The complexity of the BAFF TNF-family members: Implications for autoimmunity

Journal of Autoimmunity

Volumn 39, Issue 3, 2012, Pages 189-198

  Lahiri, Ayan ^a   Pochard, Pierre ^a   Le Pottier, Laëtitia ^a   Tobón, Gabriel J ^a   Bendaoud, Boutahar ^a   Youinou, Pierre ^a   Pers, Jacques Olivier ^a  

^a Universite de Brest   (France)

Author keywords

APRIL; Autoimmune diseases; BAFF; SNPs; TWE PRIL; TWEAK; Variants

Indexed keywords

APRIL PROTEIN; B CELL ACTIVATING FACTOR; MEMBRANE PROTEIN; PROTEIN TWEAK; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE; BAFF GENE; CELL GROWTH; CELL SURVIVAL; CHROMOSOME 8; DISEASE PREDISPOSITION; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXON; GENE; GENE EXPRESSION; GENE LOCATION; GENE MAPPING; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; AUTOIMMUNITY; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; EXONS; HUMANS; INTRONS; MICE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN CONFORMATION; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; TUMOR NECROSIS FACTOR LIGAND SUPERFAMILY MEMBER 13; TUMOR NECROSIS FACTORS;

EID: 84865348756     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2012.05.009     Document Type: Review

References (112)

1. Varin M.M., Le Pottier L., Youinou P., Saulep D., Mackay F., Pers J.O. B-cell tolerance breakdown in Sjogren's syndrome: focus on BAFF. Autoimmunity Reviews 2010, 9:604-608.
2. Daridon C., Youinou P., Pers J.O. BAFF, APRIL, TWE-PRIL: who's who?. Autoimmunity Reviews 2008, 7:267-271.
3. Schneider P., MacKay F., Steiner V., Hofmann K., Bodmer J.L., Holler N., et al. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. The Journal of Experimental Medicine 1999, 189:1747-1756.
4. Mackay F., Woodcock S.A., Lawton P., Ambrose C., Baetscher M., Schneider P., et al. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. The Journal of Experimental Medicine 1999, 190:1697-1710.
5. Groom J., Kalled S.L., Cutler A.H., Olson C., Woodcock S.A., Schneider P., et al. Association of BAFF/BLyS overexpression and altered B cell differentiation with Sjogren's syndrome. The Journal of Clinical Investigation 2002, 109:59-68.
6. Mackay F., Schneider P., Rennert P., Browning J. BAFF and APRIL: a tutorial on B cell survival. Annual Review of Immunology 2003, 21:231-264.
7. Mackay F., Schneider P. Cracking the BAFF code. Nature Reviews Immunology 2009, 9:491-502.
8. Youinou P., Pers J.O. The late news on BAFF in autoimmune diseases. Autoimmunity Reviews 2010, 9:804-806.
9. Meyer-Bahlburg A., Andrews S.F., Yu K.O., Porcelli S.A., Rawlings D.J. Characterization of a late transitional B cell population highly sensitive to BAFF-mediated homeostatic proliferation. The Journal of Experimental Medicine 2008, 205:155-168.
10. Thien M., Phan T.G., Gardam S., Amesbury M., Basten A., Mackay F., et al. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 2004, 20:785-798.
11. Rochas C., Hillion S., Saraux A., Mageed R.A., Youinou P., Jamin C., et al. Transmembrane BAFF from rheumatoid synoviocytes requires interleukin-6 to induce the expression of recombination-activating gene in B lymphocytes. Arthritis and Rheumatism 2009, 60:1261-1271.
12. Pers J.O., Daridon C., Devauchelle V., Jousse S., Saraux A., Jamin C., et al. BAFF overexpression is associated with autoantibody production in autoimmune diseases. Annals of the New York Academy of Sciences 2005, 1050:34-39.
13. Youinou P., Saraux A., Pers J.O. B-Lymphocytes govern the pathogenesis of Sjogren's syndrome. Current Pharmaceutical Biotechnology 2012.
