Germinal centre protein HGAL promotes lymphoid hyperplasia and amyloidosis via BCR-mediated Syk activation

Nature Communications

Volumn 4, Issue , 2013, Pages

  Romero Camarero, Isabel ^a,b   Jiang, Xiaoyu ^c   Natkunam, Yasodha ^d   Lu, Xiaoqing ^c   Vicente Dueñas, Carolina ^a,b   Gonzalez Herrero, Ines ^a,b   Flores, Teresa ^a,b   Garcia, Juan Luis ^a,b   McNamara, George ^c   Kunder, Christian ^d   Zhao, Shuchun ^d   Segura, Victor ^e   Fontan, Lorena ^e   Martínez Climent, Jose A ^e   García Criado, Francisco Javier ^a   Theis, Jason D ^f   Dogan, Ahmet ^f   Campos Sánchez, Elena ^g   Green, Michael R ^d   Alizadeh, Ash A ^d   Cobaleda, Cesar ^g   Sánchez García, Isidro ^a,b   Lossos, Izidore S ^c   more..

^a UNIVERSITY OF SALAMANCA   (Spain)

^b INSTITUTO DE INVESTIGACIÓN BIOMÉDICA DE SALAMANCA IBSAL   (Spain)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF NAVARRA   (Spain)

^f MAYO CLINIC   (United States)

^g UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; AMYLOID A PROTEIN; APOLIPOPROTEIN A1; APOLIPOPROTEIN A2; APOLIPOPROTEIN A4; APOLIPOPROTEIN E; B LYMPHOCYTE RECEPTOR; BREAST CANCER RESISTANCE PROTEIN; CD5 ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; COMPLEMENTARY DNA; HUMAN GERMINAL CENTRE ASSOCIATED LYMPHOMA PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN HEAVY CHAIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C; PROTEIN KINASE SYK; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SERUM AMYLOID A; SERUM AMYLOID A2; SERUM AMYLOID P; SIGNAL PEPTIDE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NFAT; TUMOR PROTEIN; UNCLASSIFIED DRUG; CELL EXTRACT; GCET2 PROTEIN, HUMAN; LY ANTIGEN; LY6A PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; PROTEIN TYROSINE KINASE; SAA2 PROTEIN, MOUSE; TRANSCRIPTOME;

DISEASE CONTROL; ENZYME ACTIVITY; HEALTH CARE; HUMAN GEOGRAPHY; PROTEIN; RODENT; SIGNALING;

AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EX VIVO STUDY; FLOW CYTOMETRY; GENE FUNCTION; GERMINAL CENTER; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; HYPERGAMMAGLOBULINEMIA; HYPOTHESIS; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOGLOBULIN HEAVY CHAIN GENE; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; LIQUID CHROMATOGRAPHY; LYMPHOCYTE PROLIFERATION; LYMPHOID HYPERPLASIA; LYMPHOMA CELL LINE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RAJI CELL; REPORTER GENE; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING; SPLEEN CELL; TANDEM MASS SPECTROMETRY; TRANSGENIC MOUSE; AMINO ACID SEQUENCE; ANIMAL; B CELL LYMPHOMA; CHEMISTRY; DISEASE MODEL; ENZYMOLOGY; GENETICS; HYPERPLASIA; INTRACELLULAR SPACE; KAPLAN MEIER METHOD; METABOLISM; MOLECULAR GENETICS; PATHOLOGY; PROTEIN BINDING; SPLEEN;

AMINO ACID SEQUENCE; AMYLOIDOSIS; ANIMALS; ANTIGENS, LY; CELL EXTRACTS; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; GERMINAL CENTER; HUMANS; HYPERGAMMAGLOBULINEMIA; HYPERPLASIA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SPACE; KAPLAN-MEIER ESTIMATE; LYMPHOMA, B-CELL; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; RECEPTORS, ANTIGEN, B-CELL; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SERUM AMYLOID A PROTEIN; SIGNAL TRANSDUCTION; SPLEEN; TRANSCRIPTOME;

MLCS; MLOWN;

