CD163+ M2c-like macrophages predominate in renal biopsies from patients with lupus nephritis

Arthritis Research and Therapy

Volumn 18, Issue 1, 2016, Pages

  Olmes, Gregor ^a   Büttner Herold, Maike ^a   Ferrazzi, Fulvia ^a   Distel, Luitpold ^a   Amann, Kerstin ^a   Daniel, Christoph ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Lupus nephritis; Macrophage subtypes; Macrophages; T reg cells

Indexed keywords

ANTIGEN; CD163 ANTIGEN; CD206 ANTIGEN; CD68 ANTIGEN; CREATININE; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; UREA; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL INFILTRATION; CELL SUBPOPULATION; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE COURSE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KIDNEY BIOPSY; KIDNEY FUNCTION; LUPUS ERYTHEMATOSUS NEPHRITIS; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PROTEINURIA; UREA BLOOD LEVEL; BIOPSY; CLUSTER ANALYSIS; CYTOLOGY; IMMUNOLOGY; MIDDLE AGED; PATHOLOGY; REGULATORY T LYMPHOCYTE;

ADULT; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BIOPSY; CELL DIFFERENTIATION; CLUSTER ANALYSIS; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; LUPUS NEPHRITIS; MACROPHAGES; MALE; MIDDLE AGED; RECEPTORS, CELL SURFACE; T-LYMPHOCYTES, REGULATORY;

EID: 84963594033     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/s13075-016-0989-y     Document Type: Article

References (57)

