A balance between B cell receptor and inhibitory receptor signaling controls plasma cell differentiation by maintaining optimal Ets1 levels

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 909-920

  Luo, Wei ^a   Mayeux, Jessica ^b   Gutierrez, Toni ^b   Russell, Lisa ^a   Getahun, Andrew ^c   Müller, Jennifer ^d   Tedder, Thomas ^e   Parnes, Jane ^f,h   Rickert, Robert ^g   Nitschke, Lars ^d   Cambier, John ^c   Satterthwaite, Anne B ^b   Garrett Sinha, Lee Ann ^a  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g BURNHAM INSTITUTE   (United States)

^h AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; BRUTON TYROSINE KINASE; CD22 ANTIGEN; I KAPPA B KINASE BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE LYN; PROTEIN TYROSINE PHOSPHATASE SHP 1; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN G; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR ETS 1; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ARTICLE; B LYMPHOCYTE ACTIVATION; B LYMPHOCYTE DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; FETUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL LINE, TUMOR; GENE EXPRESSION; LECTINS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PLASMA CELLS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEIN C-ETS-1; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, CELL SURFACE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIALIC ACID BINDING IG-LIKE LECTIN 2; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 84904256707     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400666     Document Type: Article

References (84)

1. Packard, T. A., and J. C. Cambier. 2013. B lymphocyte antigen receptor signaling: initiation, amplification, and regulation. F1000Prime Rep. 5: 40.
2. Nitschke, L. 2005. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr. Opin. Immunol. 17: 290-297. (Pubitemid 40692664)
3. Poe, J. C., and T. F. Tedder. 2012. CD22 and Siglec-G in B cell function and tolerance. Trends Immunol. 33: 413-420.
4. Tsubata, T. 2012. Role of inhibitory BCR co-receptors in immunity. Infect. Disord. Drug Targets 12: 181-190.
5. Vang, T., A. V. Miletic, Y. Arimura, L. Tautz, R. C. Rickert, and T. Mustelin. 2008. Protein tyrosine phosphatases in autoimmunity. Annu. Rev. Immunol. 26: 29-55. (Pubitemid 351600370)
6. Nishizumi, H., I. Taniuchi, Y. Yamanashi, D. Kitamura, D. Ilic, S. Mori, T. Watanabe, and T. Yamamoto. 1995. Impaired proliferation of peripheral B cells and indication of autoimmune disease in lyn-deficient mice. Immunity 3: 549-560.
7. Hibbs, M. L., D. M. Tarlinton, J. Armes, D. Grail, G. Hodgson, R. Maglitto, S. A. Stacker, and A. R. Dunn. 1995. Multiple defects in the immune system of Lyn-deficient mice, culminating in autoimmune disease. Cell 83: 301-311.
8. Chan, V. W., F. Meng, P. Soriano, A. L. DeFranco, and C. A. Lowell. 1997. Characterization of the B lymphocyte populations in Lyn-deficient mice and the role of Lyn in signal initiation and down-regulation. Immunity 7: 69-81. (Pubitemid 27357266)
9. Chan, V. W., C. A. Lowell, and A. L. DeFranco. 1998. Defective negative regulation of antigen receptor signaling in Lyn-deficient B lymphocytes. Curr. Biol. 8: 545-553. (Pubitemid 28222888)
10. Liossis, S. N., E. E. Solomou, M. A. Dimopoulos, P. Panayiotidis, M. M. Mavrikakis, and P. P. Sfikakis. 2001. B-cell kinase lyn deficiency in patients with systemic lupus erythematosus. J. Investig. Med. 49: 157-165. (Pubitemid 32187089)
11. Flores-Borja, F., P. S. Kabouridis, E. C. Jury, D. A. Isenberg, and R. A. Mageed. 2005. Decreased Lyn expression and translocation to lipid raft signaling domains in B lymphocytes from patients with systemic lupus erythematosus. Arthritis Rheum. 52: 3955-3965. (Pubitemid 41798235)
12. Tsui, H. W., K. A. Siminovitch, L. de Souza, and F. W. Tsui. 1993. Motheaten and viable motheaten mice have mutations in the haematopoietic cell phosphatase gene. Nat. Genet. 4: 124-129.
