The emerging role of soluble HLA-G in the control of chemotaxis

Cytokine and Growth Factor Reviews

Volumn 25, Issue 3, 2014, Pages 327-335

  Morandi, Fabio ^a   Rouas Freiss, Nathalie ^b   Pistoia, Vito ^a  

^a G GASLINI INSTITUTE   (Italy)

^b SAINT LOUIS HOSPITAL   (France)

Author keywords

Chemokine receptors; Chemotaxis; HLA G

Indexed keywords

CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CHEMOKINE RECEPTOR CXCR5; CXCL13 CHEMOKINE; HLA G ANTIGEN;

ANTIBODY PRODUCTION; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGEN PRESENTING CELL; AUTOIMMUNE DISEASE; AUTOIMMUNITY; B LYMPHOCYTE DIFFERENTIATION; CELL MIGRATION; CELL POPULATION; CHEMOTAXIS; CYTOKINE RELEASE; DOWN REGULATION; EFFECTOR CELL; GERMINAL CENTER; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INFLAMMATION; INNATE IMMUNITY; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SHORT SURVEY; TUMOR MICROENVIRONMENT; VIRUS INFECTION; ANIMAL; B LYMPHOCYTE; CELL DIFFERENTIATION; IMMUNOLOGY; PATHOLOGY; SOLUBILITY;

ANIMALS; AUTOIMMUNE DISEASES; B-LYMPHOCYTES; CELL DIFFERENTIATION; CHEMOTAXIS; HLA-G ANTIGENS; HUMANS; NEOPLASMS; SOLUBILITY; VIRUS DISEASES;

EID: 84902077948     PISSN: 13596101     EISSN: 18790305     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2014.04.004     Document Type: Short Survey

References (102)