1. Maroz N, Segal MS. Lupus nephritis and end-stage kidney disease. Am J Med Sci. 2013;346(4):319-23.
2. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J Am Soc Nephrol. 2004;15(2):241-50.
3. Kuroiwa T, Lee EG. Cellular interactions in the pathogenesis of lupus nephritis: the role of T cells and macrophages in the amplification of the inflammatory process in the kidney. Lupus. 1998;7(9):597-603.
4. Bergtold A, Gavhane A, D'Agati V, Madaio M, Clynes R. FcR-bearing myeloid cells are responsible for triggering murine lupus nephritis. J Immunol. 2006;177(10):7287-95.
5. Biermann MH, Veissi S, Maueroder C, Chaurio R, Berens C, Herrmann M, Munoz LE. The role of dead cell clearance in the etiology and pathogenesis of systemic lupus erythematosus: dendritic cells as potential targets. Expert Rev Clin Immunol. 2014;10(9):1151-64.
6. Tucci M, Stucci S, Strippoli S, Silvestris F. Cytokine overproduction, T-cell activation, and defective T-regulatory functions promote nephritis in systemic lupus erythematosus. J Biomed Biotechnol. 2010;2010:457146.
7. Williams TM, Little MH, Ricardo SD. Macrophages in renal development, injury, and repair. Semin Nephrol. 2010;30(3):255-67.
8. Chalmers SA, Chitu V, Herlitz LC, Sahu R, Stanley ER, Putterman C. Macrophage depletion ameliorates nephritis induced by pathogenic antibodies. J Autoimmun. 2015;57:42-52.
9. Ferenbach DA, Sheldrake TA, Dhaliwal K, Kipari TM, Marson LP, Kluth DC, Hughes J. Macrophage/monocyte depletion by clodronate, but not diphtheria toxin, improves renal ischemia/reperfusion injury in mice. Kidney Int. 2012;82(8):928-33.
10. Ko GJ, Boo CS, Jo SK, Cho WY, Kim HK. Macrophages contribute to the development of renal fibrosis following ischaemia/reperfusion-induced acute kidney injury. Nephrol Dial Transplant. 2008;23(3):842-52.
11. Vielhauer V, Kulkarni O, Reichel CA, Anders HJ. Targeting the recruitment of monocytes and macrophages in renal disease. Semin Nephrol. 2010;30(3):318-33.
12. Hasegawa H, Kohno M, Sasaki M, Inoue A, Ito MR, Terada M, Hieshima K, Maruyama H, Miyazaki J, Yoshie O et al. Antagonist of monocyte chemoattractant protein 1 ameliorates the initiation and progression of lupus nephritis and renal vasculitis in MRL/lpr mice. Arthritis Rheum. 2003;48(9):2555-66.
13. Bignon A, Gaudin F, Hemon P, Tharinger H, Mayol K, Walzer T, Loetscher P, Peuchmaur M, Berrebi D, Balabanian K. CCR1 inhibition ameliorates the progression of lupus nephritis in NZB/W mice. J Immunol. 2014;192(3):886-96.
14. Liu H, Diao C, Wu C, Xia L, Duan H, Fang F, Ding S, Xiao W. Anti-macrophage-derived chemokine antibody relieves murine lupus nephritis. Rheumatol Int. 2011;31(11):1459-64.
15. Perez de Lema G, Maier H, Franz TJ, Escribese M, Chilla S, Segerer S, Camarasa N, Schmid H, Banas B, Kalaydjiev S et al. Chemokine receptor Ccr2 deficiency reduces renal disease and prolongs survival in MRL/lpr lupus-prone mice. J Am Soc Nephrol. 2005;16(12):3592-601.
16. Tanaka H, Oki E, Tsuruga K, Aizawa-Yashiro T, Ito Y, Sato N, Kawasaki Y, Suzuki J. Mizoribine attenuates renal injury and macrophage infiltration in patients with severe lupus nephritis. Clin Rheumatol. 2010;29(9):1049-54.
17. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 2004;25(12):677-86.
18. Ndisang JF, Mishra M. The heme oxygenase system selectively suppresses the proinflammatory macrophage m1 phenotype and potentiates insulin signaling in spontaneously hypertensive rats. Am J Hypertens. 2013;26(9):1123-31.
19. Anders HJ, Ryu M. Renal microenvironments and macrophage phenotypes determine progression or resolution of renal inflammation and fibrosis. Kidney Int. 2011;80(9):915-25.
20. Sironi M, Martinez FO, D'Ambrosio D, Gattorno M, Polentarutti N, Locati M, Gregorio A, Iellem A, Cassatella MA, Van Damme J et al. Differential regulation of chemokine production by Fcgamma receptor engagement in human monocytes: association of CCL1 with a distinct form of M2 monocyte activation (M2b, Type 2). J Leukoc Biol. 2006;80(2):342-9.
