Differential expression of functional Fc-receptors and additional immune complex receptors on mouse kidney cells

Molecular Immunology

Volumn 56, Issue 4, 2013, Pages 369-379

  Suwanichkul, Adisak ^a   Wenderfer, Scott E ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Endothelial cell; Fc receptor; Glomerulonephritis; Immune complex; Lupus; Mouse model

Indexed keywords

BLOCKING ANTIBODY; ENDOTHELIN 1; FC RECEPTOR; FC RECEPTOR IIB; GRANULOCYTE COLONY STIMULATING FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IMMUNOGLOBULIN G; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 2; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; THROMBOCYTE FACTOR 4; TRANSFERRIN RECEPTOR; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; PROTEIN BINDING; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; AUTOIMMUNE DISEASE; CELL INFILTRATION; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; ENDOTHELIUM CELL; GLOMERULUS; IMMUNOHISTOCHEMISTRY; KIDNEY CELL; KIDNEY INJURY; MACROPHAGE; MESANGIUM CELL; MOUSE; NONHUMAN; PHAGOCYTE; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENAL ENDOTHELIAL CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOLOGY; KIDNEY; METABOLISM;

ANIMALS; ANTIBODIES, BLOCKING; CELLS, CULTURED; ENDOTHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOGLOBULIN G; KIDNEY; MESANGIAL CELLS; MICE; MICE, INBRED C57BL; PODOCYTES; PROTEIN BINDING; RECEPTORS, FC; RECEPTORS, IGG; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTOME;

EID: 84881118246     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2013.05.219     Document Type: Article

References (91)

1. Aarli A., Matre R., Thunold S. IgG Fc receptors on epithelial cells of distal tubuli and on endothelial cells in human kidney. International Archives of Allergy and Applied Immunology 1991, 95:64-69.
2. Akilesh S., Huber T.B., Wu H., Wang G., Hartleben B., Kopp J.B., Miner J.H., Roopenian D.C., Unanue E.R., Shaw A.S. Podocytes use FcRn to clear IgG from the glomerular basement membrane. Proceedings of the National Academy of Science 2008, 105:967-972.
3. Alexander J.J., Wang Y., Chang A., Jacob A., Minto A.W., Karmegam M., Haas M., Quigg R.J. Mouse podocyte complement factor H: the functional analog to human complement receptor 1. Journal of the American Society of Nephrology 2007, 18:1157-1166.
4. Alpers C.E., Hudkins K.L., Pritzl P., Johnson R.J. Mechanisms of clearance of immune complexes from peritubular capillaries in the rat. The American Journal of Pathology 1991, 139:855-867.
5. Appay M.D., Kazatchkine M.D., Levi-Strauss M., Hinglais N., Bariety J. Expression of CR1 (CD35) mRNA in podocytes from adult and fetal human kidneys. Kidney International 1990, 38:289-293.
6. Bagheri N., Chintalacharuvu S.R., Emancipator S.N. Proinflammatory cytokines regulate Fc alphaR expression by human mesangial cells in vitro. Clinical and Experimental Immunology 1997, 107:404-409.
7. Barnes J., Camussi G., Tetta C., Venkatachalam M.A. Glomerular localization of platelet cationic proteins after immune complex-induced platelet activation. Laboratory Investigation; a Journal of Technical Methods and Pathology 1990, 63:755-761.
8. Briganti E.M., Dowling J., Finlay M., Hill P.A., Jones C.L., Kincaid-Smith P.S., Sinclair R., McNeil J.J., Atkins R.C. The incidence of biopsy-proven glomerulonephritis in Australia. Nephrology, Dialysis, Transplantation 2001, 16:1364-1367.
9. Brown H.J., Lock H.R., Wolfs T.G., Buurman W.A., Sacks S.H., Robson M.G. Toll-like receptor 4 ligation on intrinsic renal cells contributes to the induction of antibody-mediated glomerulonephritis via CXCL1 and CXCL2. Journal of the American Society of Nephrology 2007, 18:1732-1739.
10. Campbell I.K., Rich M.J., Bischof R.J., Dunn A.R., Grail D., Hamilton J.A. Protection from collagen-induced arthritis in GM-CSF-deficient mice. Journal of Immunology 1998, 161:3639-3644.