1. Le Bouteiller P., Lenfant F. Antigen-presenting function(s) of the non-classical HLA-E, -F and -G class I molecules: the beginning of a story. Res Immunol 1996, 147:301-313.
2. Kievits F., Ivanyi P., Krimpenfort P., Berns A., Ploegh H.L. HLA-restricted recognition of viral antigens in HLA transgenic mice. Nature 1987, 329:447-449.
3. Malnati M.S., Lusso P., Ciccone E., Moretta A., Moretta L., Long E.O. Recognition of virus-infected cells by natural killer cell clones is controlled by polymorphic target cell elements. J Exp Med 1993, 178:961-969.
4. Moretta A., Vitale M., Bottino C., Orengo A.M., Morelli L., Augugliaro R., et al. P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J Exp Med 1993, 178:597-604.
5. Braud V.M., Allan D.S., McMichael A.J. Functions of nonclassical MHC and non-MHC-encoded class I molecules. Curr Opin Immunol 1999, 11:100-108.
6. Pistoia V., Morandi F., Wang X., Ferrone S. Soluble HLA-G: are they clinically relevant?. Semin Cancer Biol 2007, 17:469-479.
7. Munz C., Stevanovic S., Rammensee H.G. Peptide presentation and NK inhibition by HLA-G. J Reprod Immunol 1999, 43:139-155.
8. Baudhuin J., Migraine J., Faivre V., Loumagne L., Lukaszewicz A.C., Payen D., et al. Exocytosis acts as a modulator of the ILT4-mediated inhibition of neutrophil functions. Proc Natl Acad Sci U S A 2013, 110:17957-17962.
9. Le Page M.E., Goodridge J.P., John E., Christiansen F.T., Witt C.S. Killer Ig-like receptor 2DL4 does not mediate NK cell IFN-gamma responses to soluble HLA-G preparations. J Immunol 2014, 192:732-740.
10. Lila N., Rouas-Freiss N., Dausset J., Carpentier A., Carosella E.D. Soluble HLA-G protein secreted by allo-specific CD4+ T cells suppresses the allo-proliferative response: a CD4+ T cell regulatory mechanism. Proc Natl Acad Sci U S A 2001, 98:12150-12155.
11. Le Gal F.A., Riteau B., Sedlik C., Khalil-Daher I., Menier C., Dausset J., et al. HLA-G-mediated inhibition of antigen-specific cytotoxic T lymphocytes. Int Immunol 1999, 11:1351-1356.
12. Fournel S., Aguerre-Girr M., Huc X., Lenfant F., Alam A., Toubert A., et al. Cutting edge: soluble HLA-G1 triggers CD95/CD95 ligand-mediated apoptosis in activated CD8+ cells by interacting with CD8. J Immunol 2000, 164:6100-6104.
13. Le Rond S., Azema C., Krawice-Radanne I., Durrbach A., Guettier C., Carosella E.D., et al. Evidence to support the role of HLA-G5 in allograft acceptance through induction of immunosuppressive/regulatory T cells. J Immunol 2006, 176:3266-3276.
14. Naji A., Menier C., Morandi F., Agaugue S., Maki G., Ferretti E., et al. Binding of HLA-G to ITIM-bearing Ig-like transcript 2 receptor suppresses B cell responses. J Immunol 2014, 192:1536-1546.
15. Pazmany L., Mandelboim O., Vales-Gomez M., Davis D.M., Reyburn H.T., Strominger J.L. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science 1996, 274:792-795.
16. Rouas-Freiss N., Marchal R.E., Kirszenbaum M., Dausset J., Carosella E.D. The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors?. Proc Natl Acad Sci U S A 1997, 94:5249-5254.
17. van der Meer A., Lukassen H.G., van Cranenbroek B., Weiss E.H., Braat D.D., van Lierop M.J., et al. Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod 2007, 13:123-133.
18. van der Meer A., Lukassen H.G., van Lierop M.J., Wijnands F., Mosselman S., Braat D.D., et al. Membrane-bound HLA-G activates proliferation and interferon-gamma production by uterine natural killer cells. Mol Hum Reprod 2004, 10:189-195.
19. Fons P., Chabot S., Cartwright J.E., Lenfant F., L'Faqihi F., Giustiniani J., et al. Soluble HLA-G1 inhibits angiogenesis through an apoptotic pathway and by direct binding to CD160 receptor expressed by endothelial cells. Blood 2006, 108:2608-2615.
20. Rouas-Freiss N., Goncalves R.M., Menier C., Dausset J., Carosella E.D. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc Natl Acad Sci U S A 1997, 94:11520-11525.
21. Rizzo R., Melchiorri L., Stignani M., Baricordi O.R. HLA-G expression is a fundamental prerequisite to pregnancy. Hum Immunol 2007, 68:244-250.
22. Moreau P., Adrian-Cabestre F., Menier C., Guiard V., Gourand L., Dausset J., et al. IL-10 selectively induces HLA-G expression in human trophoblasts and monocytes. Int Immunol 1999, 11:803-811.
23. Yang Y., Chu W., Geraghty D.E., Hunt J.S. Expression of HLA-G in human mononuclear phagocytes and selective induction by IFN-gamma. J Immunol 1996, 156:4224-4231.
24. Gros F., Sebti Y., de Guibert S., Branger B., Bernard M., Fauchet R., et al. Soluble HLA-G molecules increase during acute leukemia, especially in subtypes affecting monocytic and lymphoid lineages. Neoplasia 2006, 8:223-230.
25. Sebti Y., Le Friec G., Pangault C., Gros F., Drenou B., Guilloux V., et al. Soluble HLA-G molecules are increased in lymphoproliferative disorders. Hum Immunol 2003, 64:1093-1101.