13. Pao, L. I., K. P. Lam, J. M. Henderson, J. L. Kutok, M. Alimzhanov, L. Nitschke, M. L. Thomas, B. G. Neel, and K. Rajewsky. 2007. B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity 27: 35-48. (Pubitemid 47089020)
14. Nitschke, L., R. Carsetti, B. Ocker, G. Köhler, and M. C. Lamers. 1997. CD22 is a negative regulator of B-cell receptor signalling. Curr. Biol. 7: 133-143. (Pubitemid 27155622)
15. Pan, C., N. Baumgarth, and J. R. Parnes. 1999. CD72-deficient mice reveal nonredundant roles of CD72 in B cell development and activation. Immunity 11: 495-506. (Pubitemid 29504204)
16. Hoffmann, A., S. Kerr, J. Jellusova, J. Zhang, F. Weisel, U. Wellmann, T. H. Winkler, B. Kneitz, P. R. Crocker, and L. Nitschke. 2007. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat. Immunol. 8: 695-704. (Pubitemid 46965345)
17. Bolland, S., and J. V. Ravetch. 2000. Spontaneous autoimmune disease in FcgRIIBdeficient mice results from strain-specific epistasis. Immunity 13: 277-285.
18. Jellusova, J., U. Wellmann, K. Amann, T. H. Winkler, and L. Nitschke. 2010. CD22 X Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J. Immunol. 184: 3618-3627.
19. Satterthwaite, A. B., C. A. Lowell, W. N. Khan, P. Sideras, F. W. Alt, and O. N. Witte. 1998. Independent and opposing roles for Btk and lyn in B and myeloid signaling pathways. J. Exp. Med. 188: 833-844. (Pubitemid 28433410)
20. Whyburn, L. R., K. E. Halcomb, C. M. Contreras, C. A. Lowell, O. N. Witte, and A. B. Satterthwaite. 2003. Reduced dosage of Bruton's tyrosine kinase uncouples B cell hyperresponsiveness from autoimmunity in lyn-/- mice. J. Immunol. 171: 1850-1858. (Pubitemid 36966468)
21. Gutierrez, T., K. E. Halcomb, A. J. Coughran, Q. Z. Li, and A. B. Satterthwaite. 2010. Separate checkpoints regulate splenic plasma cell accumulation and IgG autoantibody production in Lyn-deficient mice. Eur. J. Immunol. 40: 1897-1905.
22. Nutt, S. L., N. Taubenheim, J. Hasbold, L. M. Corcoran, and P. D. Hodgkin. 2011. The genetic network controlling plasma cell differentiation. Semin. Immunol. 23: 341-349.
23. Wang, D., S. A. John, J. L. Clements, D. H. Percy, K. P. Barton, and L. A. Garrett- Sinha. 2005. Ets-1 deficiency leads to altered B cell differentiation, hyperresponsiveness to TLR9 and autoimmune disease. Int. Immunol. 17: 1179-1191. (Pubitemid 41236075)
24. Seo, S., J. Buckler, and J. Erikson. 2001. Novel roles for Lyn in B cell migration and lipopolysaccharide responsiveness revealed using anti-double-stranded DNA Ig transgenic mice. J. Immunol. 166: 3710-3716. (Pubitemid 32224893)
25. Khan, W. N., F. W. Alt, R. M. Gerstein, B. A. Malynn, I. Larsson, G. Rathbun, L. Davidson, S. Müller, A. B. Kantor, L. A. Herzenberg, et al. 1995. Defective B cell development and function in Btk-deficient mice. Immunity 3: 283-299.
26. Satterthwaite, A. B., H. Cheroutre, W. N. Khan, P. Sideras, and O. N. Witte. 1997. Btk dosage determines sensitivity to B cell antigen receptor cross-linking. Proc. Natl. Acad. Sci. USA 94: 13152-13157.
27. Satterthwaite, A. B., F. Willis, P. Kanchanastit, D. Fruman, L. C. Cantley, C. D. Helgason, R. K. Humphries, C. A. Lowell, M. Simon, M. Leitges, et al. 2000. A sensitized genetic system for the analysis of murine B lymphocyte signal transduction pathways dependent on Bruton's tyrosine kinase. Proc. Natl. Acad. Sci. USA 97: 6687-6692. (Pubitemid 30412775)
28. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, et al. 1988. Altered immunoglobulin expression and functional silencing of selfreactive B lymphocytes in transgenic mice. Nature 334: 676-682.
