysaccharide and is independent of caspase-1 cleavage. J Biol Chem 276(6):3820–3826
83. Gracie JA, Forsey RJ, Chan WL, Gilmour A, Leung BP, Greer MR, Kennedy K, Carter R, Wei XQ, Xu D, Field M, Foulis A, Liew FY, McInnes IB (1999) A proinflammatory role for IL-18 in rheumatoid arthritis. J Clin Invest 104(10):1393–1401
84. Moller B, Kessler U, Rehart S, Kalina U, Ottmann OG, Kaltwasser JP, Hoelzer D, Kukoc-Zivojnov N (2002) Expression of interleukin-18 receptor in fibroblast-like synoviocytes. Arthritis Res 4:139–144
85. Verri WA Jr, Cunha TM, Ferreira SH, Wei X, Leung BP, Fraser A, McInnes IB, Liew FY, Cunha FQ (2007) IL-15 mediates antigen-induced neutrophil migration by triggering IL-18 production. Eur J Immunol 37(12):3373–3380
86. Marotte H, Ahmed S, Ruth JH, Koch AE (2010) Blocking ERK-1/2 reduces tumor necrosis factor alpha-induced interleukin-18 bioactivity in rheumatoid arthritis synovial fibroblasts by induction of interleukin-18 binding protein A. Arthritis Rheum 62(3):722–731
87. Volin MV, Koch AE (2011) Interleukin-18: a mediator of inflammation and angiogenesis in rheumatoid arthritis. J Interferon Cytokine Res 31(10):745–751
88. Canetti CA, Leung BP, Culshaw S, McInnes IB, Cunha FQ, Liew FY (2003) IL-18 enhances collagen-induced arthritis by recruiting neutrophils via TNF-alpha and leukotriene B4. J Immunol 171(2):1009–1015
89. Ruth JH, Park CC, Amin MA, Lesch C, Marotte H, Shahrara S, Koch AE (2010) Interleukin-18 as an in vivo mediator of monocyte recruitment in rodent models of rheumatoid arthritis. Arthritis Res Ther 12(3):R118
90. Amin MA, Rabquer BJ, Mansfield PJ, Ruth JH, Marotte H, Haas CS, Reamer EN, Koch AE (2010) Interleukin 18 induces angiogenesis in vitro and in vivo via Src and Jnk kinases. Ann Rheum Dis 69(12):2204–2212
91. Park CC, Morel JC, Amin MA, Connors MA, Harlow LA, Koch AE (2001) Evidence of IL-18 as a novel angiogenic mediator. J Immunol 167(3):1644–1653
92. Amin MA, Mansfield PJ, Pakozdi A, Campbell PL, Ahmed S, Martinez RJ, Koch AE (2007) Interleukin-18 induces angiogenic factors in rheumatoid arthritis synovial tissue fibroblasts via distinct signaling pathways. Arthritis Rheum 56(6):1787–1797
93. Morel JC, Park CC, Kumar P, Koch AE (2001) Interleukin-18 induces rheumatoid arthritis synovial fibroblast CXC chemokine production through NFkappaB activation. Lab Invest 81(10):1371–1383
94. Yoo JK, Kwon H, Khil LY, Zhang L, Jun HS, Yoon JW (2005) IL-18 induces monocyte chemotactic protein-1 production in macrophages through the phosphatidylinositol 3-kinase/Akt and MEK/ERK1/2 pathways. J Immunol 175(12):8280–8286
95. Onodera S, Tanji H, Suzuki K, Kaneda K, Mizue Y, Sagawa A, Nishihira J (1999) High expression of macrophage migration inhibitory factor in the synovial tissues of rheumatoid joints. Cytokine 11(2):163–167
96. Leech M, Metz C, Hall P, Hutchinson P, Gianis K, Smith M, Weedon H, Holdsworth SR, Bucala R, Morand EF (1999) Macrophage migration inhibitory factor in rheumatoid arthritis: evidence of proinflammatory function and regulation by glucocorticoids. Arthritis Rheum 42(8):1601–1608
97. Calandra T, Bernhagen J, Mitchell RA, Bucala R (1994) The macrophage is an important and previously unrecognized source of macrophage migration inhibitory factor. J Exp Med 179(6):1895–1902
98. Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377(6544):68–71