14. Mariette X., Roux S., Zhang J., Bengoufa D., Lavie F., Zhou T., et al. The level of BLyS (BAFF) correlates with the titre of autoantibodies in human Sjogren's syndrome. Annals of the Rheumatic Diseases 2003, 62:168-171.
15. Collins C.E., Gavin A.L., Migone T.S., Hilbert D.M., Nemazee D., Stohl W. B lymphocyte stimulator (BLyS) isoforms in systemic lupus erythematosus: disease activity correlates better with blood leukocyte BLyS mRNA levels than with plasma BLyS protein levels. Arthritis Research & Therapy 2006, 8:R6.
16. Le Pottier L., Bendaoud B., Renaudineau Y., Youinou P., Pers J.O., Daridon C. New ELISA for B cell-activating factor. Clinical Chemistry 2009, 55:1843-1851.
17. Fu L., Lin-Lee Y.C., Pham L.V., Tamayo A., Yoshimura L., Ford R.J. Constitutive NF-kappaB and NFAT activation leads to stimulation of the BLyS survival pathway in aggressive B-cell lymphomas. Blood 2006, 107:4540-4548.
18. Lin-Lee Y.C., Pham L.V., Tamayo A.T., Fu L., Zhou H.J., Yoshimura L.C., et al. Nuclear localization in the biology of the CD40 receptor in normal and neoplastic human B lymphocytes. The Journal of Biological Chemistry 2006, 281:18878-18887.
19. Fu L., Lin-Lee Y.C., Pham L.V., Tamayo A.T., Yoshimura L.C., Ford R.J. BAFF-R promotes cell proliferation and survival through interaction with IKKbeta and NF-kappaB/c-Rel in the nucleus of normal and neoplastic B-lymphoid cells. Blood 2009, 113:4627-4636.
20. Zhou H.J., Pham L.V., Tamayo A.T., Lin-Lee Y.C., Fu L., Yoshimura L.C., et al. Nuclear CD40 interacts with c-Rel and enhances proliferation in aggressive B-cell lymphoma. Blood 2007, 110:2121-2127.
21. Moon E.Y., Park H. B cell activating factor (BAFF) gene promoter activity depends upon co-activator, p300. Immunobiology 2007, 212:637-645.
22. Kim H.A., Jeon S.H., Seo G.Y., Park J.B., Kim P.H. TGF-beta1 and IFN-gamma stimulate mouse macrophages to express BAFF via different signaling pathways. Journal of Leukocyte Biology 2008, 83:1431-1439.
23. Gavin A.L., Ait-Azzouzene D., Ware C.F., Nemazee D. DeltaBAFF, an alternate splice isoform that regulates receptor binding and biopresentation of the B cell survival cytokine, BAFF. The Journal of Biological Chemistry 2003, 278:38220-38228.
24. Guan Z.B., Dan W.B., Shui Y., Ye J.L., Zhang S.Q. cDNA cloning, expression and bioactivity of porcine BAFF. Developmental and Comparative Immunology 2007, 31:1211-1219.
25. Lu W., Cao P., Cai X., Yu J., Hu C., Cao M., et al. Molecular cloning, expression, and bioactivity of dove B lymphocyte stimulator (doBAFF). Veterinary Immunology and Immunopathology 2009, 128:374-380.
26. Guan Z.B., Ye J.L., Dan W.B., Yao W.J., Zhang S.Q. Cloning, expression and bioactivity of duck BAFF. Molecular Immunology 2007, 44:1471-1476.
27. Schneider K., Kothlow S., Schneider P., Tardivel A., Gobel T., Kaspers B., et al. Chicken BAFF-a highly conserved cytokine that mediates B cell survival. International Immunology 2004, 16:139-148.
28. Liu Y., Xu L., Opalka N., Kappler J., Shu H.B., Zhang G. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Cell 2002, 108:383-394.
29. Oren D.A., Li Y., Volovik Y., Morris T.S., Dharia C., Das K., et al. Structural basis of BLyS receptor recognition. Nature Structural Biology 2002, 9:288-292.
30. Karpusas M., Cachero T.G., Qian F., Boriack-Sjodin A., Mullen C., Strauch K., et al. Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes. Journal of Molecular Biology 2002, 315:1145-1154.
