In vivo imaging implicates CCR2+ monocytes as regulators of neutrophil recruitment during arthritis

Cellular Immunology

Volumn 278, Issue 1-2, 2012, Pages 103-112

  Wang, Baomei ^a   Zinselmeyer, Bernd H ^a   Runnels, Herbert A ^b   LaBranche, Timothy P ^b   Morton, Phillip A ^b   Kreisel, Daniel ^a   Mack, Matthias ^c   Nickerson Nutter, Cheryl ^b   Allen, Paul M ^a   Miller, Mark J ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PFIZER INC   (United States)

^c UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Arthritis; K B N serum; Monocyte; Neutrophil; Two photon microscopy

Indexed keywords

CHEMOKINE RECEPTOR CCR2; CLODRONIC ACID; LIPOSOME; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY MC 21; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL ISOLATION; CELL MIGRATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FOOT PAD; HISTOPATHOLOGY; IN VIVO STUDY; MONOCYTE; MOUSE; MULTIPHOTON MICROSCOPY; NEUTROPHIL CHEMOTAXIS; NEUTROPHIL RECRUITMENT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; T CELL DEPLETION; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CLODRONIC ACID; FEMALE; HUMANS; INJECTIONS, SUBCUTANEOUS; LIPOSOMES; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE, MULTIPHOTON; MONOCYTES; NEUTROPHIL INFILTRATION; NEUTROPHILS; RECEPTORS, CCR2;

BACTERIA (MICROORGANISMS);

EID: 84868283623     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2012.07.005     Document Type: Article

References (50)