EID: 84878539934     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2334     Document Type: Article

References (42)

1. Lossos, I. S., Alizadeh, A. A., Rajapaksa, R., Tibshirani, R. & Levy, R. HGAL is a novel interleukin-4-inducible gene that strongly predicts survival in diffuse large B-cell lymphoma. Blood 101, 433-440 (2003). (Pubitemid 36077560)
2. Pan, Z. et al. Studies of a germinal centre B-cell expressed gene, GCET2, suggest its role as a membrane associated adapter protein. Br. J. Haematol. 137, 578-590 (2007). (Pubitemid 46817334)
3. Natkunam, Y. et al. Expression of the human germinal center-associated lymphoma (HGAL) protein, a new marker of germinal center B-cell derivation. Blood 105, 3979-3986 (2005). (Pubitemid 40656146)
4. Natkunam, Y. et al. Expression of the human germinal center-associated lymphoma (HGAL) protein identifies a subset of classic Hodgkin lymphoma of germinal center derivation and improved survival. Blood 109, 298-305 (2007). (Pubitemid 46053070)
5. Schenten, D., Egert, A., Pasparakis, M. & Rajewsky, K. M17, a gene specific for germinal center (GC) B cells and a prognostic marker for GC B-cell lymphomas, is dispensable for the GC reaction in mice. Blood 107, 4849-4856 (2006). (Pubitemid 43882637)
6. Lu, X. et al. HGAL, a lymphoma prognostic biomarker, interacts with the cytoskeleton and mediates the effects of IL-6 on cell migration. Blood 110, 4268-4277 (2007). (Pubitemid 351377791)
7. Jiang, X. et al. HGAL, a germinal center specific protein, decreases lymphoma cell motility by modulation of the RhoA signaling pathway. Blood 116, 5217-5227 (2010).
8. Lu, X. et al. Germinal center-specific protein human germinal center associated lymphoma directly interacts with both myosin and actin and increases the binding of myosin to actin. FEBS. J. 278, 1922-1931 (2011).
9. Niiro, H. & Clark, E. A. Regulation of B-cell fate by antigen-receptor signals. Nat. Rev. Immunol. 2, 945-956 (2002). (Pubitemid 37323215)
10. Sada, K., Takano, T., Yanagi, S. & Yamamura, H. Structure and function of Syk protein-tyrosine kinase. J. Biochem. 130, 177-186 (2001). (Pubitemid 32785863)
11. Turner, M. et al. Perinatal lethality and blocked B-cell development in mice lacking the tyrosine kinase Syk. Nature 378, 298-302 (1995).
12. Cheng, A. M. et al. Syk tyrosine kinase required for mouse viability and B-cell development. Nature 378, 303-306 (1995).
13. Koretzky, G. A., Abtahian, F. & Silverman, M. A. SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond. Nat. Rev. Immunol. 6, 67-78 (2006). (Pubitemid 43279754)
14. Jiang, A., Craxton, A., Kurosaki, T. & Clark, E. A. 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 (1998). (Pubitemid 28478018)
15. Miles, C., Sanchez, M. J., Sinclair, A. & Dzierzak, E. Expression of the Ly-6E.1 (Sca-1) transgene in adult hematopoietic stem cells and the developing mouse embryo. Development 124, 537-547 (1997). (Pubitemid 27101687)
16. Fossati, V., Kumar, R. & Snoeck, H. W. Progenitor cell origin plays a role in fate choices of mature B cells. J. Immunol. 184, 1251-1260 (2010).
17. Perez-Caro, M. et al. Cancer induction by restriction of oncogene expression to the stem cell compartment. EMBO. J. 28, 8-20 (2009).
18. Vicente-Dueñasa, C. et al. Expression of MALT1 oncogene in hematopoietic stem/progenitor cells recapitulates the pathogenesis of human lymphoma in mice. Proc. Natl Acad. Sci. USA 109, 10534-10539 (2012).
19. Vicente-Duenas, C. et al. A novel molecular mechanism involved in multiple myeloma development revealed by targeting MafB to haematopoietic progenitors. EMBO. J. 31, 3704-3717 (2012).