11. Chan R.W., Lai F.M., Li E.K., Tam L.S., Chow K.M., Li P.K., Szeto C.C. Messenger RNA expression of RANTES in the urinary sediment of patients with lupus nephritis. Nephrology 2006, 11:219-225.
12. Chen A., Wong S.S., Rifai A. Glomerular immune deposits in experimental IgA nephropathy. The American Journal of Pathology 1988, 130:216-222.
13. Chen W.S., Lin K.C., Chen C.H., Liao H.T., Wang H.P., Li W.Y., Lee H.T., Tsai C.Y., Chou C.T. Autoantibody and biopsy grading are associated with expression of ICAM-1, MMP-3, and TRAIL in salivary gland mononuclear cells of Chinese patients with Sjogren's syndrome. The Journal of Rheumatology 2009, 36:989-996.
14. Cines D.B., Lyss A.P., Reeber M., Bina M., DeHoratius R.J. Presence of complement-fixing anti-endothelial cell antibodies in systemic lupus erythematosus. The Journal of Clinical Investigation 1984, 73:611-625.
15. Devaraj S., Du Clos T.W., Jialal I. Binding and internalization of C-reactive protein by Fcgamma receptors on human aortic endothelial cells mediates biological effects. Arteriosclerosis, Thrombosis, and Vascular Biology 2005, 25:1359-1363.
16. Dhaun N., Lilitkarntakul P., Macintyre I.M., Muilwijk E., Johnston N.R., Kluth D.C., Webb D.J., Goddard J. Urinary endothelin-1 in chronic kidney disease and as a marker of disease activity in lupus nephritis. American Journal of Physiology 2009, 296:F1477-F1483.
17. Fujii H., Nakatani K., Arita N., Ito M.R., Terada M., Miyazaki T., Yoshida M., Ono M., Fujiwara T., Saiga K., Ota T., Ohtani H., Lockwood M., Sasaki T., Nose M. Internalization of antibodies by endothelial cells via fibronectin implicating a novel mechanism in lupus nephritis. Kidney International 2003, 64:1662-1670.
18. Furuichi K., Wada T., Sakai N., Iwata Y., Yoshimoto K., Shimizu M., Kobayashi K., Takasawa K., Kida H., Takeda S.I., Mukaida N., Matsushima K., Yokoyama H. Distinct expression of CCR1 and CCR5 in glomerular and interstitial lesions of human glomerular diseases. American Journal of Nephrology 2000, 20:291-299.
19. Gauthier V.J., Mannik M., Striker G.E. Effect of cationized antibodies in performed immune complexes on deposition and persistence in renal glomeruli. The Journal of Experimental Medicine 1982, 156:766-777.
20. Gomez-Guerrero C., Lopez-Armada M.J., Gonzalez E., Egido J. Soluble IgA and IgG aggregates are catabolized by cultured rat mesangial cells and induce production of TNF-alpha and IL-6, and proliferation. Journal of Immunology 1994, 153:5247-5255.
21. Greenwood J., Heasman S.J., Alvarez J.I., Prat A., Lyck R., Engelhardt B. Review: leucocyte-endothelial cell crosstalk at the blood-brain barrier: a prerequisite for successful immune cell entry to the brain. Neuropathology and Applied Neurobiology 2011, 37:24-39.
22. Haymann J.P., Delarue F., Baud L., Sraer J.D. Aggregated IgG bind to glomerular epithelial cells to stimulate urokinase release through an endocytosis-independent process. Nephron Experimental Nephrology 2004, 98:e13-e21.
23. Haymann J.P., Levraud J.P., Bouet S., Kappes V., Hagege J., Nguyen G., Xu Y., Rondeau E., Sraer J.D. Characterization and localization of the neonatal Fc receptor in adult human kidney. Journal of the American Society of Nephrology 2000, 11:632-639.
24. Hellmich B., Schnabel A., Gross W.L. Treatment of severe neutropenia due to Felty's syndrome or systemic lupus erythematosus with granulocyte colony-stimulating factor. Seminars in Arthritis and Rheumatism 1999, 29:82-99.