99. Donnelly SC, Haslett C, Reid PT, Grant IS, Wallace WA, Metz CN, Bruce LJ, Bucala R (1997) Regulatory role for macrophage migration inhibitory factor in acute respiratory distress syndrome. Nat Med 3(3):320–323
100. Onodera S, Kaneda K, Mizue Y, Koyama Y, Fujinaga M, Nishihira J (2000) Macrophage migration inhibitory factor up-regulates expression of matrix metalloproteinases in synovial fibroblasts of rheumatoid arthritis. J Biol Chem 275(1):444–450
101. Onodera S, Nishihira J, Koyama Y, Majima T, Aoki Y, Ichiyama H, Ishibashi T, Minami A (2004) Macrophage migration inhibitory factor up-regulates the expression of interleukin-8 messenger RNA in synovial fibroblasts of rheumatoid arthritis patients: common transcriptional regulatory mechanism between interleukin-8 and interleukin-1beta. Arthritis Rheum 50(5):1437–1447
102. Amin MA, Volpert OV, Woods JM, Kumar P, Harlow LA, Koch AE (2003) Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res 93(4):321–329
103. Nishihira J, Koyama Y, Mizue Y (1998) Identification of macrophage migration inhibitory factor (MIF) in human vascular endothelial cells and its induction by lipopolysaccharide. Cytokine 10(3):199–205
104. Ogawa H, Nishihira J, Sato Y, Kondo M, Takahashi N, Oshima T, Todo S (2000) An antibody for macrophage migration inhibitory factor suppresses tumour growth and inhibits tumour-associated angiogenesis. Cytokine 12(4):309–314
105. Leech M, Metz C, Santos L, Peng T, Holdsworth SR, Bucala R, Morand EF (1998) Involvement of macrophage migration inhibitory factor in the evolution of rat adjuvant arthritis. Arthritis Rheum 41(5):910–917
106. Santos LL, Dacumos A, Yamana J, Sharma L, Morand EF (2008) Reduced arthritis in MIF deficient mice is associated with reduced T cell activation: down-regulation of ERK MAP kinase phosphorylation. Clin Exp Immunol 152(2):372–380
107. Singh A, Leng L, Fan J, Gajda M, Brauer R, Fingerle-Rowson G, Bucala R, Illges H (2013) Macrophage-derived, macrophage migration inhibitory factor (MIF) is necessary to induce disease in the K/BxN serum-induced model of arthritis. Rheumatol Int 33(9):2301–2308
108. Szekanecz Z, Vegvari A, Szabo Z, Koch AE (2010) Chemokines and chemokine receptors in arthritis. Front Biosci (Schol Ed) 2:153–167
109. Maruotti N, Cantatore FP, Crivellato E, Vacca A, Ribatti D (2007) Macrophages in rheumatoid arthritis. Histol Histopathol 22(5):581–586
110. Asquith DL, Bryce SA, Nibbs RJ (2015) Targeting cell migration in rheumatoid arthritis. Curr Opin Rheumatol 27(2):204–211
111. Park YJ, Kim JY, Park J, Choi JJ, Kim WU, Cho CS (2014) Bone erosion is associated with reduction of circulating endothelial progenitor cells and endothelial dysfunction in rheumatoid arthritis. Arthritis Rheumatol 66(6):1450–1460
112. Wu PF, Lu ZP, Cai BB, Tian L, Zou C, Jiang KR, Miao Y (2013) Role of CXCL12/CXCR4 signaling axis in pancreatic cancer. Chin Med J 126(17):3371–3374
113. Wang H, Liu W, Wei D, Hu K, Wu X, Yao Y (2014) Effect of the LPA-mediated CXCL12–CXCR4 axis in the tumor proliferation, migration and invasion of ovarian cancer cell lines. Oncol Lett 7(5):1581–1585
114. Ghanem I, Riveiro ME, Paradis V, Faivre S, de Parga PM, Raymond E (2014) Insights on the CXCL12-CXCR4 axis in hepatocellular carcinoma carcinogenesis. Am J Transl Res 6(4):340–352