29. Rickert, R. C., J. Roes, and K. Rajewsky. 1997. B lymphocyte?specific, Cremediated mutagenesis in mice. Nucleic Acids Res. 25: 1317-1318.
30. Sasaki, Y., E. Derudder, E. Hobeika, R. Pelanda, M. Reth, K. Rajewsky, and M. Schmidt-Supprian. 2006. Canonical NF-κB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24: 729-739. (Pubitemid 43867365)
31. Hao, Z., and K. Rajewsky. 2001. Homeostasis of peripheral B cells in the absence of B cell influx from the bone marrow. J. Exp. Med. 194: 1151-1164.
32. Takai, T., M. Ono, M. Hikida, H. Ohmori, and J. V. Ravetch. 1996. Augmented humoral and anaphylactic responses in Fc gRII-deficient mice. Nature 379: 346-349. (Pubitemid 26033077)
33. Anzelon, A. N., H. Wu, and R. C. Rickert. 2003. Pten inactivation alters peripheral B lymphocyte fate and reconstitutes CD19 function. Nat. Immunol. 4: 287-294. (Pubitemid 36322140)
34. Karlsson, M. C., R. Guinamard, S. Bolland, M. Sankala, R. M. Steinman, and J. V. Ravetch. 2003. Macrophages control the retention and trafficking of B lymphocytes in the splenic marginal zone. J. Exp. Med. 198: 333-340. (Pubitemid 36987858)
35. Hobeika, E., S. Thiemann, B. Storch, H. Jumaa, P. J. Nielsen, R. Pelanda, and M. Reth. 2006. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103: 13789-13794. (Pubitemid 44413986)
36. Sato, S., A. S. Miller, M. Inaoki, C. B. Bock, P. J. Jansen, M. L. Tang, and T. F. Tedder. 1996. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5: 551-562. (Pubitemid 27062065)
37. Ujike, A., K. Takeda, A. Nakamura, S. Ebihara, K. Akiyama, and T. Takai. 2002. Impaired dendritic cell maturation and increased T(H)2 responses in PIR-B-/- mice. Nat. Immunol. 3: 542-548. (Pubitemid 34662306)
38. Eyquem, S., K. Chemin, M. Fasseu, M. Chopin, F. Sigaux, A. Cumano, and J. C. Bories. 2004. The development of early and mature B cells is impaired in mice deficient for the Ets-1 transcription factor. Eur. J. Immunol. 34: 3187-3196. (Pubitemid 39549397)
39. Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IκB kinases essential for NF-κB activation. Science 278: 860-866. (Pubitemid 27467923)
40. Lei, K., A. Nimnual, W. X. Zong, N. J. Kennedy, R. A. Flavell, C. B. Thompson, D. Bar-Sagi, and R. J. Davis. 2002. The Bax subfamily of Bcl2-related proteins is essential for apoptotic signal transduction by c-Jun NH2-terminal kinase. Mol. Cell. Biol. 22: 4929-4942. (Pubitemid 34620425)
41. John, S., L. Russell, S. S. Chin, W. Luo, R. Oshima, and L. A. Garrett-Sinha. 2014. Transcription factor Ets1, but not the closely related factor Ets2, inhibits antibody-secreting cell differentiation. Mol. Cell. Biol. 34: 522-532.
42. John, S. A., J. L. Clements, L. M. Russell, and L. A. Garrett-Sinha. 2008. Ets-1 regulates plasma cell differentiation by interfering with the activity of the transcription factor Blimp-1. J. Biol. Chem. 283: 951-962.
43. Yamanashi, Y., S. Mori, M. Yoshida, T. Kishimoto, K. Inoue, T. Yamamoto, and K. Toyoshima. 1989. Selective expression of a protein-tyrosine kinase, p56lyn, in hematopoietic cells and association with production of human T-cell lymphotropic virus type I. Proc. Natl. Acad. Sci. USA 86: 6538-6542. (Pubitemid 19236313)
44. Bhattacharya, D., M. T. Cheah, C. B. Franco, N. Hosen, C. L. Pin, W. C. Sha, and I. L. Weissman. 2007. Transcriptional profiling of antigen-dependent murine B cell differentiation and memory formation. J. Immunol. 179: 6808-6819.