21. Lu J, Cao Q, Zheng D, Sun Y, Wang C, Yu X, Wang Y, Lee VW, Zheng G, Tan TK et al. Discrete functions of M2a and M2c macrophage subsets determine their relative efficacy in treating chronic kidney disease. Kidney Int. 2013;84(4):745-55.
22. Zizzo G, Guerrieri J, Dittman LM, Merrill JT, Cohen PL. Circulating levels of soluble MER in lupus reflect M2c activation of monocytes/macrophages, autoantibody specificities and disease activity. Arthritis Res Ther. 2013;15(6):R212.
23. Iwata Y, Bostrom EA, Menke J, Rabacal WA, Morel L, Wada T, Kelley VR. Aberrant macrophages mediate defective kidney repair that triggers nephritis in lupus-susceptible mice. J Immunol. 2012;188(9):4568-80.
24. Sahu R, Bethunaickan R, Singh S, Davidson A. Structure and function of renal macrophages and dendritic cells from lupus-prone mice. Arthritis Rheumatol. 2014;66(6):1596-607.
25. Orme J, Mohan C. Macrophage subpopulations in systemic lupus erythematosus. Discov Med. 2012;13(69):151-8.
26. Ciccia F, Alessandro R, Rizzo A, Accardo-Palumbo A, Raimondo S, Raiata F, Guggino G, Giardina A, De Leo G, Sireci G et al. Macrophage phenotype in the subclinical gut inflammation of patients with ankylosing spondylitis. Rheumatology (Oxford). 2014;53(1):104-13.
27. Edin S, Wikberg ML, Dahlin AM, Rutegard J, Oberg A, Oldenborg PA, Palmqvist R. The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PLoS One. 2012;7(10):e47045.
28. Gensel JC, Zhang B. Macrophage activation and its role in repair and pathology after spinal cord injury. Brain Res. 2015;1619:1-11.
29. You H, Gao T, Cooper TK, Brian Reeves W, Awad AS. Macrophages directly mediate diabetic renal injury. Am J Physiol Renal Physiol. 2013;305(12):F1719-27.
30. Ohlsson SM, Linge CP, Gullstrand B, Lood C, Johansson A, Ohlsson S, Lundqvist A, Bengtsson AA, Carlsson F, Hellmark T. Serum from patients with systemic vasculitis induces alternatively activated macrophage M2c polarization. Clin Immunol. 2014;152(1-2):10-9.
31. Hainz N, Thomas S, Neubert K, Meister S, Benz K, Rauh M, Daniel C, Wiesener M, Voll RE, Amann K. The proteasome inhibitor bortezomib prevents lupus nephritis in the NZB/W F1 mouse model by preservation of glomerular and tubulointerstitial architecture. Nephron Exp Nephrol. 2012;120(2):e47-58.
32. Solez K, Colvin RB, Racusen LC, Haas M, Sis B, Mengel M, Halloran PF, Baldwin W, Banfi G, Collins AB et al. Banff 07 classification of renal allograft pathology: updates and future directions. Am J Transplant. 2008;8(4):753-60.
33. Austin 3rd HA, Muenz LR, Joyce KM, Antonovych TT, Balow JE. Diffuse proliferative lupus nephritis: identification of specific pathologic features affecting renal outcome. Kidney Int. 1984;25(4):689-95.
34. Li J, Liu CH, Xu DL, Gao B. Significance of CD163-positive macrophages in proliferative glomerulonephritis. Am J Med Sci. 2015;350(5):387-92.
35. Brugos B, Vincze Z, Sipka S, Szegedi G, Zeher M. Serum and urinary cytokine levels of SLE patients. Pharmazie. 2012;67(5):411-3.
36. Cigni A, Pileri PV, Faedda R, Gallo P, Sini A, Satta AE, Marras R, Carta E, Argiolas D, Rum I et al. Interleukin 1, interleukin 6, interleukin 10, and tumor necrosis factor alpha in active and quiescent systemic lupus erythematosus. J Investig Med. 2014;62(5):825-9.
37. Tang Z, Niven-Fairchild T, Tadesse S, Norwitz ER, Buhimschi CS, Buhimschi IA, Guller S. Glucocorticoids enhance CD163 expression in placental Hofbauer cells. Endocrinology. 2013;154(1):471-82.
38. Paulus P, Holfeld J, Urbschat A, Mutlak H, Ockelmann PA, Tacke S, Zacharowski K, Reissig C, Stay D, Scheller B. Prednisolone as preservation additive prevents from ischemia reperfusion injury in a rat model of orthotopic lung transplantation. PLoS One. 2013;8(8):e73298.
39. Sekerkova A, Krepsova E, Brabcova E, Slatinska J, Viklicky O, Lanska V, Striz I. CD14 + CD16+ and CD14 + CD163+ monocyte subpopulations in kidney allograft transplantation. BMC Immunol. 2014;15:4.