25. Herman W.H., Emancipator S.N., Rhoten R.L., Simonson M.S. Vascular and glomerular expression of endothelin-1 in normal human kidney. The American Journal of Physiology 1998, 275:F8-F17.
26. Hickey M.J., Kubes P. Intravascular immunity: the host-pathogen encounter in blood vessels. Nature Reviews 2009, 9:364-375.
27. Hiraoka S., Furumoto Y., Koseki H., Takagaki Y., Taniguchi M., Okumura K., Ra C. Fc receptor beta subunit is required for full activation of mast cells through Fc receptor engagement. International Immunology 1999, 11:199-207.
28. Hunt J.S., Jackson A.E., Day W.A., McGiven A.R. Mouse glomerular culture. British Journal of Experimental Pathology 1981, 62:52-58.
29. Jennette J.C., Olson J.L., Schwartz M.M., Silva F.G. Heptinstall's Pathology of the Kidney 2006, Lippincott Williams & Wilkins, Market Street Philadelphia, PA. 6th ed.
30. Julkunen H., Saijonmaa O., Gronhagen-Riska C., Teppo A.M., Fyhrquist F. Raised plasma concentrations of endothelin-1 in systemic lupus erythematosus. Annals of the Rheumatic Diseases 1991, 50:526-527.
31. Kazatchkine M.D., Fearon D.T., Appay M.D., Mandet C., Bariety J. Immunohistochemical study of the human glomerular C3b receptor in normal kidney and in seventy-five cases of renal diseases: loss of C3b receptor antigen in focal hyalinosis and in proliferative nephritis of systemic lupus erythematosus. The Journal of Clinical Investigation 1982, 69:900-912.
32. Kowalska M.A., Rauova L., Poncz M. Role of the platelet chemokine platelet factor 4 (PF4) in hemostasis and thrombosis. Thrombosis Research 2010, 125:292-296.
33. Kristoffersen E.K., Ulvestad E., Bjorge L., Aarli A., Matre R. Fc gamma-receptor activity of placental annexin II. Scandinavian Journal of Immunology 1994, 40:237-242.
34. Kurosaki T., Gander I., Wirthmueller U., Ravetch J.V. The beta subunit of the Fc epsilon RI is associated with the Fc gamma RIII on mast cells. The Journal of Experimental Medicine 1992, 175:447-451.
35. Lloyd C.M., Minto A.W., Dorf M.E., Proudfoot A., Wells T.N., Salant D.J., Gutierrez-Ramos J.C. RANTES and MCP-1 play an important role in the inflammatory phase of crescentic nephritis, but only MCP-1 is involved in crescent formation and interstitial fibrosis. Journal of Experimental Medicine 1997, 185:1371-1380.
36. Luo Y., Lloyd C., Gutierrez-Ramos J.C., Dorf M.E. Chemokine amplification in mesangial cells. Journal of Immunology 1999, 163:3985-3992.
37. Matre R., Tonder O., Wesenberg F. Human renal glomeruli possess no Fc gamma receptors. Clinical Immunology and Immunopathology 1980, 17:157-162.
38. Mauer S.M., Fish A.J., Blau E.B., Michael A.F. The glomerular mesangium I. Kinetic studies of macromolecular uptake in normal and nephrotic rats. The Journal of Clinical Investigation 1972, 51:1092-1101.
39. McCluskey R.T., Benacerraf B., Potter J.L., Miller F. The pathologic effects of intravenously administered soluble antigen-antibody complexes I. Passive serum sickness in mice. The Journal of Experimental Medicine 1960, 111:181-194.
40. Moore K.J., Wada T., Barbee S.D., Kelley V.R. Gene transfer of RANTES elicits autoimmune renal injury in MRL-Fas(lpr) mice. Kidney International 1998, 53:1631-1641.
41. Morcos M., Hansch G.M., Schonermark M., Ellwanger S., Harle M., Heckl-Ostreicher B. Human glomerular mesangial cells express CD16 and may be stimulated via this receptor. Kidney International 1994, 46:1627-1634.