45. Barton, K., N. Muthusamy, C. Fischer, C. N. Ting, T. L. Walunas, L. L. Lanier, and J. M. Leiden. 1998. The Ets-1 transcription factor is required for the development of natural killer cells in mice. Immunity 9: 555-563. (Pubitemid 28499206)
46. Bhat, N. K., K. L. Komschlies, S. Fujiwara, R. J. Fisher, B. J. Mathieson, T. A. Gregorio, H. A. Young, J. W. Kasik, K. Ozato, and T. S. Papas. 1989. Expression of ets genes in mouse thymocyte subsets and T cells. J. Immunol. 142: 672-678. (Pubitemid 19039993)
47. Sotirellis, N., T. M. Johnson, M. L. Hibbs, I. J. Stanley, E. Stanley, A. R. Dunn, and H. C. Cheng. 1995. Autophosphorylation induces autoactivation and a decrease in the Src homology 2 domain accessibility of the Lyn protein kinase. J. Biol. Chem. 270: 29773-29780. (Pubitemid 26001645)
48. McPherson, V. A., N. Sharma, S. Everingham, J. Smith, H. H. Zhu, G. S. Feng, and A. W. Craig. 2009. SH2 domain-containing phosphatase-2 protein-tyrosine phosphatase promotes FcεRI-induced activation of Fyn and Erk pathways leading to TNFα release from bone marrow-derived mast cells. J. Immunol. 183: 4940-4947.
49. ten Hacken, E., C. Scielzo, M. T. Bertilaccio, L. Scarfò, B. Apollonio, F. Barbaglio, K. Stamatopoulos, M. Ponzoni, P. Ghia, and F. Caligaris-Cappio. 2013. Targeting the LYN/HS1 signaling axis in chronic lymphocytic leukemia. Blood 121: 2264-2273.
50. Alvarez-Errico, D., Y. Yamashita, R. Suzuki, S. Odom, Y. Furumoto, T. Yamashita, and J. Rivera. 2010. Functional analysis of Lyn kinase A and B isoforms reveals redundant and distinct roles in FcεRI-dependent mast cell activation. J. Immunol. 184: 5000-5008.
51. Silver, K. L., T. L. Crockford, T. Bouriez-Jones, S. Milling, T. Lambe, and R. J. Cornall. 2007. MyD88-dependent autoimmune disease in Lyn-deficient mice. Eur. J. Immunol. 37: 2734-2743. (Pubitemid 47578292)
52. Tsantikos, E., S. A. Oracki, C. Quilici, G. P. Anderson, D. M. Tarlinton, and M. L. Hibbs. 2010. Autoimmune disease in Lyn-deficient mice is dependent on an inflammatory environment established by IL-6. J. Immunol. 184: 1348-1360.
53. Hauser, J., J. Verma-Gaur, A. Wallenius, and T. Grundström. 2009. Initiation of antigen receptor-dependent differentiation into plasma cells by calmodulin inhibition of E2A. J. Immunol. 183: 1179-1187.
54. Raghunandan, R., F. W. Frissora, and N. Muthusamy. 2013. Modulation of Ets-1 expression in B lymphocytes is dependent on the antigen receptor-mediated activation signals and cell cycle status. Scand. J. Immunol. 77: 75-83.
55. Bolland, S., R. N. Pearse, T. Kurosaki, and J. V. Ravetch. 1998. SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity 8: 509-516. (Pubitemid 28196804)
56. Maeda, A., A. M. Scharenberg, S. Tsukada, J. B. Bolen, J. P. Kinet, and T. Kurosaki. 1999. Paired immunoglobulin-like receptor B (PIR-B) inhibits BCR-induced activation of Syk and Btk by SHP-1. Oncogene 18: 2291-2297. (Pubitemid 29192706)
57. Li, Z., M. I. Wahl, A. Eguinoa, L. R. Stephens, P. T. Hawkins, and O. N. Witte. 1997. Phosphatidylinositol 3-kinase-γ activates Bruton's tyrosine kinase in concert with Src family kinases. Proc. Natl. Acad. Sci. USA 94: 13820-13825. (Pubitemid 28009668)
58. Saito, K., A. M. Scharenberg, and J. P. Kinet. 2001. Interaction between the Btk PH domain and phosphatidylinositol-3,4,5-trisphosphate directly regulates Btk. J. Biol. Chem. 276: 16201-16206.
