Increased plasma levels of the soluble Mer tyrosine kinase receptor in systemic lupus erythematosus relate to disease activity and nephritis

Arthritis Research and Therapy

Volumn 13, Issue 2, 2011, Pages

  Wu, Jun ^a,b   Ekman, Carl ^a   Jönsen, Andreas ^a   Sturfelt, Gunnar ^a   Bengtsson, Anders A ^a   Gottsäter, Anders ^a   Lindblad, Bengt ^a   Lindqvist, Elisabet ^a   Saxne, Tore ^a   Dahlbäck, Björn ^a  

^a LUND UNIVERSITY   (Sweden)

^b PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C1Q; DNA ANTIBODY; TYROSINE KINASE RECEPTOR; BIOLOGICAL MARKER; MERTK PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN TYROSINE KINASE; TYRO3 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMAN; LIMB ISCHEMIA; MAJOR CLINICAL STUDY; MALE; NEPHRITIS; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; ADULT; BLOOD; ISCHEMIA; LUPUS ERYTHEMATOSUS NEPHRITIS;

ADULT; ARTHRITIS, RHEUMATOID; BIOLOGICAL MARKERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; ISCHEMIA; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MALE; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES;

EID: 79955100531     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3316     Document Type: Article

References (44)

1. Linger RM, Keating AK, Earp HS, Graham DK. TAM receptor tyrosine kinases: biologic functions, signaling, and potential therapeutic targeting in human cancer. Adv Cancer Res 2008, 100:35-83.
2. Lemke G, Rothlin CV. Immunobiology of the TAM receptors. Nat Rev Immunol 2008, 8:327-336. 10.1038/nri2303, 2856445, 18421305.
3. Hafizi S, Dahlback B. Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 2006, 273:5231-5244. 10.1111/j.1742-4658.2006.05529.x, 17064312.
4. Hafizi S, Dahlback B. Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 2006, 17:295-304. 10.1016/j.cytogfr.2006.04.004, 16737840.
5. Shao WH, Zhen Y, Eisenberg RA, Cohen PL. The Mer receptor tyrosine kinase is expressed on discrete macrophage subpopulations and mainly uses Gas6 as its ligand for uptake of apoptotic cells. Clin Immunol 2009, 133:138-144. 10.1016/j.clim.2009.06.002, 2746995, 19631584.
6. Nandrot EF, Dufour EM. Mertk in daily retinal phagocytosis: a history in the making. Adv Exp Med Biol 2010, 664:133-140. 10.1007/978-1-4419-1399-9_16, 20238011.
7. Rothlin CV, Ghosh S, Zuniga EI, Oldstone MB, Lemke G. TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 2007, 131:1124-1136. 10.1016/j.cell.2007.10.034, 18083102.
8. Gregory CD, Devitt A. The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically?. Immunology 2004, 113:1-14. 10.1111/j.1365-2567.2004.01959.x, 1782607, 15569176.
9. Cohen PL, Caricchio R, Abraham V, Camenisch TD, Jennette JC, Roubey RA, Earp HS, Matsushima G, Reap EA. Delayed apoptotic cell clearance and lupus-like autoimmunity in mice lacking the c-mer membrane tyrosine kinase. J Exp Med 2002, 196:135-140. 10.1084/jem.20012094, 2194017, 12093878.
10. Sather S, Kenyon KD, Lefkowitz JB, Liang X, Varnum BC, Henson PM, Graham DK. A soluble form of the Mer receptor tyrosine kinase inhibits macrophage clearance of apoptotic cells and platelet aggregation. Blood 2007, 109:1026-1033. 1785151, 17047157.
11. Ekman C, Stenhoff J, Dahlback B. Gas6 is complexed to the soluble tyrosine kinase receptor Axl in human blood. J Thromb Haemost 2010, 8:838-844. 10.1111/j.1538-7836.2010.03752.x, 20088931.
12. Ekman C, Linder A, Akesson P, Dahlback B. Plasma concentrations of Gas6 (growth arrest specific protein 6) and its soluble tyrosine kinase receptor sAxl in sepsis and systemic inflammatory response syndromes. Crit Care 2010, 14:R158. 10.1186/cc9233, 2945142, 20731857.
