Lysophosphatidic acid receptor 5 inhibits B cell antigen receptor signaling and antibody response

Journal of Immunology

Volumn 193, Issue 1, 2014, Pages 85-95

  Hu, Jiancheng ^a,d   Oda, Shannon K ^a,e   Shotts, Kristin ^a   Donovan, Erin E ^a   Strauch, Pamela ^a   Pujanauski, Lindsey M ^a,f   Victorino, Francisco ^a   Al Shami, Amin ^b   Fujiwara, Yuko ^c   Tigyi, Gabor ^c   Oravecz, Tamas ^b   Pelanda, Roberta ^a   Torres, Raul M ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b LEXICON PHARMACEUTICALS INC   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^d WASHINGTON UNIVERSITY   (United States)

^e Fred Hutchinson Cancer Research Center   (United States)

^f NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; B LYMPHOCYTE ANTIGEN RECEPTOR; CD69 ANTIGEN; CD86 ANTIGEN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR; LYSOPHOSPHATIDIC ACID RECEPTOR 5; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE ACTIVATION; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL MATURATION; CONTROLLED STUDY; FEMALE; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODY FORMATION; ANTIGENS, CD; ANTIGENS, CD86; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; B-LYMPHOCYTES; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; IMMUNITY, HUMORAL; LECTINS, C-TYPE; MICE; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, B-CELL; RECEPTORS, LYSOPHOSPHATIDIC ACID; SIGNAL TRANSDUCTION;

EID: 84903635470     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300429     Document Type: Article

References (63)

1. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature 381: 751-758. (Pubitemid 26243107)
2. Meffre, E., R. Casellas, and M. C. Nussenzweig. 2000. Antibody regulation of B cell development. Nat. Immunol. 1: 379-385.
3. Buhl, A. M., and J. C. Cambier. 1997. Co-receptor and accessory regulation of B-cell antigen receptor signal transduction. Immunol. Rev. 160: 127-138. (Pubitemid 28021372)
4. Rickert, R. C. 2005. Regulation of B lymphocyte activation by complement C3 and the B cell coreceptor complex. Curr. Opin. Immunol. 17: 237-243.
5. Dempsey, P. W., M. E. Allison, S. Akkaraju, C. C. Goodnow, and D. T. Fearon. 1996. C3d of complement as a molecular adjuvant: bridging innate and acquired immunity. Science 271: 348-350.
6. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcgamma receptors: old friends and new family members. Immunity 24: 19-28. (Pubitemid 43077197)
7. Dorsam, G., M. H. Graeler, C. Seroogy, Y. Kong, J. K. Voice, and E. J. Goetzl. 2003. Transduction of multiple effects of sphingosine 1-phosphate (S1P) on T cell functions by the S1P1 G protein-coupled receptor. J. Immunol. 171: 3500-3507. (Pubitemid 37254552)
8. Kumar, A., T. D. Humphreys, K. N. Kremer, P. S. Bramati, L. Bradfield, C. E. Edgar, and K. E. Hedin. 2006. CXCR4 physically associates with the T cell receptor to signal in T cells. Immunity 25: 213-224. (Pubitemid 44224150)
9. Gold, M. R., J. P. Jakway, and A. L. DeFranco. 1987. Involvement of a guaninenucleotide- binding component in membrane IgM-stimulated phosphoinositide breakdown. J. Immunol. 139: 3604-3613. (Pubitemid 18013630)
10. Harnett, M. M., and G. G. Klaus. 1988. G protein coupling of antigen receptorstimulated polyphosphoinositide hydrolysis in B cells. J. Immunol. 140: 3135- 3139.
11. Blaho, V. A., and T. Hla. 2011. Regulation of mammalian physiology, development, and disease by the sphingosine 1-phosphate and lysophosphatidic acid receptors. Chem. Rev. 111: 6299-6320.
12. Allende, M. L., G. Tuymetova, B. G. Lee, E. Bonifacino, Y. P. Wu, and R. L. Proia. 2010. S1P1 receptor directs the release of immature B cells from bone marrow into blood. J. Exp. Med. 207: 1113-1124.
13. Donovan, E. E., R. Pelanda, and R. M. Torres. 2010. S1P3 confers differential S1P-induced migration by autoreactive and non-autoreactive immature B cells and is required for normal B-cell development. Eur. J. Immunol. 40: 688-698.
14. Pereira, J. P., Y. Xu, and J. G. Cyster. 2010. A role for S1P and S1P1 in immature- B cell egress from mouse bone marrow. PLoS ONE 5: e9277.
15. Rosen, H., P. Gonzalez-Cabrera, D. Marsolais, S. Cahalan, A. S. Don, and M. G. Sanna. 2008. Modulating tone: the overture of S1P receptor immunotherapeutics. Immunol. Rev. 223: 221-235. (Pubitemid 351986190)
16. Cyster, J. G., and S. R. Schwab. 2012. Sphingosine-1-phosphate and lymphocyte egress from lymphoid organs. Annu. Rev. Immunol. 30: 69-94.
17. Choi, J. W., D. R. Herr, K. Noguchi, Y. C. Yung, C. W. Lee, T. Mutoh, M. E. Lin, S. T. Teo, K. E. Park, A. N. Mosley, and J. Chun. 2010. LPA receptors: subtypes and biological actions. Annu. Rev. Pharmacol. Toxicol. 50: 157-186.
18. Tigyi, G. 2010. Aiming drug discovery at lysophosphatidic acid targets. Br. J. Pharmacol. 161: 241-270.
19. Baker, D. L., P. Morrison, B. Miller, C. A. Riely, B. Tolley, A. M. Westermann, J. M. Bonfrer, E. Bais, W. H. Moolenaar, and G. Tigyi. 2002. Plasma lysophosphatidic acid concentration and ovarian cancer. JAMA 287: 3081-3082. (Pubitemid 34633980)
20. Smyth, S. S., H. Y. Cheng, S. Miriyala, M. Panchatcharam, and A. J. Morris. 2008. Roles of lysophosphatidic acid in cardiovascular physiology and disease. Biochim. Biophys. Acta 1781: 563-570.
21. Liu, S., M. Umezu-Goto, M. Murph, Y. Lu, W. Liu, F. Zhang, S. Yu, L. C. Stephens, X. Cui, G. Murrow, et al. 2009. Expression of autotaxin and lysophosphatidic acid receptors increases mammary tumorigenesis, invasion, and metastases. Cancer Cell 15: 539-550.
22. Mills, G. B., and W. H. Moolenaar. 2003. The emerging role of lysophosphatidic acid in cancer. Nat. Rev. Cancer 3: 582-591. (Pubitemid 37328830)