59. Petro, J. B., S. M. Rahman, D. W. Ballard, and W. N. Khan. 2000. Bruton's tyrosine kinase is required for activation of IκB kinase and nuclear factor kappaB in response to B cell receptor engagement. J. Exp. Med. 191: 1745-1754.
60. Bajpai, U. D., K. Zhang, M. Teutsch, R. Sen, and H. H. Wortis. 2000. Bruton's tyrosine kinase links the B cell receptor to nuclear factor κB activation. J. Exp. Med. 191: 1735-1744. (Pubitemid 30331570)
61. Inabe, K., T. Miyawaki, R. Longnecker, H. Matsukura, S. Tsukada, and T. Kurosaki. 2002. Bruton's tyrosine kinase regulates B cell antigen receptormediated JNK1 response through Rac1 and phospholipase C-γ2 activation. FEBS Lett. 514: 260-262. (Pubitemid 34273950)
62. Forssell, J., A. Nilsson, and P. Sideras. 2000. Reduced formation of phosphatidic acid upon B-cell receptor triggering of mouse B-lymphocytes lacking Bruton's tyrosine kinase. Scand. J. Immunol. 52: 30-38. (Pubitemid 30435982)
63. Jiang, A., A. Craxton, T. Kurosaki, and E. A. Clark. 1998. Different protein tyrosine kinases are required for B cell antigen receptor-mediated activation of extracellular signal-regulated kinase, c-Jun NH2-terminal kinase 1, and p38 mitogen-activated protein kinase. J. Exp. Med. 188: 1297-1306. (Pubitemid 28478018)
64. Halcomb, K. E., C. M. Contreras, R. M. Hinman, T. G. Coursey, H. L. Wright, and A. B. Satterthwaite. 2007. Btk and phospholipase Cγ2 can function independently during B cell development. Eur. J. Immunol. 37: 1033-1042. (Pubitemid 46927835)
65. O'Neill, S. K., A. Getahun, S. B. Gauld, K. T. Merrell, I. Tamir, M. J. Smith, J. M. Dal Porto, Q. Z. Li, and J. C. Cambier. 2011. Monophosphorylation of CD79a and CD79b ITAM motifs initiates a SHIP-1 phosphatase-mediated inhibitory signaling cascade required for B cell anergy. Immunity 35: 746-756.
66. Xu, M., R. Hou, A. Sato-Hayashizaki, R. Man, C. Zhu, C. Wakabayashi, S. Hirose, T. Adachi, and T. Tsubata. 2013. Cd72(c) is a modifier gene that regulates Fas(lpr)-induced autoimmune disease. J. Immunol. 190: 5436-5445.
67. Shultz, L. D., D. R. Coman, C. L. Bailey,W. G. Beamer, and C. L. Sidman. 1984. "Viable motheaten," a new allele at the motheaten locus. I. Pathology. Am. J. Pathol. 116: 179-192.
68. Kersseboom, R., L. Kil, R. Flierman, M. van der Zee, G. M. Dingjan, S. Middendorp, A. Maas, and R. W. Hendriks. 2010. Constitutive activation of Bruton's tyrosine kinase induces the formation of autoreactive IgM plasma cells. Eur. J. Immunol. 40: 2643-2654.
69. Hug, E., E. Hobeika, M. Reth, and H. Jumaa. 2013. Inducible expression of hyperactive Syk in B cells activates Blimp-1-dependent terminal differentiation. Oncogene. In press.
70. Lamagna, C., Y. Hu, A. L. DeFranco, and C. A. Lowell. 2014. B cell-specific loss of Lyn kinase leads to autoimmunity. J. Immunol. 192: 919-928.