42. Moura I.C., Centelles M.N., Arcos-Fajardo M., Malheiros D.M., Collawn J.F., Cooper M.D., Monteiro R.C. Identification of the transferrin receptor as a novel IgA1 receptor and its enhanced expression on mesangial cells in IgA nephropathy. The Journal of Experimental Medicine 2001, 194:417-425.
43. Nakamura T., Ebihara I., Fukui M., Osada S., Tomino Y., Masaki T., Goto K., Furuichi Y., Koide H. Renal expression of mRNAs for endothelin-1, endothelin-3 and endothelin receptors in NZB/W F1 mice. Renal Physiology and Biochemistry 1993, 16:233-243.
44. Nakamura T., Ebihara I., Tomino Y., Koide H. Effect of a specific endothelin A receptor antagonist on murine lupus nephritis. Kidney International 1995, 47:481-489.
45. Nguyen V., Cudrici C., Zernetkina V., Niculescu F., Rus H., Drachenberg C., Rus V. TRAIL, DR4 and DR5 are upregulated in kidneys from patients with lupus nephritis and exert proliferative and proinflammatory effects. Clinical Immunology 2009, 132:32-42.
46. Nishimura M., Takanashi M., Okazaki H., Satake M., Nakajima K. Role of CD7 expressed in lung microvascular endothelial cells as Fc receptor for immunoglobulin M. Endothelium 2006, 13:287-292.
47. Pan L.F., Kreisle R.A., Shi Y.D. Detection of Fcgamma receptors on human endothelial cells stimulated with cytokines TNF-alpha and IFN-gamma. Clinical and Experimental Immunology 1998, 112:533-538.
48. Perez de Lema G., Maier H., Nieto E., Vielhauer V., Luckow B., Mampaso F., Schlondorff D. Chemokine expression precedes inflammatory cell infiltration and chemokine receptor and cytokine expression during the initiation of murine lupus nephritis. Journal of the American Society of Nephrology 2001, 12:1369-1382.
49. Pettersson E.E., Bhan A.K., Schneeberger E.E., Collins A.B., Colvin R.B., McCluskey R.T. Glomerular C3 receptors in human renal disease. Kidney International 1978, 13:245-252.
50. Quigg R.J., Sneed 3rd A.E. Molecular characterization of rat glomerular epithelial cell complement receptors. Journal of the American Society of Nephrology 1994, 4:1912-1919.
51. Radeke H.H., Gessner J.E., Uciechowski P., Magert H.J., Schmidt R.E., Resch K. Intrinsic human glomerular mesangial cells can express receptors for IgG complexes (hFc gamma RIII-A) and the associated Fc epsilon RI gamma-chain. Journal of Immunology 1994, 153:1281-1292.
52. Radeke H.H., Janssen-Graalfs I., Sowa E.N., Chouchakova N., Skokowa J., Loscher F., Schmidt R.E., Heeringa P., Gessner J.E. Opposite regulation of type II and III receptors for immunoglobulin G in mouse glomerular mesangial cells and in the induction of anti-glomerular basement membrane (GBM) nephritis. The Journal of Biological Chemistry 2002, 277:27535-27544.
53. Rajagopalan S., Somers E.C., Brook R.D., Kehrer C., Pfenninger D., Lewis E., Chakrabarti A., Richardson B.C., Shelden E., McCune W.J., Kaplan M.J. Endothelial cell apoptosis in systemic lupus erythematosus. Blood 2004, 103:3677-3683.
54. Ravetch J.V., Bolland S. IgG Fc receptors. Annual Review of Immunology 2001, 19:275-290.
55. Remuzzi G., Benigni A. Endothelins in the control of cardiovascular and renal function. Lancet 1993, 342:589-593.
56. Rops A.L., van der Vlag J., Jacobs C.W., Dijkman H.B., Lensen J.F., Wijnhoven T.J., Van Den Heuvel L.P., van Kuppevelt T.H., Berden J.H. Isolation and characterization of conditionally immortalized mouse glomerular endothelial cell lines. Kidney International 2004, 66:2193-2201.
57. Ryan U.S., Schultz D.R., Ruan J.W. Fc and C3b receptors on pulmonary endothelial cells. Science 1981, 214:557-558.
58. Santiago A., Satriano J., DeCandido S., Holthofer H., Schreiber R., Unkeless J., Schlondorff D. A specific Fc gamma receptor on cultured rat mesangial cells. Journal of Immunology 1989, 143:2575-2582.
