CD73 expression is dynamically regulated in the germinal center and bone marrow plasma cells are diminished in its absence

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Conter, Laura J ^a   Song, Eunice ^a   Shlomchik, Mark J ^a   Tomayko, Mary M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ARTICLE; B LYMPHOCYTE; BONE MARROW; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; GENE DELETION; GERMINAL CENTER; HELPER CELL; HUMORAL IMMUNITY; IMMUNIZATION; INTRACELLULAR SPACE; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PLASMA CELL; PLASMABLAST; SIGNAL TRANSDUCTION; SPLEEN CELL; T LYMPHOCYTE; UPREGULATION; ANIMAL; C57BL MOUSE; CELL SIZE; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; KINETICS; METABOLISM; SPLEEN;

5'-NUCLEOTIDASE; ANIMALS; BONE MARROW; CELL SIZE; GENE EXPRESSION REGULATION; GERMINAL CENTER; IMMUNITY, HUMORAL; IMMUNIZATION; KINETICS; MICE; MICE, INBRED C57BL; PLASMA CELLS; SPLEEN;

EID: 84899765944     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092009     Document Type: Article

References (55)

1. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362: 299-309.
2. Bours MJ, Swennen EL, Di Virgilio F, Cronstein BN, Dagnelie PC (2006) Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation. Pharmacol Ther 112: 358-404. (Pubitemid 44486409)
3. Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783: 673-694.
4. Regateiro FS, Cobbold SP, Waldmann H (2013) CD73 and adenosine generation in the creation of regulatory microenvironments. Clin Exp Immunol 171: 1-7.
5. Thompson LF, Eltzschig HK, Ibla JC, Van De Wiele CJ, Resta R, et al. (2004) Crucial role for ecto-5′-nucleotidase (CD73) in vascular leakage during hypoxia. J Exp Med 200: 1395-1405. (Pubitemid 39657287)
6. Volmer JB, Thompson LF, Blackburn MR (2006) Ecto-5′-nucleotidase (CD73)-mediated adenosine production is tissue protective in a model of bleomycin-induced lung injury. J Immunol 176: 4449-4458. (Pubitemid 44264425)
7. Yegutkin GG, Hytonen J, Samburski SS, Yrjanainen H, Jalkanen S, et al. (2010) Disordered lymphoid purine metabolism contributes to the pathogenesis of persistent Borrelia garinii infection in mice. J Immunol 184: 5112-5120.
8. Hasko G, Csoka B, Koscso B, Chandra R, Pacher P, et al. (2011) Ecto-5′-nucleotidase (CD73) decreases mortality and organ injury in sepsis. J Immunol 187: 4256-4267.
9. Huang S, Apasov S, Koshiba M, Sitkovsky M (1997) Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 90: 1600-1610. (Pubitemid 27355433)
10. Kumar V, Sharma A (2009) Adenosine: an endogenous modulator of innate immune system with therapeutic potential. Eur J Pharmacol 616: 7-15.
11. Deaglio S, Dwyer KM, Gao W, Friedman D, Usheva A, et al. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204: 1257-1265. (Pubitemid 46919862)
12. Borsellino G, Kleinewietfeld M, Di Mitri D, Sternjak A, Diamantini A, et al. (2007) Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression. Blood 110: 1225-1232. (Pubitemid 47281420)
13. Mandapathil M, Hilldorfer B, Szczepanski MJ, Czystowska M, Szajnik M, et al. (2010) Generation and accumulation of immunosuppressive adenosine by human CD4+CD25highFOXP3+ regulatory T cells. J Biol Chem 285: 7176-7186.
14. Romio M, Reinbeck B, Bongardt S, Huls S, Burghoff S, et al. (2011) Extracellular purine metabolism and signaling of CD73-derived adenosine in murine Treg and Teff cells. Am J Physiol Cell Physiol 301: C530-539.
15. Jin D, Fan J, Wang L, Thompson LF, Liu A, et al. (2010) CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res 70: 2245-2255.
16. Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z (2011) Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 187: 676-683.
17. Ohta A, Gorelik E, Prasad SJ, Ronchese F, Lukashev D, et al. (2006) A2A adenosine receptor protects tumors from antitumor T cells. Proc Natl Acad Sci U S A 103: 13132-13137. (Pubitemid 44338928)
18. Stagg J, Divisekera U, Duret H, Sparwasser T, Teng MW, et al. (2011) CD73-deficient mice have increased antitumor immunity and are resistant to experimental metastasis. Cancer Res 71: 2892-2900.
19. Stagg J, Divisekera U, McLaughlin N, Sharkey J, Pommey S, et al. (2010) Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci U S A 107: 1547-1552.
20. Tomayko MM, Steinel NC, Anderson SM, Shlomchik MJ (2010) Cutting edge: Hierarchy of maturity of murine memory B cell subsets. J Immunol 185: 7146-7150.
21. Bastian JF, Ruedi JM, MacPherson GA, Golembesky HE, O'Connor RD, et al. (1984) Lymphocyte ecto-5′-nucleotidase activity in infancy: increasing activity in peripheral blood B cells precedes their ability to synthesize IgG in vitro. J Immunol 132: 1767-1772. (Pubitemid 14171441)
22. Yamashita Y, Hooker SW, Jiang H, Laurent AB, Resta R, et al. (1998) CD73 expression and fyn-dependent signaling on murine lymphocytes. Eur J Immunol 28: 2981-2990. (Pubitemid 28470244)
23. Resta R, Yamashita Y, Thompson LF (1998) Ecto-enzyme and signaling functions of lymphocyte CD73. Immunol Rev 161: 95-109.
24. Taylor JJ, Pape KA, Jenkins MK (2012) A germinal center-independent pathway generates unswitched memory B cells early in the primary response. J Exp Med 209: 597-606.
25. Kaji T, Ishige A, Hikida M, Taka J, Hijikata A, et al. (2012) Distinct cellular pathways select germline-encoded and somatically mutated antibodies into immunological memory. J Exp Med 209: 2079-2097.
26. Castrop H, Huang Y, Hashimoto S, Mizel D, Hansen P, et al. (2004) Impairment of tubuloglomerular feedback regulation of GFR in ecto-5′-nucleotidase/CD73-deficient mice. J Clin Invest 114: 634-642. (Pubitemid 39578753)
27. Tomayko MM, Anderson SM, Brayton CE, Sadanand S, Steinel NC, et al. (2008) Systematic comparison of gene expression between murine memory and naive B cells demonstrates that memory B cells have unique signaling capabilities. J Immunol 181: 27-38.
28. Scholz JL, Crowley JE, Tomayko MM, Steinel N, O'Neill PJ, et al. (2008) BLyS inhibition eliminates primary B cells but leaves natural and acquired humoral immunity intact. Proc Natl Acad Sci U S A 105: 15517-15522.
29. Shlomchik MJ, Zharhary D, Saunders T, Camper SA, Weigert MG (1993) A rheumatoid factor transgenic mouse model of autoantibody regulation. Int Immunol 5: 1329-1341. (Pubitemid 23308094)
30. Allman DM, Ferguson SE, Lentz VM, Cancro MP (1993) Peripheral B cell maturation. II. Heat-stable antigen(hi) splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J Immunol 151: 4431-4444. (Pubitemid 23318496)
31. Anderson SM, Khalil A, Uduman M, Hershberg U, Louzoun Y, et al. (2009) Taking advantage: high-affinity B cells in the germinal center have lower death rates, but similar rates of division, compared to low-affinity cells. J Immunol 183: 7314-7325.
32. Anderson SM, Tomayko MM, Ahuja A, Haberman AM, Shlomchik MJ (2007) New markers for murine memory B cells that define mutated and unmutated subsets. J Exp Med 204: 2103-2114. (Pubitemid 47360872)
33. Hershberg U, Uduman M, Shlomchik MJ, Kleinstein SH (2008) Improved methods for detecting selection by mutation analysis of Ig V region sequences. Int Immunol 20: 683-694. (Pubitemid 351619236)