115. Villalvilla A, Gomez R, Roman-Blas JA, Largo R, Herrero-Beaumont G (2014) SDF-1 signaling: a promising target in rheumatic diseases. Expert Opin Ther Targets 18(9):1077–1087
116. Pablos JL, Santiago B, Galindo M, Torres C, Brehmer MT, Blanco FJ, Garcia-Lazaro FJ (2003) Synoviocyte-derived CXCL12 is displayed on endothelium and induces angiogenesis in rheumatoid arthritis. J Immunol 170(4):2147–2152
117. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, Kishimoto T, Nagasawa T (1998) The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 393(6685):591–594
118. Blades MC, Ingegnoli F, Wheller SK, Manzo A, Wahid S, Panayi GS, Perretti M, Pitzalis C (2002) Stromal cell-derived factor 1 (CXCL12) induces monocyte migration into human synovium transplanted onto SCID mice. Arthritis Rheum 46(3):824–836
119. Madge LA, Kluger MS, Orange JS, May MJ (2008) Lymphotoxin-alpha 1 beta 2 and LIGHT induce classical and noncanonical NF-kappa B-dependent proinflammatory gene expression in vascular endothelial cells. J Immunol 180(5):3467–3477
120. Noort AR, van Zoest KP, Weijers EM, Koolwijk P, Maracle CX, Novack DV, Siemerink MJ, Schlingemann RO, Tak PP, Tas SW (2014) NF-kappaB-inducing kinase is a key regulator of inflammation-induced and tumour-associated angiogenesis. J Pathol 234(3):375–385
121. Salcedo R, Wasserman K, Young HA, Grimm MC, Howard OM, Anver MR, Kleinman HK, Murphy WJ, Oppenheim JJ (1999) Vascular endothelial growth factor and basic fibroblast growth factor induce expression of CXCR4 on human endothelial cells: in vivo neovascularization induced by stromal-derived factor-1alpha. Am J Pathol 154(4):1125–1135
122. Rempel SA, Dudas S, Ge S, Gutierrez JA (2000) Identification and localization of the cytokine SDF1 and its receptor, CXC chemokine receptor 4, to regions of necrosis and angiogenesis in human glioblastoma. Clin Cancer Res 6(1):102–111
123. Koshiba T, Hosotani R, Miyamoto Y, Ida J, Tsuji S, Nakajima S, Kawaguchi M, Kobayashi H, Doi R, Hori T, Fujii N, Imamura M (2000) Expression of stromal cell-derived factor 1 and CXCR4 ligand receptor system in pancreatic cancer: a possible role for tumor progression. Clin Cancer Res 6(9):3530–3535
124. Matthys P, Hatse S, Vermeire K, Wuyts A, Bridger G, Henson GW, De Clercq E, Billiau A, Schols D (2001) AMD3100, a potent and specific antagonist of the stromal cell-derived factor-1 chemokine receptor CXCR4, inhibits autoimmune joint inflammation in IFN-gamma receptor-deficient mice. J Immunol 167(8):4686–4692
125. Ruth JH, Haas CS, Park CC, Amin MA, Martinez RJ, Haines GK III, Shahrara S, Campbell PL, Koch AE (2006) CXCL16-mediated cell recruitment to rheumatoid arthritis synovial tissue and murine lymph nodes is dependent upon the MAPK pathway. Arthritis Rheum 54(3):765–778
126. Katschke KJ Jr, Rottman JB, Ruth JH, Qin S, Wu L, LaRosa G, Ponath P, Park CC, Pope RM, Koch AE (2001) Differential expression of chemokine receptors on peripheral blood, synovial fluid, and synovial tissue monocytes/macrophages in rheumatoid arthritis. Arthritis Rheum 44(5):1022–1032
127. Ruth JH, Rottman JB, Katschke KJ Jr, Qin S, Wu L, LaRosa G, Ponath P, Pope RM, Koch AE (2001) Selective lymphocyte chemokine receptor expression in the rheumatoid joint. Arthritis Rheum 44(12):2750–2760