59. Sarav M., Wang Y., Hack B.K., Chang A., Jensen M., Bao L., Quigg R.J. Renal FcRn reclaims albumin but facilitates elimination of IgG. Journal of the American Society of Nephrology 2009, 20:1941-1952.
60. Schadde E., Kretzler M., Banas B., Luckow B., Assmann K., Schlondorff D. Expression of chemokines and their receptors in nephrotoxic serum nephritis. Nephrology, Dialysis, Transplantation 2000, 15:1046-1053.
61. Schreiner G.F., Unanue E.R. Origin of the rat mesangial phagocyte and its expression of the leukocyte common antigen. Laboratory Investigation; a Journal of Technical Methods and Pathology 1984, 51:515-523.
62. Sedor J.R., Carey S.W., Emancipator S.N. Immune complexes bind to cultured rat glomerular mesangial cells to stimulate superoxide release. Evidence for an Fc receptor. Journal of Immunology 1987, 138:3751-3757.
63. Shankland S.J., Pippin J.W., Reiser J., Mundel P. Podocytes in culture: past, present, and future. Kidney International 2007, 72:26-36.
64. Singhal P.C., Santiago A., Satriano J., Hays R.M., Schlondorff D. Effects of vasoactive agents on uptake of immunoglobulin G complexes by mesangial cells. The American Journal of Physiology 1990, 258:F589-F596.
65. Soos T.J., Sims T.N., Barisoni L., Lin K., Littman D.R., Dustin M.L., Nelson P.J. CX3CR1+ interstitial dendritic cells form a contiguous network throughout the entire kidney. Kidney International 2006, 70:591-596.
66. Striker G.E., Striker L.J. Glomerular cell culture. Laboratory Investigation 1985, 53:122-131.
67. Sugihara A., Adachi Y., Inaba M., Hisha H., Sugiura K., Miyashima S., Amoh Y., Taketani S., Oyaizu H., Ikebukuro K., Kawamura M., Genba H., Horio T., Ikehara S. Age-dependent abnormalities of hematopoietic stem cells in (NZW×BXSB)F1 mice. Stem Cells 1999, 17:357-365.
68. Suzuki E., Karam E., Williams S., Watson D.K., Gilkeson G., Zhang X.K. Fli-1 transcription factor affects glomerulonephritis development by regulating expression of monocyte chemoattractant protein-1 in endothelial cells in the kidney. Clinical Immunology 2012, 145:201-208.
69. Swaminathan S., Leung N., Lager D.J., Melton L.J., Bergstralh E.J., Rohlinger A., Fervenza F.C. Changing incidence of glomerular disease in Olmsted County, Minnesota: a 30-year renal biopsy study. Clinical Journal of the American Society of Nephrology 2006, 1:483-487.
70. Szczypka M.S., Westover A.J., Clouthier S.G., Ferrara J.L., Humes H.D. Rare incorporation of bone marrow-derived cells into kidney after folic acid-induced injury. Stem Cells (Dayton, Ohio) 2005, 23:44-54.
71. Takemoto M., Asker N., Gerhardt H., Lundkvist A., Johansson B.R., Saito Y., Betsholtz C. A new method for large scale isolation of kidney glomeruli from mice. The American Journal of Pathology 2002, 161:799-805.
72. Tannenbaum S.H., Finko R., Cines D.B. Antibody and immune complexes induce tissue factor production by human endothelial cells. Journal of Immunology 1986, 137:1532-1537.
73. Thacker S.G., Duquaine D., Park J., Kaplan M.J. Lupus-prone New Zealand Black/New Zealand White F1 mice display endothelial dysfunction and abnormal phenotype and function of endothelial progenitor cells. Lupus 2010, 19:288-299.
74. Timoshanko J.R., Kitching A.R., Semple T.J., Holdsworth S.R., Tipping P.G. GM-CSF expression by both renal parenchymal and immune cells mediates murine crescentic glomerulonephritis. Journal of the American Society of Nephrology 2005, 16:2646-2656.