40. Guo ZS, Parimi V, O'Malley ME, Thirunavukarasu P, Sathaiah M, Austin F, Bartlett DL. The combination of immunosuppression and carrier cells significantly enhances the efficacy of oncolytic poxvirus in the pre-immunized host. Gene Ther. 2010;17(12):1465-75.
41. Lapuc I, Bolkun L, Eljaszewicz A, Rusak M, Luksza E, Singh P, Miklasz P, Piszcz J, Ptaszynska-Kopczynska K, Jasiewicz M et al. Circulating classical CD14++CD16- monocytes predict shorter time to initial treatment in chronic lymphocytic leukemia patients: differential effects of immune chemotherapy on monocyte-related membrane and soluble forms of CD163. Oncol Rep. 2015;34(3):1269-78.
42. Hagiwara E, Gourley MF, Lee S, Klinman DK. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood. Arthritis Rheum. 1996;39(3):379-85.
43. Zizzo G, Hilliard BA, Monestier M, Cohen PL. Efficient clearance of early apoptotic cells by human macrophages requires M2c polarization and MerTK induction. J Immunol. 2012;189(7):3508-20.
44. Hill GS, Delahousse M, Nochy D, Remy P, Mignon F, Mery JP, Bariety J. Predictive power of the second renal biopsy in lupus nephritis: significance of macrophages. Kidney Int. 2001;59(1):304-16.
45. Gutierrez E, Egido J, Rubio-Navarro A, Buendia I, Blanco Colio LM, Toldos O, Manzarbeitia F, de Lorenzo A, Sanchez R, Ortiz A et al. Oxidative stress, macrophage infiltration and CD163 expression are determinants of long-term renal outcome in macrohematuria-induced acute kidney injury of IgA nephropathy. Nephron Clin Pract. 2012;121(1-2):c42-53.
46. Guillen-Gomez E, Guirado L, Belmonte X, Maderuelo A, Santin S, Juarez C, Ars E, Facundo C, Ballarin JA, Vidal S et al. Monocyte implication in renal allograft dysfunction. Clin Exp Immunol. 2014;175(2):323-31.
47. Nakayama W, Jinnin M, Makino K, Kajihara I, Makino T, Fukushima S, Sakai K, Inoue Y, Ihn H. CD163 expression is increased in the involved skin and sera of patients with systemic lupus erythematosus. Eur J Dermatol. 2012;22(4):512-7.
48. Wang J, Jiang ZP, Su N, Fan JJ, Ruan YP, Peng WX, Li YF, Yu XQ. The role of peritoneal alternatively activated macrophages in the process of peritoneal fibrosis related to peritoneal dialysis. Int J Mol Sci. 2013;14(5):10369-82.
49. Evans BJ, Haskard DO, Sempowksi G, Landis RC. Evolution of the Macrophage CD163 Phenotype and Cytokine Profiles in a Human Model of Resolving Inflammation. Int J Inflamm. 2013;2013:780502.
50. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger Jr TA, Jansen-McWilliams L, D'Agostino RB, Kuller LH. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol. 1997;145(5):408-15.
51. Ryan MJ. The pathophysiology of hypertension in systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol. 2009;296(4):R1258-67.
52. Chan CT, Moore JP, Budzyn K, Guida E, Diep H, Vinh A, Jones ES, Widdop RE, Armitage JA, Sakkal S et al. Reversal of vascular macrophage accumulation and hypertension by a CCR2 antagonist in deoxycorticosterone/salt-treated mice. Hypertension. 2012;60(5):1207-12.
53. Kriska T, Cepura C, Magier D, Siangjong L, Gauthier KM, Campbell WB. Mice lacking macrophage 12/15-lipoxygenase are resistant to experimental hypertension. Am J Physiol Heart Circ Physiol. 2012;302(11):H2428-38.
54. Hashimoto-Kataoka T, Hosen N, Sonobe T, Arita Y, Yasui T, Masaki T, Minami M, Inagaki T, Miyagawa S, Sawa Y et al. Interleukin-6/interleukin-21 signaling axis is critical in the pathogenesis of pulmonary arterial hypertension. Proc Natl Acad Sci U S A. 2015;112(20):E2677-86.
55. Qian L, Li X, Fang R, Wang Z, Xu Y, Zhang H, Bai H, Yang Q, Zhu X, Ben J et al. Class A scavenger receptor deficiency augments angiotensin II-induced vascular remodeling. Biochem Pharmacol. 2014;90(3):254-64.
56. Kinsey GR, Sharma R, Huang L, Li L, Vergis AL, Ye H, Ju ST, Okusa MD. Regulatory T cells suppress innate immunity in kidney ischemia-reperfusion injury. J Am Soc Nephrol. 2009;20(8):1744-53.
57. Hu K, Zhou H, Zheng G, Wang G, Fu Y, Jiang Y. Imbalance of different types of CD4(+)Foxp3(+) T cells in renal transplant recipients. Immunol Invest. 2014;43(8):838-50.