1. Feldmann M., Brennan F.M., Maini R.N. Rheumatoid Arthritis. Cell 1996, 85:307-310.
2. Norberg B., Eriksson S. Joint fluid leukocytosis of patients with rheumatoid arthritis evidence for neutrophil and monocyte chemotaxis in vivo. Clin. Rheumatol. 1983, 2:237-242.
3. Ley K., Laudanna C., Cybulsky M.I., Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 2007, 7:678-689.
4. Chou R.C., Kim N.D., Sadik C.D., Seung E., Lan Y., Byrne M.H., et al. Lipid-cytokine-chemokine cascade drives neutrophil recruitment in a murine model of inflammatory arthritis. Immunity 2010, 33:266-278.
5. Edwards S.W., Hallett M.B. Seeing the wood for the trees: the forgotten role of neutrophils in rheumatoid arthritis. Immunol. Today 1997, 18:320-324.
6. Barsante M.M., Cunha T.M., Allegretti M., Cattani F., Policani F., Bizzarri C., et al. Blockade of the chemokine receptor CXCR2 ameliorates adjuvant-induced arthritis in rats. Br. J. Pharmacol. 2008, 153:992-1002.
7. Grespan R., Fukada S.Y., Lemos H.P., Vieira S.M., Napimoga M.H., Teixeira M.M., et al. CXCR2-specific chemokines mediate leukotriene B4-dependent recruitment of neutrophils to inflamed joints in mice with antigen-induced arthritis. Arthritis Rheum. 2008, 58:2030-2040.
8. Monach P.A., Nigrovic P.A., Chen M., Hock H., Lee D.M., Benoist C., et al. Neutrophils in a mouse model of autoantibody-mediated arthritis: critical producers of Fc receptor γ, the receptor for C5a, and lymphocyte function-associated antigen 1. Arthritis Rheum. 2010, 62:753-764.
9. Wipke B.T., Allen P.M. Essential role of neutrophils in the initiation and progression of a murine model of rheumatoid arthritis. J Immunol 2001, 167:1601-1608.
10. Bruhl H., Cihak J., Schneider M.A., Plachy J., Rupp T., Wenzel I., et al. 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.
11. Nanki T., Urasaki Y., Imai T., Nishimura M., Muramoto K., Kubota T., et al. Inhibition of fractalkine ameliorates murine collagen-induced arthritis. J. Immunol. 2004, 173:7010-7016.
12. Geissmann F., Jung S., Littman D.R. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003, 19:71-82.
13. Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D.N., et al. Nomenclature of monocytes and dendritic cells in blood. Blood 2010, 116:e74-e80.
14. Auffray C., Fogg D., Garfa M., Elain G., Join-Lambert O., Kayal S., et al. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007, 317:666-670.
15. Kreisel D., Nava R.G., Li W., Zinselmeyer B.H., Wang B., Lai J., et al. In vivo two-photon imaging reveals monocyte-dependent neutrophil extravasation during pulmonary inflammation. Proc. Nat. Acad. Sci. 2010, 107:18073-18078.
16. Maus U.A., Waelsch K., Kuziel W.A., Delbeck T., Mack M., Blackwell T.S., et al. Monocytes are potent facilitators of alveolar neutrophil emigration during lung inflammation: role of the CCL2-CCR2 axis. J Immunol 2003, 170:3273-3278.
17. Monach P., Hattori K., Huang H., Hyatt E., Morse J., Nguyen L., et al. The K/BxN Mouse Model of Inflammatory Arthritis. 2007, 269-282.
18. Garcia-Vicuna R., Gomez-Gaviro M.V., Dominguez-Luis M.J., Pec M.K., Gonzalez-Alvaro I., Alvaro-Gracia J.M., et al. CC and CXC chemokine receptors mediate migration, proliferation, and matrix metalloproteinase production by fibroblast-like synoviocytes from rheumatoid arthritis patients. Arthritis Rheum. 2004, 50:3866-3877.
19. Valencia X., Higgins J.M., Kiener H.P., Lee D.M., Podrebarac T.A., Dascher C.C., et al. Cadherin-11 provides specific cellular adhesion between fibroblast-like synoviocytes. J. Exp. Med. 2004, 200:1673-1679.
20. B. Wang, B.H. Zinselmeyer, J.R. McDole, P.A. Gieselman, M.J. Miller, Non-invasive imaging of leukocyte homing and migration in vivo, J. Vis. Exp. 46 (2010) e2062.
21. Zinselmeyer B.H, Lynch J., Zhang X., Aoshi T., Miller M. Video-rate two-photon imaging of mouse paw - a promising model for studying leukocyte recruitment dynamics during inflammation. Inflamm. Res. 2008, 57:93-96.
22. Graham D.B., Zinselmeyer B.H., Mascarenhas F., Delgado R., Miller M.J., Swat W. ITAM Signaling by Vav Family Rho Guanine Nucleotide Exchange Factors Regulates Interstitial Transit Rates of Neutrophils In Vivo. PLoS ONE 2009, 4:e4652.
23. Zinselmeyer B.H., Dempster J., Wokosin D.L., Cannon J.J., Pless R., Parker I., et al. Two-photon microscopy and multidimensional analysis of cell dynamics. Methods Enzymol. 2009, 461:349-378. Chapter 16.
24. Oh D.-J., Dursun B., He Z., Lu L., Hoke T.S., Ljubanovic D., et al. Fractalkine receptor (CX3CR1) inhibition is protective against ischemic acute renal failure in mice. Am. J. Physiol. - Renal Physiol. 2008, 294:F264-F271.
25. McDonald B., Pittman K., Menezes G.B., Hirota S.A., Slaba I., Waterhouse C.C.M., et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 2010, 330:362-366.
26. Weninger W., Carlsen H.S., Goodarzi M., Moazed F., Crowley M.A., Baekkevold E.S., et al. Naive T cell recruitment to nonlymphoid tissues: a role for endothelium-expressed CC chemokine ligand 21 in autoimmune disease and lymphoid neogenesis. J. Immunol. 2003, 170:4638-4648.