31. Bodmer J.L., Meier P., Tschopp J., Schneider P. Cysteine 230 is essential for the structure and activity of the cytotoxic ligand TRAIL. The Journal of Biological Chemistry 2000, 275:20632-20637.
32. Smith R.A., Baglioni C. The active form of tumor necrosis factor is a trimer. The Journal of Biological Chemistry 1987, 262:6951-6954.
33. Cachero T.G., Schwartz I.M., Qian F., Day E.S., Bossen C., Ingold K., et al. Formation of virus-like clusters is an intrinsic property of the tumor necrosis factor family member BAFF (B cell activating factor). Biochemistry 2006, 45:2006-2013.
34. Kawasaki A., Tsuchiya N., Fukazawa T., Hashimoto H., Tokunaga K. Analysis on the association of human BLYS (BAFF, TNFSF13B) polymorphisms with systemic lupus erythematosus and rheumatoid arthritis. Genes and Immunity 2002, 3:424-429.
35. Gottenberg J.E., Sellam J., Ittah M., Lavie F., Proust A., Zouali H., et al. No evidence for an association between the -871 T/C promoter polymorphism in the B-cell-activating factor gene and primary Sjogren's syndrome. Arthritis Research & Therapy 2006, 8:R30.
36. Novak A.J., Grote D.M., Ziesmer S.C., Kline M.P., Manske M.K., Slager S., et al. Elevated serum B-lymphocyte stimulator levels in patients with familial lymphoproliferative disorders. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 2006, 24:983-987.
37. Novak A.J., Slager S.L., Fredericksen Z.S., Wang A.H., Manske M.M., Ziesmer S., et al. Genetic variation in B-cell-activating factor is associated with an increased risk of developing B-cell non-Hodgkin lymphoma. Cancer Research 2009, 69:4217-4224.
38. Zhai K., Tian X., Wu C., Lu N., Chang J., Huang L., et al. Cytokine BAFF gene variation is associated with survival of patients with T-cell lymphomas. Clinical Cancer Research: an Official Journal of the American Association for Cancer Research 2012, 18:2250-2256.
39. Abdel-Hamid S.M., Al-Lithy H.N. B cell activating factor gene polymorphisms in patients with risk of idiopathic thrombocytopenic purpura. The American Journal of the Medical Sciences 2011, 342:9-14.
40. Nossent J.C., Lester S., Zahra D., Mackay C.R., Rischmueller M. Polymorphism in the 5' regulatory region of the B-lymphocyte activating factor gene is associated with the Ro/La autoantibody response and serum BAFF levels in primary Sjogren's syndrome. Rheumatology (Oxford) 2008, 47:1311-1316.
41. Gavin A.L., Duong B., Skog P., Ait-Azzouzene D., Greaves D.R., Scott M.L., et al. DeltaBAFF, a splice isoform of BAFF, opposes full-length BAFF activity in vivo in transgenic mouse models. Journal of Immunology 2005, 175:319-328.
42. Ota M., Duong B.H., Torkamani A., Doyle C.M., Gavin A.L., Ota T., et al. Regulation of the B cell receptor repertoire and self-reactivity by BAFF. Journal of Immunology 2010, 185:4128-4136.
43. Krumbholz M., Theil D., Derfuss T., Rosenwald A., Schrader F., Monoranu C.M., et al. BAFF is produced by astrocytes and up-regulated in multiple sclerosis lesions and primary central nervous system lymphoma. The Journal of Experimental Medicine 2005, 201:195-200.
44. Diao Z., Ye T., Cao P., Zhang J., Mei J., Lin Z., et al. Expression, purification, and characterization of recombinant human soluble BAFF secreted from the yeast Pichia pastoris. Protein Expression and Purification 2007, 54:11-17.
45. Roschke V., Sosnovtseva S., Ward C.D., Hong J.S., Smith R., Albert V., et al. BLyS and APRIL form biologically active heterotrimers that are expressed in patients with systemic immune-based rheumatic diseases. Journal of Immunology 2002, 169:4314-4321.