23. Watanabe, N., H. Ikeda, K. Nakamura, R. Ohkawa, Y. Kume, J. Aoki, K. Hama, S. Okudaira, M. Tanaka, T. Tomiya, et al. 2007. Both plasma lysophosphatidic acid and serum autotaxin levels are increased in chronic hepatitis C. J. Clin. Gastroenterol. 41: 616-623. (Pubitemid 46956520)
24. Fourcade, O., M. F. Simon, C. Viodé, N. Rugani, F. Leballe, A. Ragab, B. Fournié, L. Sarda, and H. Chap. 1995. Secretory phospholipase A2 generates the novel lipid mediator lysophosphatidic acid in membrane microvesicles shed from activated cells. Cell 80: 919-927.
25. Sonoda, E., Y. Pewzner-Jung, S. Schwers, S. Taki, S. Jung, D. Eilat, and K. Rajewsky. 1997. B cell development under the condition of allelic inclusion. Immunity 6: 225-233. (Pubitemid 27148589)
26. Rubtsov, A., P. Strauch, A. Digiacomo, J. Hu, R. Pelanda, and R. M. Torres. 2005. Lsc regulates marginal-zone B cell migration and adhesion and is required for the IgM T-dependent antibody response. Immunity 23: 527-538. (Pubitemid 41587892)
27. Contos, J. J., I. Ishii, N. Fukushima, M. A. Kingsbury, X. Ye, S. Kawamura, J. H. Brown, and J. Chun. 2002. Characterization of lpa(2) (Edg4) and lpa(1)/lpa (2) (Edg2/Edg4) lysophosphatidic acid receptor knockout mice: signaling deficits without obvious phenotypic abnormality attributable to lpa(2). Mol. Cell. Biol. 22: 6921-6929.
28. Wattler, S., M. Kelly, and M. Nehls. 1999. Construction of gene targeting vectors from lambda KOS genomic libraries. Biotechniques 26: 1150-1156, 1158, 1160.
29. Hu, J., P. Strauch, A. Rubtsov, E. E. Donovan, R. Pelanda, and R. M. Torres. 2008. Lsc activity is controlled by oligomerization and regulates integrin adhesion. Mol. Immunol. 45: 1825-1836.
30. Shin, K. J., E. A. Wall, J. R. Zavzavadjian, L. A. Santat, J. Liu, J. I. Hwang, R. Rebres, T. Roach, W. Seaman, M. I. Simon, and I. D. Fraser. 2006. A single lentiviral vector platform for microRNA-based conditional RNA interference and coordinated transgene expression. Proc. Natl. Acad. Sci. USA 103: 13759- 13764.
31. Halverson, R., R. M. Torres, and R. Pelanda. 2004. Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat. Immunol. 5: 645-650. (Pubitemid 38811890)
32. Swanson, C. L., T. J. Wilson, P. Strauch, M. Colonna, R. Pelanda, and R. M. Torres. 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. J. Exp. Med. 207: 1485-1500.
33. Goetzl, E. J., Y. Kong, and J. K. Voice. 2000. Cutting edge: differential constitutive expression of functional receptors for lysophosphatidic acid by human blood lymphocytes. J. Immunol. 164: 4996-4999. (Pubitemid 30305167)
34. Rubenfeld, J., J. Guo, N. Sookrung, R. Chen, W. Chaicumpa, V. Casolaro, Y. Zhao, V. Natarajan, and S. Georas. 2006. Lysophosphatidic acid enhances interleukin-13 gene expression and promoter activity in T cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 290: L66-L74.
35. Nam, J. H., D. H. Shin, J. E. Min, S. K. Ye, J. H. Jeon, and S. J. Kim. 2010. Ca2+ signaling induced by sphingosine 1-phosphate and lysophosphatidic acid in mouse B cells. Mol. Cells 29: 85-91.
36. Engelke, M., N. Engels, K. Dittmann, B. Stork, and J. Wienands. 2007. Ca(2+) signaling in antigen receptor-activated B lymphocytes. Immunol. Rev. 218: 235- 246. (Pubitemid 47052309)
37. Scharenberg, A. M., L. A. Humphries, and D. J. Rawlings. 2007. Calcium signalling and cell-fate choice in B cells. Nat. Rev. Immunol. 7: 778-789.
38. Hogan, P. G., R. S. Lewis, and A. Rao. 2010. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28: 491-533.
39. Irvine, R. F., and M. J. Schell. 2001. Back in the water: the return of the inositol phosphates. Nat. Rev. Mol. Cell Biol. 2: 327-338. (Pubitemid 33674045)
40. Cahalan, M. D. 2009. STIMulating store-operated Ca(2+) entry. Nat. Cell Biol. 11: 669-677.
41. Putney, J. W. 2009. Capacitative calcium entry: from concept to molecules. Immunol. Rev. 231: 10-22.
42. Lytton, J., M. Westlin, and M. R. Hanley. 1991. Thapsigargin inhibits the sarcoplasmic or endoplasmic reticulum Ca-ATPase family of calcium pumps. J. Biol. Chem. 266: 17067-17071. (Pubitemid 21907906)
43. Lee, C. W., R. Rivera, S. Gardell, A. E. Dubin, and J. Chun. 2006. GPR92 as a new G12/13- and Gq-coupled lysophosphatidic acid receptor that increases cAMP, LPA5. J. Biol. Chem. 281: 23589-23597. (Pubitemid 44274133)