26. Bamberger A.M., Jenatschke S., Schulte H.M., Loning T., Bamberger M.C. Leukemia inhibitory factor (LIF) stimulates the human HLA-G promoter in JEG3 choriocarcinoma cells. J Clin Endocrinol Metab 2000, 85:3932-3936.
27. Moreau P., Faure O., Lefebvre S., Ibrahim E.C., O'Brien M., Gourand L., et al. Glucocorticoid hormones upregulate levels of HLA-G transcripts in trophoblasts. Transplant Proc 2001, 33:2277-2280.
28. Tirado-Gonzalez I., Freitag N., Barrientos G., Shaikly V., Nagaeva O., Strand M., et al. Galectin-1 influences trophoblast immune evasion and emerges as a predictive factor for the outcome of pregnancy. Mol Hum Reprod 2013, 19:43-53.
29. Lopez A.S., Alegre E., LeMaoult J., Carosella E., Gonzalez A. Regulatory role of tryptophan degradation pathway in HLA-G expression by human monocyte-derived dendritic cells. Mol Immunol 2006, 43:2151-2160.
30. Chang C.C., Murphy S.P., Ferrone S. Differential in vivo and in vitro HLA-G expression in melanoma cells: potential mechanisms. Hum Immunol 2003, 64:1057-1063.
31. Mouillot G., Marcou C., Zidi I., Guillard C., Sangrouber D., Carosella E.D., et al. Hypoxia modulates HLA-G gene expression in tumor cells. Hum Immunol 2007, 68:277-285.
32. Morandi F., Ferretti E., Castriconi R., Dondero A., Petretto A., Bottino C., et al. Soluble HLA-G dampens CD94/NKG2A expression and function and differentially modulates chemotaxis and cytokine and chemokine secretion in CD56bright and CD56dim NK cells. Blood 2011, 118:5840-5850.
33. Morandi F., Ferretti E., Bocca P., Prigione I., Raffaghello L., Pistoia V. A novel mechanism of soluble HLA-G mediated immune modulation: downregulation of T cell chemokine receptor expression and impairment of chemotaxis. PLoS ONE 2010, 5:e11763.
34. Schall T.J., Bacon K.B. Chemokines, leukocyte trafficking, and inflammation. Curr Opin Immunol 1994, 6:865-873.
35. Baggiolini M. Chemotactic and inflammatory cytokines-CXC and CC proteins. Adv Exp Med Biol 1993, 351:1-11.
36. Kelvin D.J., Michiel D.F., Johnston J.A., Lloyd A.R., Sprenger H., Oppenheim J.J., et al. Chemokines and serpentines: the molecular biology of chemokine receptors. J Leukoc Biol 1993, 54:604-612.
37. Neel N.F., Schutyser E., Sai J., Fan G.H., Richmond A. Chemokine receptor internalization and intracellular trafficking. Cytokine Growth Factor Rev 2005, 16:637-658.
38. Locati M., Riboldi E., Otero K., Martinez F.O., Riva F., Perrier P., et al. Regulation of the chemokine system at the level of chemokine receptor expression and signaling activity. Immunobiology 2001, 204:536-542.
39. Zhu C.B., Wang C.X., Zhang X., Zhang J., Li W. Serum sHLA-G levels: a useful indicator in distinguishing colorectal cancer from benign colorectal diseases. Int J Cancer 2011, 128:617-622.
40. Wlasiuk P., Stec A., Piechnik A., Kaminska W., Dmoszynska A., Ksiazek A., et al. Expression of soluble HLA-G in multiple myeloma patients and patients with renal failure. Leuk Res 2012, 36:881-883.
41. Ugurel S., Rebmann V., Ferrone S., Tilgen W., Grosse-Wilde H., Reinhold U. Soluble human leukocyte antigen-G serum level is elevated in melanoma patients and is further increased by interferon-alpha immunotherapy. Cancer 2001, 92:369-376.
42. Morandi F., Levreri I., Bocca P., Galleni B., Raffaghello L., Ferrone S., et al. Human neuroblastoma cells trigger an immunosuppressive program in monocytes by stimulating soluble HLA-G release. Cancer Res 2007, 67:6433-6441.
43. Leleu X., Le Friec G., Facon T., Amiot L., Fauchet R., Hennache B., et al. Total soluble HLA class I and soluble HLA-G in multiple myeloma and monoclonal gammopathy of undetermined significance. Clin Cancer Res 2005, 11:7297-7303.
44. Cao M., Yie S.M., Liu J., Ye S.R., Xia D., Gao E. Plasma soluble HLA-G is a potential biomarker for diagnosis of colorectal, gastric, esophageal and lung cancer. Tissue Antigens 2011, 78:120-128.
45. Weng P.J., Fu Y.M., Ding S.X., Xu D.P., Lin A., Yan W.H. Elevation of plasma soluble human leukocyte antigen-G in patients with chronic hepatitis C virus infection. Hum Immunol 2011, 72:406-411.
46. Shi W.W., Lin A., Xu D.P., Bao W.G., Zhang J.G., Chen S.Y., et al. Plasma soluble human leukocyte antigen-G expression is a potential clinical biomarker in patients with hepatitis B virus infection. Hum Immunol 2011, 72:1068-1073.
47. Park Y., Lim H.S., Kim Y.S., Hong D.J., Kim H.S. Soluble human leukocyte antigen-G expression in hepatitis B virus infection and hepatocellular carcinoma. Tissue Antigens 2012, 79:97-103.
48. Han Q., Li N., Zhu Q., Li Z., Zhang G., Chen J., et al. Association of serum soluble human leukocyte antigen-G levels with chronic hepatitis B virus infection. Clin Exp Med 2012.