128. Shahrara S, Amin MA, Woods JM, Haines GK, Koch AE (2003) Chemokine receptor expression and in vivo signaling pathways in the joints of rats with adjuvant-induced arthritis. Arthritis Rheum 48(12):3568–3583
129. Shahrara S, Proudfoot AE, Woods JM, Ruth JH, Amin MA, Park CC, Haas CS, Pope RM, Haines GK, Zha YY, Koch AE (2005) Amelioration of rat adjuvant-induced arthritis by Met-RANTES. Arthritis Rheum 52(6):1907–1919
130. Shahrara S, Proudfoot AE, Park CC, Volin MV, Haines GK, Woods JM, Aikens CH, Handel TM, Pope RM (2008) Inhibition of monocyte chemoattractant protein-1 ameliorates rat adjuvant-induced arthritis. J Immunol 180(5):3447–3456
131. Pickens SR, Chamberlain ND, Volin MV, Pope RM, Talarico NE, Mandelin AM II, Shahrara S (2012) Role of the CCL21 and CCR7 pathways in rheumatoid arthritis angiogenesis. Arthritis Rheum 64(8):2471–2481
132. Ruth JH, Volin MV, Haines GK III, Woodruff DC, Katschke KJ Jr, Woods JM, Park CC, Morel JC, Koch AE (2001) Fractalkine, a novel chemokine in rheumatoid arthritis and in rat adjuvant-induced arthritis. Arthritis Rheum 44(7):1568–1581
133. Garcia GE, Xia Y, Chen S, Wang Y, Ye RD, Harrison JK, Bacon KB, Zerwes HG, Feng L (2000) NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1beta, TNF-alpha, and LPS. J Leukoc Biol 67(4):577–584
134. Imaizumi T, Matsumiya T, Fujimoto K, Okamoto K, Cui X, Ohtaki U, Hidemi Yoshida, Satoh K (2000) Interferon-gamma stimulates the expression of CX3CL1/fractalkine in cultured human endothelial cells. Tohoku J Exp Med 192(2):127–139
135. Volin MV, Woods JM, Amin MA, Connors MA, Harlow LA, Koch AE (2001) Fractalkine: a novel angiogenic chemokine in rheumatoid arthritis. Am J Pathol 159(4):1521–1530
136. Murphy G, Knauper V, Atkinson S, Butler G, English W, Hutton M, Stracke J, Clark I (2002) Matrix metalloproteinases in arthritic disease. Arthritis Res 4(Suppl 3):S39–S49
137. Pap T, Shigeyama Y, Kuchen S, Fernihough JK, Simmen B, Gay RE, Billingham M, Gay S (2000) Differential expression pattern of membrane-type matrix metalloproteinases in rheumatoid arthritis. Arthritis Rheum 43(6):1226–1232
138. Ahrens D, Koch AE, Pope RM, Stein-Picarella M, Niedbala MJ (1996) Expression of matrix metalloproteinase 9 (96-kd gelatinase B) in human rheumatoid arthritis. Arthritis Rheum 39(9):1576–1587
139. Freemont AJ, Hampson V, Tilman R, Goupille P, Taiwo Y, Hoyland JA (1997) Gene expression of matrix metalloproteinases 1, 3, and 9 by chondrocytes in osteoarthritic human knee articular cartilage is zone and grade specific. Ann Rheum Dis 56(9):542–549
140. Vincenti MP, Brinckerhoff CE (2002) Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 4:157–164
141. Brinckerhoff CE, Matrisian LM (2002) Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 3(3):207–214
142. Akhavani MA, Madden L, Buysschaert I, Sivakumar B, Kang N, Paleolog EM (2009) Hypoxia upregulates angiogenesis and synovial cell migration in rheumatoid arthritis. Arthritis Res Ther 11(3):R64
143. Burrage PS, Mix KS, Brinckerhoff CE (2006) Matrix metalloproteinases: role in arthritis. Front Biosci 11:529–543
144. Kim KS, Choi HM, Lee YA, Choi IA, Lee SH, Hong SJ, Yang HI, Yoo MC (2011) Expression levels and association of gelatinases MMP-2 and MMP-9 and collagenases MMP-1 and MMP-13 with VEGF in synovial fluid of patients with arthritis. Rheumatol Int 31(4):543–547