46. Browning J.L., Ngam-ek A., Lawton P., DeMarinis J., Tizard R., Chow E.P., et al. Lymphotoxin beta, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell 1993, 72:847-856.
47. Wallweber H.J., Compaan D.M., Starovasnik M.A., Hymowitz S.G. The crystal structure of a proliferation-inducing ligand, APRIL. Journal of Molecular Biology 2004, 343:283-290.
48. Moore P.A., Belvedere O., Orr A., Pieri K., LaFleur D.W., Feng P., et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 1999, 285:260-263.
49. Shu H.B., Hu W.H., Johnson H. TALL-1 is a novel member of the TNF family that is down-regulated by mitogens. Journal of Leukocyte Biology 1999, 65:680-683.
50. Mukhopadhyay A., Ni J., Zhai Y., Yu G.L., Aggarwal B.B. Identification and characterization of a novel cytokine, THANK, a TNF homologue that activates apoptosis, nuclear factor-kappaB, and c-Jun NH2-terminal kinase. The Journal of Biological Chemistry 1999, 274:15978-15981.
51. Huard B., Arlettaz L., Ambrose C., Kindler V., Mauri D., Roosnek E., et al. BAFF production by antigen-presenting cells provides T cell co-stimulation. International Immunology 2004, 16:467-475.
52. Kern C., Cornuel J.F., Billard C., Tang R., Rouillard D., Stenou V., et al. Involvement of BAFF and APRIL in the resistance to apoptosis of B-CLL through an autocrine pathway. Blood 2004, 103:679-688.
53. Daridon C., Devauchelle V., Hutin P., Le Berre R., Martins-Carvalho C., Bendaoud B., et al. Aberrant expression of BAFF by B lymphocytes infiltrating the salivary glands of patients with primary Sjogren's syndrome. Arthritis and Rheumatism 2007, 56:1134-1144.
54. Schaumann D.H., Tuischer J., Ebell W., Manz R.A., Lauster R. VCAM-1-positive stromal cells from human bone marrow producing cytokines for B lineage progenitors and for plasma cells: SDF-1, flt3L, and BAFF. Molecular Immunology 2007, 44:1606-1612.
55. Hase H., Kanno Y., Kojima M., Hasegawa K., Sakurai D., Kojima H., et al. BAFF/BLyS can potentiate B-cell selection with the B-cell coreceptor complex. Blood 2004, 103:2257-2265.
56. Ohata J., Zvaifler N.J., Nishio M., Boyle D.L., Kalled S.L., Carson D.A., et al. Fibroblast-like synoviocytes of mesenchymal origin express functional B cell-activating factor of the TNF family in response to proinflammatory cytokines. Journal of Immunology 2005, 174:864-870.
57. Daridon C., Pers J.O., Devauchelle V., Martins-Carvalho C., Hutin P., Pennec Y.L., et al. Identification of transitional type II B cells in the salivary glands of patients with Sjogren's syndrome. Arthritis and Rheumatism 2006, 54:2280-2288.
58. Nardelli B., Belvedere O., Roschke V., Moore P.A., Olsen H.S., Migone T.S., et al. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 2001, 97:198-204.
59. Litinskiy M.B., Nardelli B., Hilbert D.M., He B., Schaffer A., Casali P., et al. DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nature Immunology 2002, 3:822-829.
60. Scapini P., Nardelli B., Nadali G., Calzetti F., Pizzolo G., Montecucco C., et al. G-CSF-stimulated neutrophils are a prominent source of functional BLyS. The Journal of Experimental Medicine 2003, 197:297-302.
61. Lopez-Fraga M., Fernandez R., Albar J.P., Hahne M. Biologically active APRIL is secreted following intracellular processing in the Golgi apparatus by furin convertase. EMBO Reports 2001, 2:945-951.
62. Pradet-Balade B., Medema J.P., Lopez-Fraga M., Lozano J.C., Kolfschoten G.M., Picard A., et al. An endogenous hybrid mRNA encodes TWE-PRIL, a functional cell surface TWEAK-APRIL fusion protein. The EMBO Journal 2002, 21:5711-5720.