20. van der Hilst, J. C. Recent insights into the pathogenesis of type AA amyloidosis. ScientificWorld Journal 11, 641-650 (2011).
21. Tusher, V. G., Tibshirani, R. & Chu, G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl Acad. Sci. USA 98, 5116-5121 (2001). (Pubitemid 32397092)
22. Green, M. R. et al. Signatures of murine B-cell development implicate Yy1 as a regulator of the germinal center-specific program. Proc. Natl Acad Sci. USA 108, 2873-2878 (2011).
23. Boylan, K. L. M. et al. A transgenic mouse model of plasma cell malignancy shows phenotypic, cytogenetic, and gene expression heterogeneity similar to human multiple myeloma. Cancer. Res. 67, 4069-4078 (2007). (Pubitemid 46815051)
24. Pasqualucci, L. et al. AID is required for germinal center-derived lymphomagenesis. Nat. Genet. 40, 108-112 (2008).
25. Marshall, A. J. et al. A novel B lymphocyte-associated adaptor protein, Bam32, regulates antigen receptor signaling downstream of phosphatidylinositol 3-kinase. J. Exp. Med. 191, 1319-1332 (2000).
26. Shlapatska, L. M. et al. CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J. Immunol. 166, 5480-5487 (2001). (Pubitemid 32374169)
27. Kojima, M., Motoori, T. & Nakamura, S. Benign, atypical and malignant lymphoproliferative disorders in rheumatoid arthritis patients. Biomed. Pharmacother. 60, 663-672 (2006). (Pubitemid 44822653)
28. Solomon, A. et al. Transgenic mouse model of AA amyloidosis. Am. J. Pathol. 154, 1267-1272 (1999). (Pubitemid 29169760)
29. Ray, A., Shakya, A., Kumar, D., Benson, M. D. & Ray, B. K. Inflammation-responsive transcription factor SAF-1 activity is linked to the development of amyloid A amyloidosis. J. Immunol. 177, 2601-2609 (2006). (Pubitemid 44201019)
30. McDonnell, T. J. et al. Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell 57, 79-88 (1989). (Pubitemid 19098870)
31. Xiang, H. et al. The immunoglobulin heavy chain gene 3' enhancers induce Bcl2 deregulation and lymphomagenesis in murine B cells. Leukemia 25, 1484-1493 (2011).
32. Egle, A., Harris, A. W., Bath, M. L., O'Reilly, L. & Cory, S. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood 103, 2276-2283 (2004). (Pubitemid 38326247)
33. Strasser, A. et al. Enforced BCL2 expression in B-lymphoid cells prolongs antibody responses and elicits autoimmune disease. Proc. Natl Acad. Sci. USA 88, 8661-8665 (1991). (Pubitemid 21915417)
34. Refaeli, Y. et al. The B cell antigen receptor and overexpression of MYC can cooperate in the genesis of B cell lymphomas. PLoS. Biol. 6, e152 (2008).
35. Sarosiek, K. A. et al. Novel IL-21 signaling pathway up-regulates c-Myc and induces apoptosis of diffuse large B-cell lymphomas. Blood 115, 570-580 (2010).
36. Camper, S. A. Research applications of transgenic mice. Biotechniques 5, 638-650 (1987). (Pubitemid 18016243)
37. Kwon, K. et al. Instructive role of the transcription factor E2A in early B lymphopoiesis and germinal center B cell development. Immunity 28, 751-762 (2008).
38. Willig, K. I., Harke, B., Medda, R. & Hell, S. W. STED microscopy with continuous wave beams. Nat. Methods 4, 915-918 (2007). (Pubitemid 350042378)
39. Dai, M. et al. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33, e175 (2005).
40. Irizarry, R. A. et al. Summaries of affymetrix genechip probe level data. Nucleic Acids Res. 31, e15 (2003).
41. Dennis, Jr G. et al. DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3 (2003).
42. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005). (Pubitemid 41528093)