27. Phillipson M., Heit B., Colarusso P., Liu L., Ballantyne C.M., Kubes P. Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 2006, 203:2569-2575.
28. Chtanova T., Schaeffer M., Han S.-J., van Dooren G.G., Nollmann M., Herzmark P., et al. Dynamics of neutrophil migration in lymph nodes during infection. Immunity 2008, 29:487-496.
29. Peters N.C., Egen J.G., Secundino N., Debrabant A., Kimblin N., Kamhawi S., et al. In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008, 321:970-974.
30. Calderon B., Suri A., Unanue E.R. In CD4+ T-cell-induced diabetes, macrophages are the final effector cells that mediate islet beta-cell killing: studies from an acute model. Am. J. Pathol. 2006, 169:2137-2147.
31. Van Rooijen N.S.A. Liposome mediated depletion of macrophages mechanism of action preparation of liposomes and applications. J. Immunol. Meth. 1994, 174:83-93.
32. Solomon S., Rajasekaran N., Jeisy-Walder E., Snapper S.B., Illges H. A crucial role for macrophages in the pathology of K/B×N serum-induced arthritis. Eur. J. Immunol. 2005, 35:3064-3073.
33. Sunderkotter C., Nikolic T., Dillon M.J., Van Rooijen N., Stehling M., Drevets D.A., et al. Subpopulations of mouse blood monocytes differ in maturation stage and inflammatory response. J. Immunol. 2004, 172:4410-4417.
34. Tacke F., Alvarez D., Kaplan T.J., Jakubzick C., Spanbroek R., Llodra J., et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Investig. 2007, 117:185-194.
35. Quinones M.P., Ahuja S.K., Jimenez F., Schaefer J., Garavito E., Rao A., et al. Experimental arthritis in CC chemokine receptor 2-null mice closely mimics severe human rheumatoid arthritis. J. Clin. Investig. 2004, 113:856-866.
36. Brühl H., Cihak J., Plachý J., Kunz-Schughart L., Niedermeier M., Denzel A., et al. Targeting of Gr-1+, CCR2+ monocytes in collagen-induced arthritis. Arthritis Rheum. 2007, 56:2975-2985.
37. Souto F.O., Alves-Filho J.C., Turato W.M., Auxiliadora-Martins M., Basile-Filho A., Cunha F.Q. Essential role of CCR2 in neutrophil tissue infiltration and multiple organ dysfunction in sepsis. Am. J. Respir. Crit. Care Med. 2011, 183:234-242.
38. Wipke B.T., Wang Z., Nagengast W., Reichert D.E., Allen P.M. Staging the initiation of autoantibody-induced arthritis: a critical role for immune complexes. J. Immunol. 2004, 172:7694-7702.
39. Matsumoto I., Maccioni M., Lee D.M., Maurice M., Simmons B., Brenner M., et al. How antibodies to a ubiquitous cytoplasmic enzyme may provoke joint-specific autoimmune disease. Nat. Immunol. 2002, 3:360-365.
40. Henderson R.B., Hobbs J.A., Mathies M., Hogg N. Rapid recruitment of inflammatory monocytes is independent of neutrophil migration. Blood 2003, 102:328-335.
41. Soehnlein O., Zernecke A., Eriksson E.E., Rothfuchs A.G., Pham C.T., Herwald H., et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 2008, 112:1461-1471.
42. Liu L., Kubes P. Molecular mechanisms of leukocyte recruitment: organ-specific mechanisms of action. Thromb. Haemost. 2003, 89:213-220.
43. Brühl H., Wagner K., Kellner H., Schattenkirchner M., Schlöndorff D., Mack M. Surface expression of CC- and CXC-chemokine receptors on leucocyte subsets in inflammatory joint diseases. Clin. Exp. Immunol. 2001, 126:551-559.
44. Brodmerkel C.M., Huber R., Covington M., Diamond S., Hall L., Collins R., et al. Discovery and pharmacological characterization of a novel rodent-active CCR2 antagonist, INCB3344. J. Immunol. 2005, 175:5370-5378.
45. Haringman J.J., Smeets T.J.M., Reinders-Blankert P., Tak P.P. Chemokine and chemokine receptor expression in paired peripheral blood mononuclear cells and synovial tissue of patients with rheumatoid arthritis, osteoarthritis, and reactive arthritis. Ann. Rheum. Dis. 2006, 65:294-300.
46. Jacobs J.P., Ortiz-Lopez A., Campbell J.J., Gerard C.J., Mathis D., Benoist C. Deficiency of CXCR2, but not other chemokine receptors, attenuates autoantibody-mediated arthritis in a murine model. Arthritis Rheum. 2010, 62:1921-1932.
47. Saederup N., Chan L., Lira S.A., Charo I.F. Fractalkine deficiency markedly reduces macrophage accumulation and atherosclerotic lesion formation in CCR2-/- mice. Evidence for independent chemokine functions in atherogenesis. Circulation 2008, 117:1642-1648.
48. Angyal A., Egelston C., Kobezda T., Olasz K., László A., Glant T.T., et al. Development of proteoglycan-induced arthritis depends on T cell-supported autoantibody production, but does not involve significant influx of T cells into the joints. Arthritis Res. Ther. 2010, 12:R44.
49. van der Goes A., Wouters D., van der Pol S.M.A., Huizinga R., Ronken E., Adamson P., et al. Reactive oxygen species enhance the migration of monocytes across the blood-brain barrier in vitro. FASEB J. 2001, 15:1852-1854.
50. Huber A.R., Kunkel S.L., Todd R.F., Weiss S.J. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 1991, 254:99-102.