63. Koyama T., Tsukamoto H., Masumoto K., Himeji D., Hayashi K., Harada M., et al. A novel polymorphism of the human APRIL gene is associated with systemic lupus erythematosus. Rheumatology (Oxford) 2003, 42:980-985.
64. Lee Y.H., Ota F., Kim-Howard X., Kaufman K.M., Nath S.K. APRIL polymorphism and systemic lupus erythematosus (SLE) susceptibility. Rheumatology (Oxford) 2007, 46:1274-1276.
65. Kawasaki A., Tsuchiya N., Ohashi J., Murakami Y., Fukazawa T., Kusaoi M., et al. Role of APRIL (TNFSF13) polymorphisms in the susceptibility to systemic lupus erythematosus in Japanese. Rheumatology (Oxford) 2007, 46:776-782.
66. Hymowitz S.G., Patel D.R., Wallweber H.J., Runyon S., Yan M., Yin J., et al. Structures of APRIL-receptor complexes: like BCMA, TACI employs only a single cysteine-rich domain for high affinity ligand binding. The Journal of Biological Chemistry 2005, 280:7218-7227.
67. Dillon S.R., Gross J.A., Ansell S.M., Novak A.J. An APRIL to remember: novel TNF ligands as therapeutic targets. Nature Reviews Drug Discovery 2006, 5:235-246.
68. Kalled S.L., Ambrose C., Hsu Y.M. The biochemistry and biology of BAFF, APRIL and their receptors. Current Directions in Autoimmunity 2005, 8:206-242.
69. Bossen C., Schneider P. BAFF, APRIL and their receptors: structure, function and signaling. Seminars in Immunology 2006, 18:263-275.
70. Xia X.Z., Treanor J., Senaldi G., Khare S.D., Boone T., Kelley M., et al. TACI is a TRAF-interacting receptor for TALL-1, a tumor necrosis factor family member involved in B cell regulation. The Journal of Experimental Medicine 2000, 192:137-143.
71. Hatzoglou A., Roussel J., Bourgeade M.F., Rogier E., Madry C., Inoue J., et al. TNF receptor family member BCMA (B cell maturation) associates with TNF receptor-associated factor (TRAF) 1, TRAF2, and TRAF3 and activates NF-kappa B, elk-1, c-Jun N-terminal kinase, and p38 mitogen-activated protein kinase. Journal of Immunology 2000, 165:1322-1330.
72. Han S., Yoon K., Lee K., Kim K., Jang H., Lee N.K., et al. TNF-related weak inducer of apoptosis receptor, a TNF receptor superfamily member, activates NF-kappa B through TNF receptor-associated factors. Biochemical and Biophysical Research Communications 2003, 305:789-796.
73. Day E.S., Cachero T.G., Qian F., Sun Y., Wen D., Pelletier M., et al. Selectivity of BAFF/BLyS and APRIL for binding to the TNF family receptors BAFFR/BR3 and BCMA. Biochemistry 2005, 44:1919-1931.
74. Koyama T., Tsukamoto H., Miyagi Y., Himeji D., Otsuka J., Miyagawa H., et al. Raised serum APRIL levels in patients with systemic lupus erythematosus. Annals of the Rheumatic Diseases 2005, 64:1065-1067.
75. Huard B., Tran N.L., Benkhoucha M., Manzin-Lorenzi C., Santiago-Raber M.L. Selective APRIL blockade delays systemic lupus erythematosus in mouse. PloS One 2012, 7:e31837.
76. Seyler T.M., Park Y.W., Takemura S., Bram R.J., Kurtin P.J., Goronzy J.J., et al. BLyS and APRIL in rheumatoid arthritis. The Journal of Clinical Investigation 2005, 115:3083-3092.
77. Thangarajh M., Masterman T., Rot U., Duvefelt K., Brynedal B., Karrenbauer V.D., et al. Increased levels of APRIL (a proliferation-inducing ligand) mRNA in multiple sclerosis. Journal of Neuroimmunology 2005, 167:210-214.