44. Strathmann, M. P., and M. I. Simon. 1991. G alpha 12 and G alpha 13 subunits define a fourth class of G protein alpha subunits. Proc. Natl. Acad. Sci. USA 88: 5582-5586.
45. Fukuhara, S., H. Chikumi, and J. S. Gutkind. 2001. RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 20: 1661- 1668. (Pubitemid 32336855)
46. Cumano, A., and K. Rajewsky. 1985. Structure of primary anti-(4-hydroxy-3- nitrophenyl)acetyl (NP) antibodies in normal and idiotypically suppressed C57BL/6 mice. Eur. J. Immunol. 15: 512-520. (Pubitemid 15071585)
47. Williams, J. R., A. L. Khandoga, P. Goyal, J. I. Fells, D. H. Perygin, W. Siess, A. L. Parrill, G. Tigyi, and Y. Fujiwara. 2009. Unique ligand selectivity of the GPR92/LPA5 lysophosphatidate receptor indicates role in human platelet activation. J. Biol. Chem. 284: 17304-17319.
48. Kiss, G. N., J. I. Fells, R. Gupte, S. C. Lee, J. Liu, N. Nusser, K. G. Lim, R. M. Ray, F. T. Lin, A. L. Parrill, et al. 2012. Virtual screening for LPA2- specific agonists identifies a nonlipid compound with antiapoptotic actions. Mol. Pharmacol. 82: 1162-1173.
49. Guinamard, R., M. Okigaki, J. Schlessinger, and J. V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1: 31-36.
50. Otipoby, K. L., K. B. Andersson, K. E. Draves, S. J. Klaus, A. G. Farr, J. D. Kerner, R. M. Perlmutter, C. L. Law, and E. A. Clark. 1996. CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 384: 634-637.
51. Samardzic, T., D. Marinkovic, C. P. Danzer, J. Gerlach, L. Nitschke, and T. Wirth. 2002. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32: 561-567. (Pubitemid 34173347)
52. Shih, T. A., M. Roederer, and M. C. Nussenzweig. 2002. Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 3: 399-406. (Pubitemid 34308629)
53. Oda, S. K., P. Strauch, Y. Fujiwara, A. Al-Shami, T. Oravecz, G. Tigyi, R. Pelanda, and R. M. Torres. 2013. Lysophosphatidic Acid inhibits CD8 T cell activation and control of tumor progression. Cancer Immunol. Res. 1: 245-255.
54. Dolmetsch, R. E., R. S. Lewis, C. C. Goodnow, and J. I. Healy. 1997. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386: 855-858. (Pubitemid 27181262)
55. Loh, C., J. A. Carew, J. Kim, P. G. Hogan, and A. Rao. 1996. T-cell receptor stimulation elicits an early phase of activation and a later phase of deactivation of the transcription factor NFAT1. Mol. Cell. Biol. 16: 3945-3954. (Pubitemid 26199914)
56. Oh-hora, M., and A. Rao. 2008. Calcium signaling in lymphocytes. Curr. Opin. Immunol. 20: 250-258.
57. Zeng, W., D. O. Mak, Q. Li, D. M. Shin, J. K. Foskett, and S. Muallem. 2003. A new mode of Ca2+ signaling by G protein-coupled receptors: gating of IP3 receptor Ca2+ release channels by Gbetagamma. Curr. Biol. 13: 872-876.
58. Mongini, P. K., D. L. Longo, and W. E. Paul. 1984. T cell regulation of immunoglobulin class expression in the B cell response to TNP-Ficoll: characterization of the T cell responsible for preferential enhancement of the IgG2a response. J. Immunol. 132: 1647-1653.
59. Hausmann, J., S. Kamtekar, E. Christodoulou, J. E. Day, T. Wu, Z. Fulkerson, H. M. Albers, L. A. van Meeteren, A. J. Houben, L. van Zeijl, et al. 2011. Structural basis of substrate discrimination and integrin binding by autotaxin. Nat. Struct. Mol. Biol. 18: 198-204.
60. Nishimasu, H., S. Okudaira, K. Hama, E. Mihara, N. Dohmae, A. Inoue, R. Ishitani, J. Takagi, J. Aoki, and O. Nureki. 2011. Crystal structure of autotaxin and insight into GPCR activation by lipid mediators. Nat. Struct. Mol. Biol. 18: 205-212.
61. Tabchy, A., G. Tigyi, and G. B. Mills. 2011. Location, location, location: a crystal-clear view of autotaxin saturating LPA receptors. Nat. Struct. Mol. Biol. 18: 117-118.
62. Wang, L., E. Knudsen, Y. Jin, S. Gessani, and A. A. Maghazachi. 2004. Lysophospholipids and chemokines activate distinct signal transduction pathways in T helper 1 and T helper 2 cells. Cell. Signal. 16: 991-1000. (Pubitemid 38798050)
63. Goetzl, E. J., and H. Rosen. 2004. Regulation of immunity by lysosphingolipids and their G protein-coupled receptors. J. Clin. Invest. 114: 1531-1537. (Pubitemid 40385541)