13. Ekman C, Jonsen A, Sturfelt G, Bengtsson AA, Dahlbäck B. Plasma concentrations of Gas6 and sAxl correlate with disease activity in systemic lupus erythematosus. Rheumatology (Oxford) 2011, 50:1064-9.
14. Katsiari CG, Liossis SN, Sfikakis PP. The pathophysiologic role of monocytes and macrophages in systemic lupus erythematosus: a reappraisal. Semin Arthritis Rheum 2010, 39:491-503. 10.1016/j.semarthrit.2008.11.002, 19147182.
15. Brown KD, Claudio E, Siebenlist U. The roles of the classical and alternative nuclear factor-kappaB pathways: potential implications for autoimmunity and rheumatoid arthritis. Arthritis Res Ther 2008, 10:212. 10.1186/ar2457, 2575629, 18771589.
16. Minar E. Critical limb ischaemia. Hamostaseologie 2009, 29:102-109.
17. Novo S, Coppola G, Milio G. Critical limb ischemia: definition and natural history. Curr Drug Targets Cardiovasc Haematol Disord 2004, 4:219-225. 10.2174/1568006043335989, 15379613.
18. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982, 25:1271-1277. 10.1002/art.1780251101, 7138600.
19. Lindqvist E, Saxne T, Geborek P, Eberhardt K. Ten year outcome in a cohort of patients with early rheumatoid arthritis: health status, disease process, and damage. Ann Rheum Dis 2002, 61:1055-1059. 10.1136/ard.61.12.1055, 1753974, 12429534.
20. Lindqvist E, Jonsson K, Saxne T, Eberhardt K. Course of radiographic damage over 10 years in a cohort with early rheumatoid arthritis. Ann Rheum Dis 2003, 62:611-616. 10.1136/ard.62.7.611, 1754610, 12810421.
21. Norgren L, Hiatt WR, Dormandy JA, Nehler MR, Harris KA, Fowkes FG. Inter-Society Consensus for the Management of Peripheral Arterial Disease (TASC II). J Vasc Surg 2007, 45:S5-S67. 10.1016/j.jvs.2006.12.037, 17223489.
22. Barani J, Nilsson JA, Mattiasson I, Lindblad B, Gottsater A. Inflammatory mediators are associated with 1-year mortality in critical limb ischemia. J Vasc Surg 2005, 42:75-80. 10.1016/j.jvs.2005.03.025, 16012455.
23. Nagata S, Hanayama R, Kawane K. Autoimmunity and the clearance of dead cells. Cell 2010, 140:619-630. 10.1016/j.cell.2010.02.014, 20211132.
24. Baumann I, Kolowos W, Voll RE, Manger B, Gaipl U, Neuhuber WL, Kirchner T, Kalden JR, Herrmann M. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum 2002, 46:191-201. 10.1002/1529-0131(200201)46:1<191::AID-ART10027>3.0.CO;2-K, 11817590.
25. Munoz LE, Lauber K, Schiller M, Manfredi AA, Herrmann M. The role of defective clearance of apoptotic cells in systemic autoimmunity. Nat Rev Rheumatol 2010, 6:280-289. 10.1038/nrrheum.2010.46, 20431553.
26. Munoz LE, Gaipl US, Franz S, Sheriff A, Voll RE, Kalden JR, Herrmann M. SLE--a disease of clearance deficiency?. Rheumatology (Oxford) 2005, 44:1101-1107.
27. Herrmann M, Voll RE, Zoller OM, Hagenhofer M, Ponner BB, Kalden JR. Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum 1998, 41:1241-1250. 10.1002/1529-0131(199807)41:7<1241::AID-ART15>3.0.CO;2-H, 9663482.
28. Scott RS, McMahon EJ, Pop SM, Reap EA, Caricchio R, Cohen PL, Earp HS, Matsushima GK. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 2001, 411:207-211. 10.1038/35075603, 11346799.
29. Seitz HM, Camenisch TD, Lemke G, Earp HS, Matsushima GK. Macrophages and dendritic cells use different Axl/Mertk/Tyro3 receptors in clearance of apoptotic cells. J Immunol 2007, 178:5635-5642.
30. Wu Y, Singh S, Georgescu MM, Birge RB. A role for Mer tyrosine kinase in alphavbeta5 integrin-mediated phagocytosis of apoptotic cells. J Cell Sci 2005, 118:539-553. 10.1242/jcs.01632, 15673687.