78. Piazza F., DiFrancesco J.C., Fusco M.L., Corti D., Pirovano L., Frigeni B., et al. Cerebrospinal fluid levels of BAFF and APRIL in untreated multiple sclerosis. Journal of Neuroimmunology 2010, 220:104-107.
79. Winkles J.A. The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nature Reviews Drug Discovery 2008, 7:411-425.
80. Schneider P., Schwenzer R., Haas E., Muhlenbeck F., Schubert G., Scheurich P., et al. TWEAK can induce cell death via endogenous TNF and TNF receptor 1. European Journal of Immunology 1999, 29:1785-1792.
81. Meyer T., Amaya M., Desai H., Robles-Carrillo L., Hatfield M., Francis J.L., et al. Human platelets contain and release TWEAK. Platelets 2010, 21:571-574.
82. van Kuijk A.W., Wijbrandts C.A., Vinkenoog M., Zheng T.S., Reedquist K.A., Tak P.P. TWEAK and its receptor Fn14 in the synovium of patients with rheumatoid arthritis compared to psoriatic arthritis and its response to tumour necrosis factor blockade. Annals of the Rheumatic Diseases 2010, 69:301-304.
83. Maecker H., Varfolomeev E., Kischkel F., Lawrence D., LeBlanc H., Lee W., et al. TWEAK attenuates the transition from innate to adaptive immunity. Cell 2005, 123:931-944.
84. Desplat-Jego S., Feuillet L., Creidy R., Malikova I., Rance R., Khrestchatisky M., et al. TWEAK is expressed at the cell surface of monocytes during multiple sclerosis. Journal of Leukocyte Biology 2009, 85:132-135.
85. Chicheportiche Y., Bourdon P.R., Xu H., Hsu Y.M., Scott H., Hession C., et al. TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. The Journal of Biological Chemistry 1997, 272:32401-32410.
86. Kolfschoten G.M., Pradet-Balade B., Hahne M., Medema J.P. TWE-PRIL; a fusion protein of TWEAK and APRIL. Biochemical Pharmacology 2003, 66:1427-1432.
87. Wiley S.R., Cassiano L., Lofton T., Davis-Smith T., Winkles J.A., Lindner V., et al. A novel TNF receptor family member binds TWEAK and is implicated in angiogenesis. Immunity 2001, 15:837-846.
88. Girgenrath M., Weng S., Kostek C.A., Browning B., Wang M., Brown S.A., et al. TWEAK, via its receptor Fn14, is a novel regulator of mesenchymal progenitor cells and skeletal muscle regeneration. The EMBO Journal 2006, 25:5826-5839.
89. Bover L.C., Cardo-Vila M., Kuniyasu A., Sun J., Rangel R., Takeya M., et al. A previously unrecognized protein-protein interaction between TWEAK and CD163: potential biological implications. Journal of Immunology 2007, 178:8183-8194.
90. Buechler C., Ritter M., Orso E., Langmann T., Klucken J., Schmitz G. Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro- and antiinflammatory stimuli. Journal of Leukocyte Biology 2000, 67:97-103.
91. Van Gorp H., Delputte P.L., Nauwynck H.J. Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Molecular Immunology 2010, 47:1650-1660.
92. Moreno J.A., Munoz-Garcia B., Martin-Ventura J.L., Madrigal-Matute J., Orbe J., Paramo J.A., et al. The CD163-expressing macrophages recognize and internalize TWEAK: potential consequences in atherosclerosis. Atherosclerosis 2009, 207:103-110.
93. Winkles J.A., Alberts G.F. Differential regulation of polo-like kinase 1, 2, 3, and 4 gene expression in mammalian cells and tissues. Oncogene 2005, 24:260-266.
94. Dharmapatni A.A., Smith M.D., Crotti T.N., Holding C.A., Vincent C., Weedon H.M., et al. TWEAK and Fn14 expression in the pathogenesis of joint inflammation and bone erosion in rheumatoid arthritis. Arthritis Research & Therapy 2011, 13:R51.
95. Park M.C., Chung S.J., Park Y.B., Lee S.K. Relationship of serum TWEAK level to cytokine level, disease activity, and response to anti-TNF treatment in patients with rheumatoid arthritis. Scandinavian Journal of Rheumatology 2008, 37:173-178.