75. Topham P.S., Csizmadia V., Soler D., Hines D., Gerard C.J., Salant D.J., Hancock W.W. Lack of chemokine receptor CCR1 enhances Th1 responses and glomerular injury during nephrotoxic nephritis. Journal of Clinical Investigation 1999, 104:1549-1557.
76. U.S.Renal Data System Incidence of Reported ESRD 2009, National Institutes of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD.
77. Uciechowski P., Schwarz M., Gessner J.E., Schmidt R.E., Resch K., Radeke H.H. IFN-gamma induces the high-affinity Fc receptor I for IgG (CD64) on human glomerular mesangial cells. European Journal of Immunology 1998, 28:2928-2935.
78. Van Den Dobbelsteen M.E., van der Woude F.J., Schroeijers W.E., Klar-Mohamad N., van Es L.A., Daha M.R. Both IgG- and C1q-receptors play a role in the enhanced binding of IgG complexes to human mesangial cells. Journal of the American Society of Nephrology 1996, 7:573-581.
79. Venegas-Pont M., Sartori-Valinotti J.C., Maric C., Racusen L.C., Glover P.H., McLemore G.R., Jones A.V., Reckelhoff J.F., Ryan M.J. Rosiglitazone decreases blood pressure and renal injury in a female mouse model of systemic lupus erythematosus. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2009, 296:R1282-R1289.
80. Vieten G., Hadam M.R., De Boer H., Olp A., Fricke M., Hartung K. Expanded macrophage precursor populations in BXSB mice: possible reason for the increasing monocytosis in male mice. Clinical Immunology and Immunopathology 1992, 65:212-218.
81. Villar M., Garcia-Bragado F., Joven J., Biosca M., Antolin M., Rodrigo M.J., Schwartz S. Cryoglobulinemia and fibronectin. Acta Haematologica 1985, 74:161-163.
82. Willeke P., Schluter B., Schotte H., Erren M., Mickholz E., Domschke W., Gaubitz M. Increased frequency of GM-CSF secreting PBMC in patients with active systemic lupus erythematosus can be reduced by immunoadsorption. Lupus 2004, 13:257-262.
83. Wilson T.J., Fuchs A., Colonna M. Cutting edge: human FcRL4 and FcRL5 are receptors for IgA and IgG. Journal of Immunology 2012, 188:4741-4745.
84. Wirta O., Mustonen J., Helin H., Pasternack A. Incidence of biopsy-proven glomerulonephritis. Nephrology, Dialysis, Transplantation 2007, 23:193-200.
85. Xie C., Zhou X.J., Liu X., Mohan C. Enhanced susceptibility to end-organ disease in the lupus-facilitating NZW mouse strain. Arthritis and Rheumatism 2003, 48:1080-1092.
86. Yoshio T., Masuyama J., Mimori A., Takeda A., Minota S., Kano S. Endothelin-1 release from cultured endothelial cells induced by sera from patients with systemic lupus erythematosus. Annals of the Rheumatic Diseases 1995, 54:361-365.
87. Yung S., Cheung K.F., Zhang Q., Chan T.M. Anti-dsDNA antibodies bind to mesangial annexin II in lupus nephritis. Journal of the American Society of Nephrology 2010, 11:1912-1927.
88. Zai-Xing Y., Yan L., Hao W., Ye Z., Chang L., Ren-Qian Z. Preliminary clinical measurement of the expression of TNF-related apoptosis inducing ligand in patients with ankylosing spondylitis. Journal of Clinical Laboratory Analysis 2008, 22:138-145.
89. Zauli G., Secchiero P. The role of the TRAIL/TRAIL receptors system in hematopoiesis and endothelial cell biology. Cytokine and Growth Factor Reviews 2006, 17:245-257.
90. Zavala F., Masson A., Hadaya K., Ezine S., Schneider E., Babin O., Bach J.F. G-CSF treatment of lupus autoimmune disease in MRL-lpr/lpr mice. Journal of Immunology 1999, 163:5125-5132.
91. Zhou L., Ida T., Marumo F. Role of thromboxane A2, endothelin-1 and endothelin-3 in rat nephrotoxic serum nephritis. The Tohoku Journal of Experimental Medicine 1996, 178:357-369.