31. Todt JC, Hu B, Curtis JL. The scavenger receptor SR-A I/II (CD204) signals via the receptor tyrosine kinase Mertk during apoptotic cell uptake by murine macrophages. J Leukoc Biol 2008, 84:510-518. 10.1189/jlb.0307135, 2718803, 18511575.
32. Alciato F, Sainaghi PP, Sola D, Castello L, Avanzi GC. TNF-alpha, IL-6, and IL-1 expression is inhibited by GAS6 in monocytes/macrophages. J Leukoc Biol 2010, 87:869-875. 10.1189/jlb.0909610, 20103767.
33. Shao WH, Eisenberg RA, Cohen PL. The Mer receptor tyrosine kinase is required for the loss of B cell tolerance in the chronic graft-versus-host disease model of systemic lupus erythematosus. J Immunol 2008, 180:7728-7735.
34. Wallet MA, Sen P, Flores RR, Wang Y, Yi Z, Huang Y, Mathews CE, Earp HS, Matsushima G, Wang B, Tisch R. MerTK is required for apoptotic cell-induced T cell tolerance. J Exp Med 2008, 205:219-232. 10.1084/jem.20062293, 2234377, 18195070.
35. Wallet MA, Flores RR, Wang Y, Yi Z, Kroger CJ, Mathews CE, Earp HS, Matsushima G, Wang B, Tisch R. MerTK regulates thymic selection of autoreactive T cells. Proc Natl Acad Sci USA 2009, 106:4810-4815. 10.1073/pnas.0900683106, 2660755, 19251650.
36. Banchereau J, Pascual V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006, 25:383-392. 10.1016/j.immuni.2006.08.010, 16979570.
37. Pascual V, Farkas L, Banchereau J. Systemic lupus erythematosus: all roads lead to type I interferons. Curr Opin Immunol 2006, 18:676-682. 10.1016/j.coi.2006.09.014, 17011763.
38. A-Gonzalez N, Bensinger SJ, Hong C, Beceiro S, Bradley MN, Zelcer N, Deniz J, Ramirez C, Diaz M, Gallardo G, De Galarreta CR, Salazar J, Lopez F, Edwards P, Parks J, Andujar M, Tontonoz P, Castrillo A. Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 2009, 31:245-258. 10.1016/j.immuni.2009.06.018, 2791787, 19646905.
39. Chaussabel D, Quinn C, Shen J, Patel P, Glaser C, Baldwin N, Stichweh D, Blankenship D, Li L, Munagala I, Bennett L, Allantaz F, Mejias A, Ardura M, Kaizer E, Monnet L, Allman W, Randall H, Johnson D, Lanier A, Punaro M, Wittkowski KM, White P, Fay J, Klintmalm G, Ramilo O, Palucka AK, Banchereau J, Pascual V. A modular analysis framework for blood genomics studies: application to systemic lupus erythematosus. Immunity 2008, 29:150-164. 10.1016/j.immuni.2008.05.012, 2727981, 18631455.
40. Prasad D, Rothlin CV, Burrola P, Burstyn-Cohen T, Lu Q, Garcia FP, Lemke G. TAM receptor function in the retinal pigment epithelium. Mol Cell Neurosci 2006, 33:96-108. 10.1016/j.mcn.2006.06.011, 16901715.
41. Brea-Fernandez AJ, Pomares E, Brion MJ, Marfany G, Blanco MJ, Sanchez-Salorio M, Gonzalez-Duarte R, Carracedo A. Novel splice donor site mutation in MERTK gene associated with retinitis pigmentosa. Br J Ophthalmol 2008, 92:1419-1423. 10.1136/bjo.2008.139204, 18815424.
42. Ekman C, Gottsater A, Lindblad B, Dahlback B. Plasma concentrations of Gas6 and soluble Axl correlate with disease and predict mortality in patients with critical limb ischemia. Clin Biochem 2010, 43:873-876. 10.1016/j.clinbiochem.2010.04.006, 20417630.
43. Castellano G, Trouw LA, Fiore N, Daha MR, Schena FP, van Kooten C. Infiltrating dendritic cells contribute to local synthesis of C1q in murine and human lupus nephritis. Mol Immunol 2010, 47:2129-2137. 10.1016/j.molimm.2010.02.006, 20417969.
44. Alzawawy A, Zohary M, Ablordiny M, Eldalie M. Estimation of monocyte-chemoattractantprotein-1 (Mcp-1) level in patients with lupus nephritis. Int J Rheum Dis 2009, 12:311-318. 10.1111/j.1756-185X.2009.01429.x, 20374368.