96. Serafini B., Magliozzi R., Rosicarelli B., Reynolds R., Zheng T.S., Aloisi F. Expression of TWEAK and its receptor Fn14 in the multiple sclerosis brain: implications for inflammatory tissue injury. Journal of Neuropathology and Experimental Neurology 2008, 67:1137-1148.
97. Iocca H.A., Plant S.R., Wang Y., Runkel L., O'Connor B.P., Lundsmith E.T., et al. TNF superfamily member TWEAK exacerbates inflammation and demyelination in the cuprizone-induced model. Journal of Neuroimmunology 2008, 194:97-106.
98. Wang J., Chen F., Zheng P., Deng W., Yuan J., Peng B., et al. Huperzine A ameliorates experimental autoimmune encephalomyelitis via the suppression of T cell-mediated neuronal inflammation in mice. Experimental Neurology 2012.
99. El-Shehaby A., Darweesh H., El-Khatib M., Momtaz M., Marzouk S., El-Shaarawy N., et al. Correlations of urinary biomarkers, TNF-like weak inducer of apoptosis (TWEAK), osteoprotegerin (OPG), monocyte chemoattractant protein-1 (MCP-1), and IL-8 with lupus nephritis. Journal of Clinical Immunology 2011, 31:848-856.
100. Liu Z.C., Zhou Q.L., Li X.Z., Yang J.H., Ao X., Veeraragoo P., et al. Elevation of human tumor necrosis factor-like weak inducer of apoptosis in peripheral blood mononuclear cells is correlated with disease activity and lupus nephritis in patients with systemic lupus erythematosus. Cytokine 2011, 53:295-300.
101. Schwartz N., Su L., Burkly L.C., Mackay M., Aranow C., Kollaros M., et al. Urinary TWEAK and the activity of lupus nephritis. Journal of Autoimmunity 2006, 27:242-250.
102. Gao H.X., Campbell S.R., Burkly L.C., Jakubowski A., Jarchum I., Banas B., et al. TNF-like weak inducer of apoptosis (TWEAK) induces inflammatory and proliferative effects in human kidney cells. Cytokine 2009, 46:24-35.
103. Tobon G.J., Pers J.O., Youinou P., Saraux A. B cell-targeted therapies in Sjogren's syndrome. Autoimmunity Reviews 2010, 9:224-228.
104. Behrens M., Smart M., Luckey D., Luthra H., Taneja V. To B or not to B: role of B cells in pathogenesis of arthritis in HLA transgenic mice. Journal of Autoimmunity 2011, 37:95-103.
105. Gershwin M.E., Shoenfeld Y. Chella David: a lifetime contribution in translational immunology. Journal of Autoimmunity 2011, 37:59-62.
106. Rose N.R. The genetics of autoimmune thyroiditis: the first decade. Journal of Autoimmunity 2011, 37:88-94.
107. Sharma R., Sung S.S.J., Ju C.Y.A., Deshmukh S., Fu S.M., Ju S.T. Regulatory T-cell (Treg) hybridoma as a novel tool to study Foxp3 regulation and Treg fate. Journal of Autoimmunity 2011, 37:113-121.
108. Youinou P., Haralampos M. Moutsopoulos: a lifetime in autoimmunity. Journal of Autoimmunity 2010, 35:171-175.
109. Juran B.D., Lazaridis K.N. Update on the genetics and genomics of PBC. Journal of Autoimmunity 2010, 35:181-187.
110. Miyagawa F., Gutermuth J., Zhang H., Katz S.I. The use of mouse models to better understand mechanisms of autoimmunity and tolerance. Journal of Autoimmunity 2010, 35:192-198.
111. Mackay I.R., Leskovsek N.V., Rose N.R. The odd couple: a fresh look at autoimmunity and immunodeficiency. Journal of Autoimmunity 2010, 35:199-205.
112. Kontagi E., Boumpas D.T. Innate immunity in systemic lupus erythematosus: sensing endogenous nucleic acids. Journal of Autoimmunity 2010, 35:206-211.