71. Leadbetter, E. A., I. R. Rifkin, A. M. Hohlbaum, B. C. Beaudette, M. J. Shlomchik, and A. Marshak-Rothstein. 2002. Chromatin-IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416: 603-607. (Pubitemid 34406754)
72. Garrett-Sinha, L. A. 2013. Review of Ets1 structure, function, and roles in immunity. Cell. Mol. Life Sci. 70: 3375-3390.
73. Keck, S., M. Freudenberg, and M. Huber. 2010. Activation of murine macrophages via TLR2 and TLR4 is negatively regulated by a Lyn/PI3K module and promoted by SHIP1. J. Immunol. 184: 5809-5818.
74. Dustin, L. B., D. R. Plas, J. Wong, Y. T. Hu, C. Soto, A. C. Chan, and M. L. Thomas. 1999. Expression of dominant-negative src-homology domain 2- containing protein tyrosine phosphatase-1 results in increased Syk tyrosine kinase activity and B cell activation. J. Immunol. 162: 2717-2724. (Pubitemid 29309294)
75. Somani, A. K., K. Yuen, F. Xu, J. Zhang, D. R. Branch, and K. A. Siminovitch. 2001. The SH2 domain containing tyrosine phosphatase-1 down-regulates activation of Lyn and Lyn-induced tyrosine phosphorylation of the CD19 receptor in B cells. J. Biol. Chem. 276: 1938-1944. (Pubitemid 32109671)
76. Lu, R., G. S. Vidal, J. A. Kelly, A. M. Delgado-Vega, X. K. Howard, S. R. Macwana, N. Dominguez, W. Klein, C. Burrell, I. T. Harley, et al. 2009. Genetic associations of LYN with systemic lupus erythematosus. Genes Immun. 10: 397-403.
77. Harley, J. B., M. E. Alarcón-Riquelme, L. A. Criswell, C. O. Jacob, R. P. Kimberly, K. L. Moser, B. P. Tsao, T. J. Vyse, C. D. Langefeld, S. K. Nath, et al. 2008. Genome-wide association scan in women with systemic lupus erythematosus identifies susceptibility variants in ITGAM, PXK, KIAA1542 and other loci. Nat. Genet. 40: 204-210. (Pubitemid 351171405)
78. Han, J. W., H. F. Zheng, Y. Cui, L. D. Sun, D. Q. Ye, Z. Hu, J. H. Xu, Z. M. Cai, W. Huang, G. P. Zhao, et al. 2009. Genome-wide association study in a Chinese Han population identifies nine new susceptibility loci for systemic lupus erythematosus. Nat. Genet. 41: 1234-1237.
79. Okada, Y., C. Terao, K. Ikari, Y. Kochi, K. Ohmura, A. Suzuki, T. Kawaguchi, E. A. Stahl, F. A. Kurreeman, N. Nishida, et al. 2012. Meta-analysis identifies nine new loci associated with rheumatoid arthritis in the Japanese population. Nat. Genet. 44: 511-516.
80. Tsoi, L. C., S. L. Spain, J. Knight, E. Ellinghaus, P. E. Stuart, F. Capon, J. Ding, Y. Li, T. Tejasvi, J. E. Gudjonsson, et al. 2012. Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat. Genet. 44: 1341-1348.
81. Li, Y., L. D. Sun, W. S. Lu, W. L. Hu, J. P. Gao, Y. L. Cheng, Z. Y. Yu, S. Yao, C. F. He, J. L. Liu, et al. 2010. Expression analysis of ETS1 gene in peripheral blood mononuclear cells with systemic lupus erythematosus by real-time reverse transcription PCR. Chin. Med. J. (Engl.) 123: 2287-2288.
82. Du, C., C. Liu, J. Kang, G. Zhao, Z. Ye, S. Huang, Z. Li, Z. Wu, and G. Pei. 2009. MicroRNA miR-326 regulates TH-17 differentiation and is associated with the pathogenesis of multiple sclerosis. Nat. Immunol. 10: 1252-1259.
83. + T regulatory cells from patients with systemic lupus erythematosus. Clin. Exp. Med. In press.
84. Franch, H. A., S. Sooparb, J. Du, and N. S. Brown. 2001. A mechanism regulating proteolysis of specific proteins during renal tubular cell growth. J. Biol. Chem. 276: 19126-19131.