145. Mengshol JA, Mix KS, Brinckerhoff CE (2002) Matrix metalloproteinases as therapeutic targets in arthritic diseases: bull’s-eye or missing the mark? Arthritis Rheum 46(1):13–20
146. Rabquer BJ, Pakozdi A, Michel JE, Gujar BS, Haines GK III, Imhof BA, Koch AE (2008) Junctional adhesion molecule C mediates leukocyte adhesion to rheumatoid arthritis synovium. Arthritis Rheum 58(10):3020–3029
147. Rabquer BJ, Amin MA, Teegala N, Shaheen MK, Tsou PS, Ruth JH, Lesch CA, Imhof BA, Koch AE (2010) Junctional adhesion molecule-C is a soluble mediator of angiogenesis. J Immunol 185(3):1777–1785
148. Palmer G, Busso N, Aurrand-Lions M, Talabot-Ayer D, Chobaz-Peclat V, Zimmerli C, Hammel P, Imhof BA, Gabay C (2007) Expression and function of junctional adhesion molecule-C in human and experimental arthritis. Arthritis Res Ther 9(4):R65
149. Leinster DA, Colom B, Whiteford JR, Ennis DP, Lockley M, McNeish IA, Aurrand-Lions M, Chavakis T, Imhof BA, Balkwill FR, Nourshargh S (2013) Endothelial cell junctional adhesion molecule C plays a key role in the development of tumors in a murine model of ovarian cancer. FASEB J 27(10):4244–4253
150. Mojcik CF, Shevach EM (1997) Adhesion molecules: a rheumatologic perspective. Arthritis Rheum 40(6):991–1004
151. McMurray RW (1996) Adhesion molecules in autoimmune disease. Semin Arthritis Rheum 25(4):215–233
152. Hosaka S, Shah MR, Pope RM, Koch AE (1996) Soluble forms of P-selectin and intercellular adhesion molecule-3 in synovial fluids. Clin Immunol Immunopathol 78(3):276–282
153. Koch AE, Shah MR, Harlow LA, Lovis RM, Pope RM (1994) Soluble intercellular adhesion molecule-1 in arthritis. Clin Immunol Immunopathol 71:208–215
154. Koch AE, Halloran MM, Haskell CJ, Shah MR, Polverini PJ (1995) Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature 376(6540):517–519
155. Schimmer RC, Schrier DJ, Flory CM, Dykens J, Tung DK, Jacobson PB, Friedl HP, Conroy MC, Schimmer BB, Ward PA (1997) Streptococcal cell wall-induced arthritis: requirements for neutrophils, P-selectin, intercellular adhesion molecule-1, and macrophage-inflammatory protein-2. J Immunol 159:4103–4108
156. Kakimoto K, Nakamura T, Ishii K, Takashi T, Iigou H, Yagita H, Okumura K, Onoue K (1992) The effect of anti-adhesion molecule antibody on the development of collagen-induced arthritis. Cell Immunol 142(2):326–337
157. Klimiuk PA, Sierakowski S, Latosiewicz R, Cylwik JP, Cylwik B, Skowronski J, Chwiecko J (2002) Soluble adhesion molecules (ICAM-1, VCAM-1, and E-selectin) and vascular endothelial growth factor (VEGF) in patients with distinct variants of rheumatoid synovitis. Ann Rheum Dis 61(9):804–809
158. Shahrara S, Huang Q, Mandelin AM II, Pope RM (2008) TH-17 cells in rheumatoid arthritis. Arthritis Res Ther 10(4):R93
159. Kim SJ, Chen Z, Chamberlain ND, Volin MV, Swedler W, Volkov S, Sweiss N, Shahrara S (2013) Angiogenesis in rheumatoid arthritis is fostered directly by Toll-like receptor 5 ligation and indirectly through interleukin-17 induction. Arthritis Rheum 65(8):2024–2036
160. Pickens SR, Chamberlain ND, Volin MV, Mandelin AM II, Agrawal H, Matsui M, Yoshimoto T, Shahrara S (2011) Local expression of interleukin-27 ameliorates collagen-induced arthritis. Arthritis Rheum 63(8):2289–2298
161. Springer TA (1994) Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76(2):301–314