34. Regateiro FS, Howie D, Nolan KF, Agorogiannis EI, Greaves DR, et al. (2011) Generation of anti-inflammatory adenosine by leukocytes is regulated by TGF-beta. Eur J Immunol 41: 2955-2965.
35. Kobie JJ, Shah PR, Yang L, Rebhahn JA, Fowell DJ, et al. (2006) T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5′-adenosine monophosphate to adenosine. J Immunol 177: 6780-6786. (Pubitemid 44715042)
36. Crotty S (2011) Follicular helper CD4 T cells (TFH). Annu Rev Immunol 29: 621-663.
37. Shlomchik MJ, Weisel F (2012) Germinal center selection and the development of memory B and plasma cells. Immunol Rev 247: 52-63.
38. Takahashi Y, Ohta H, Takemori T (2001) Fas is required for clonal selection in germinal centers and the subsequent establishment of the memory B cell repertoire. Immunity 14: 181-192. (Pubitemid 32206520)
39. Pabst O, Peters T, Czeloth N, Bernhardt G, Scharffetter-Kochanek K, et al. (2005) Cutting edge: egress of newly generated plasma cells from peripheral lymph nodes depends on beta 2 integrin. J Immunol 174: 7492-7495. (Pubitemid 40806251)
40. Hargreaves DC, Hyman PL, Lu TT, Ngo VN, Bidgol A, et al. (2001) A coordinated change in chemokine responsiveness guides plasma cell movements. J Exp Med 194: 45-56. (Pubitemid 32660436)
41. Cyster JG (2003) Homing of antibody secreting cells. Immunol Rev 194: 48-60.
42. Chu VT, Frohlich A, Steinhauser G, Scheel T, Roch T, et al. (2011) Eosinophils are required for the maintenance of plasma cells in the bone marrow. Nat Immunol 12: 151-159.
43. Rodriguez Gomez M, Talke Y, Goebel N, Hermann F, Reich B, et al. (2010) Basophils support the survival of plasma cells in mice. J Immunol 185: 7180-7185.
44. Reutershan J, Vollmer I, Stark S, Wagner R, Ngamsri KC, et al. (2009) Adenosine and inflammation: CD39 and CD73 are critical mediators in LPS-induced PMN trafficking into the lungs. FASEB J 23: 473-482.
45. Algars A, Karikoski M, Yegutkin GG, Stoitzner P, Niemela J, et al. (2011) Different role of CD73 in leukocyte trafficking via blood and lymph vessels. Blood 117: 4387-4393.
46. Kiss J, Yegutkin GG, Koskinen K, Savunen T, Jalkanen S, et al. (2007) IFN-beta protects from vascular leakage via up-regulation of CD73. Eur J Immunol 37: 3334-3338.
47. Khalil AM, Cambier JC, Shlomchik MJ (2012) B cell receptor signal transduction in the GC is short-circuited by high phosphatase activity. Science 336: 1178-1181.
48. Good-Jacobson KL, Szumilas CG, Chen L, Sharpe HH, Tomayko MM, et al. (2010) PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nature Immunol 11: 535-543.
49. Anderson SM, Tomayko MM, Shlomchik MJ (2006) Intrinsic properties of human and murine memory B cells. Immunol Rev 211: 280-294. (Pubitemid 43882979)
50. Kunkel EJ, Butcher EC (2003) Plasma-cell homing. Nat Rev Immunol 3: 822-829. (Pubitemid 37328660)
51. Takedachi M, Oohara H, Smith BJ, Iyama M, Kobashi M, et al. (2012) CD73-generated adenosine promotes osteoblast differentiation. J Cell Physiol 227: 2622-2631.
52. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, et al. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8: 315-317. (Pubitemid 44269669)
53. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9: 641-650.
54. Stewart M, Talks K, Leek R, Turley H, Pezzella F, et al. (2002) Expression of angiogenic factors and hypoxia inducible factors HIF 1, HIF 2 and CA IX in non-Hodgkin's lymphoma. Histopathology 40: 253-260. (Pubitemid 34227116)
55. Synnestvedt K, Furuta GT, Comerford KM, Louis N, Karhausen J, et al. (2002) Ecto-5′-nucleotidase (CD73) regulation by hypoxia-inducible factor-1 mediates permeability changes in intestinal epithelia. J Clin Invest 110: 993-1002.