162. Lasky LA (1992) Selectins: interpreters of cell-specific carbohydrate information during inflammation. Science 258(5084):964–969
163. Bevilacqua MP, Stengelin S, Gimbrone MA Jr, Seed B (1989) Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins. Science 243(4895):1160–1165
164. Maruotti N, Cantatore FP, Ribatti D (2014) Putative effects of potentially anti-angiogenic drugs in rheumatic diseases. Eur J Clin Pharmacol 70(2):135–140
165. Lubberts E, Koenders MI, Oppers-Walgreen B, van den Bersselaar L, Coenen-de Roo CJ, Joosten LA, van den Berg WB (2004) Treatment with a neutralizing anti-murine interleukin-17 antibody after the onset of collagen-induced arthritis reduces joint inflammation, cartilage destruction, and bone erosion. Arthritis Rheum 50(2):650–659
166. Genovese MC, Durez P, Richards HB, Supronik J, Dokoupilova E, Mazurov V, Aelion JA, Lee SH, Codding CE, Kellner H, Ikawa T, Hugot S, Mpofu S (2013) Efficacy and safety of secukinumab in patients with rheumatoid arthritis: a phase II, dose-finding, double-blind, randomised, placebo controlled study. Ann Rheum Dis 72(6):863–869
167. Genovese MC, Greenwald M, Cho CS, Berman A, Jin L, Cameron GS, Benichou O, Xie L, Braun D, Berclaz PY, Banerjee S (2014) A phase II randomized study of subcutaneous ixekizumab, an anti-interleukin-17 monoclonal antibody, in rheumatoid arthritis patients who were naive to biologic agents or had an inadequate response to tumor necrosis factor inhibitors. Arthritis Rheumatol 66(7):1693–1704
168. Mease PJ, Genovese MC, Greenwald MW, Ritchlin CT, Beaulieu AD, Deodhar A, Newmark R, Feng J, Erondu N, Nirula A (2014) Brodalumab, an anti-IL17RA monoclonal antibody, in psoriatic arthritis. N Engl J Med 370(24):2295–2306
169. Yao HP, Qian Y, Shao XT, Xu ZR, Cheng LF, Feng L, Wu NP, Yang YM (2010) Construction of a recombinant adenovirus vector expressing IL-18BP/IL-4 fusion gene and the anti-inflammatory effect induced by this gene on lipopolysaccharide-stimulated synovial fibroblasts. Inflamm Res 59(2):97–104
170. Mistry P, Reid J, Pouliquen I, McHugh S, Abberley L, DeWall S, Taylor A, Tong X, Rocha Del Cura M, McKie E (2014) Safety, tolerability, pharmacokinetics, and pharmacodynamics of single-dose antiinterleukin-18 mAb GSK1070806 in healthy and obese subjects. Int J Clin Pharmacol Ther 52(10):867–879
171. Tak PP, Bacchi M, Bertolino M (2006) Pharmacokinetics of IL-18 binding protein in healthy volunteers and subjects with rheumatoid arthritis or plaque psoriasis. Eur J Drug Metab Pharmacokinet 31(2):109–116
172. Greven D, Leng L, Bucala R (2010) Autoimmune diseases: MIF as a therapeutic target. Expert Opin Ther Targets 14(3):253–264
173. Cournia Z, Leng L, Gandavadi S, Du X, Bucala R, Jorgensen WL (2009) Discovery of human macrophage migration inhibitory factor (MIF)-CD74 antagonists via virtual screening. J Med Chem 52(2):416–424
174. Fruehauf S (2013) Current clinical indications for plerixafor. Transfus Med Hemother 40(4):246–250
175. Kuhne MR, Mulvey T, Belanger B, Chen S, Pan C, Chong C, Cao F, Niekro W, Kempe T, Henning KA, Cohen LJ, Korman AJ, Cardarelli PM (2013) BMS-936564/MDX-1338: a fully human anti-CXCR4 antibody induces apoptosis in vitro and shows antitumor activity in vivo in hematologic malignancies. Clin Cancer Res 19(2):357–366
176. Coxon A, Bready J, Min H, Kaufman S, Leal J, Yu D, Lee TA, Sun JR, Estrada J, Bolon B, McCabe J, Wang L, Rex K, Caenepeel S, Hughes P, Cordover D, Kim H, Han SJ, Michaels ML, Hsu E, Shimamoto G, Cattley R, Hurh E, Nguyen L, Wang SX, Ndifor A, Hayward IJ, Falcon BL, McDonald DM, Li L, Boone T, Kendall R, Radinsky R, Oliner JD (2010) Context-dependent role of angiopoietin-1 inhibition in the suppression of angiogenesis and tumor growth: implications for AMG 386, an angiopoietin-1/2-neutralizing peptibody. Mol Cancer Ther 9(10):2641–2651
177. Weeraratne DK, Lofgren J, Dinnogen S, Swanson SJ, Zhong ZD (2013) Development of a biosensor-based immunogenicity assay capable of blocking soluble drug target interference. J Immunol Methods 396(1–2):44–55
178. Hah YS, Koh YJ, Lim HS, Kim HO, Cheon YH, Noh HS, Jang KY, Lee SY, Lee GM, Koh GY, Lee SI (2013) Double-antiangiogenic protein DAAP targeting vascular endothelial growth factor A and angiopoietins attenuates collagen-induced arthritis. Arthritis Res Ther 15(4):R85
179. Dorman G, Cseh S, Hajdu I, Barna L, Konya D, Kupai K, Kovacs L, Ferdinandy P (2010) Matrix metalloproteinase inhibitors: a critical appraisal of design principles and proposed therapeutic utility. Drugs 70(8):949–964
180. Thabet MM, Huizinga TW (2006) Drug evaluation: apratastat, a novel TACE/MMP inhibitor for rheumatoid arthritis. Curr Opin Investig Drugs 7(11):1014–1019
181. Gordon KB, Papp KA, Hamilton TK, Walicke PA, Dummer W, Li N, Bresnahan BW, Menter A (2003) Efalizumab for patients with moderate to severe plaque psoriasis: a randomized controlled trial. JAMA 290(23):3073–3080
182. Prater EF, Day A, Patel M, Menter A (2014) A retrospective analysis of 72 patients on prior efalizumab subsequent to the time of voluntary market withdrawal in 2009. J Drugs Dermatol 13(6):712–718
183. Jones R (2000) Rovelizumab (ICOS Corp). IDrugs Investig Drugs J 3(4):442–446
184. Kavanaugh AF, Davis LS, Nichols LA, Norris SH, Rothlein R, Scharschmidt LA, Lipsky PE (1994) Treatment of refractory rheumatoid arthritis with a monoclonal antibody to intercellular adhesion molecule 1. Arthritis Rheum 37(7):992–999
185. Kavanaugh AF, Davis LS, Jain RI, Nichols LA, Norris SH, Lipsky PE (1996) A phase I/II open label study of the safety and efficacy of an anti-ICAM-1 (intercellular adhesion molecule-1; CD54) monoclonal antibody in early rheumatoid arthritis. J Rheumatol 23(8):1338–1344
186. Kavanaugh AF, Schulze-Koops H, Davis LS, Lipsky PE (1997) Repeat treatment of rheumatoid arthritis patients with a murine anti-intercellular adhesion molecule 1 monoclonal antibody. Arthritis Rheum 40(5):849–853
187. Pucci E, Giuliani G, Solari A, Simi S, Minozzi S, Di Pietrantonj C, Galea I (2011) Natalizumab for relapsing remitting multiple sclerosis. Cochrane Database Syst Rev 10:CD007621
188. Podar K, Zimmerhackl A, Fulciniti M, Tonon G, Hainz U, Tai YT, Vallet S, Halama N, Jager D, Olson DL, Sattler M, Chauhan D, Anderson KC (2011) The selective adhesion molecule inhibitor Natalizumab decreases multiple myeloma cell growth in the bone marrow microenvironment: therapeutic implications. Br J Haematol 155(4):438–448
189. Mitroulis I, Alexaki VI, Kourtzelis I, Ziogas A, Hajishengallis G, Chavakis T (2015) Leukocyte integrins: role in leukocyte recruitment and as therapeutic targets in inflammatory disease. Pharmacol Ther 147:123–135