49. Donaghy L., Gros F., Amiot L., Mary C., Maillard A., Guiguen C., et al. Elevated levels of soluble non-classical major histocompatibility class I molecule human leucocyte antigen (HLA)-G in the blood of HIV-infected patients with or without visceral leishmaniasis. Clin Exp Immunol 2007, 147:236-240.
50. Rizzo R., Hviid T.V., Govoni M., Padovan M., Rubini M., Melchiorri L., et al. HLA-G genotype and HLA-G expression in systemic lupus erythematosus: HLA-G as a putative susceptibility gene in systemic lupus erythematosus. Tissue Antigens 2008, 71:520-529.
51. Borghi A., Fogli E., Stignani M., Melchiorri L., Altieri E., Baricordi O., et al. Soluble human leukocyte antigen-G and interleukin-10 levels in plasma of psoriatic patients: preliminary study on a possible correlation between generalized immune status, treatments and disease. Arch Dermatol Res 2008, 300:551-559.
52. Prigione I., Penco F., Martini A., Gattorno M., Pistoia V., Morandi F. HLA-G and HLA-E in patients with juvenile idiopathic arthritis. Rheumatology (Oxford) 2011, 50:966-972.
53. Rizzo R., Farina I., Bortolotti D., Galuppi E., Rotola A., Melchiorri L., et al. HLA-G may predict the disease course in patients with early rheumatoid arthritis. Hum Immunol 2013, 74:425-432.
54. Monneret G., Voirin N., Krawice-Radanne I., Bohe J., Lepape A., Rouas-Freiss N., et al. Soluble human leukocyte antigen-G5 in septic shock: marked and persisting elevation as a predictor of survival. Crit Care Med 2007, 35:1942-1947.
55. Qin S., Rottman J.B., Myers P., Kassam N., Weinblatt M., Loetscher M., et al. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J Clin Invest 1998, 101:746-754.
56. Maghazachi A.A. Role of chemokines in the biology of natural killer cells. Curr Top Microbiol Immunol 2010, 341:37-58.
57. Mullins I.M., Slingluff C.L., Lee J.K., Garbee C.F., Shu J., Anderson S.G., et al. CXC chemokine receptor 3 expression by activated CD8+ T cells is associated with survival in melanoma patients with stage III disease. Cancer Res 2004, 64:7697-7701.
58. Musha H., Ohtani H., Mizoi T., Kinouchi M., Nakayama T., Shiiba K., et al. Selective infiltration of CCR5(+)CXCR3(+) T lymphocytes in human colorectal carcinoma. Int J Cancer 2005, 116:949-956.
59. Cozar J.M., Canton J., Tallada M., Concha A., Cabrera T., Garrido F., et al. Analysis of NK cells and chemokine receptors in tumor infiltrating CD4T lymphocytes in human renal carcinomas. Cancer Immunol Immunother 2005, 54:858-866.
60. Wendel M., Galani I.E., Suri-Payer E., Cerwenka A. Natural killer cell accumulation in tumors is dependent on IFN-gamma and CXCR3 ligands. Cancer Res 2008, 68:8437-8445.
61. Winter D., Moser J., Kriehuber E., Wiesner C., Knobler R., Trautinger F., et al. Down-modulation of CXCR3 surface expression and function in CD8+ T cells from cutaneous T cell lymphoma patients. J Immunol 2007, 179:4272-4282.
62. Eriksson C., Eneslatt K., Ivanoff J., Rantapaa-Dahlqvist S., Sundqvist K.G. Abnormal expression of chemokine receptors on T-cells from patients with systemic lupus erythematosus. Lupus 2003, 12:766-774.
63. Balashov K.E., Rottman J.B., Weiner H.L., Hancock W.W. CCR5(+) and CXCR3(+) T cells are increased in multiple sclerosis and their ligands MIP-1alpha and IP-10 are expressed in demyelinating brain lesions. Proc Natl Acad Sci U S A 1999, 96:6873-6878.
64. Ruth J.H., Rottman J.B., Katschke K.J., Qin S., Wu L., LaRosa G., et al. Selective lymphocyte chemokine receptor expression in the rheumatoid joint. Arthritis Rheum 2001, 44:2750-2760.
65. Xie J.H., Nomura N., Lu M., Chen S.L., Koch G.E., Weng Y., et al. Antibody-mediated blockade of the CXCR3 chemokine receptor results in diminished recruitment of T helper 1 cells into sites of inflammation. J Leukoc Biol 2003, 73:771-780.
66. He S., Cao Q., Qiu Y., Mi J., Zhang J.Z., Jin M., et al. A new approach to the blocking of alloreactive T cell-mediated graft-versus-host disease by in vivo administration of anti-CXCR3 neutralizing antibody. J Immunol 2008, 181:7581-7592.
67. Garcia J.A., Pino P.A., Mizutani M., Cardona S.M., Charo I.F., Ransohoff R.M., et al. Regulation of adaptive immunity by the fractalkine receptor during autoimmune inflammation. J Immunol 2013, 191:1063-1072.
68. Lavergne E., Combadiere B., Bonduelle O., Iga M., Gao J.L., Maho M., et al. Fractalkine mediates natural killer-dependent antitumor responses in vivo. Cancer Res 2003, 63:7468-7474.
69. Xin H., Kikuchi T., Andarini S., Ohkouchi S., Suzuki T., Nukiwa T., et al. Antitumor immune response by CX3CL1 fractalkine gene transfer depends on both NK and T cells. Eur J Immunol 2005, 35:1371-1380.
70. Yu Y.R., Fong A.M., Combadiere C., Gao J.L., Murphy P.M., Patel D.D. Defective antitumor responses in CX3CR1-deficient mice. Int J Cancer 2007, 121:316-322.
71. Nansen A., Marker O., Bartholdy C., Thomsen A.R. CCR2+ and CCR5+ CD8+ T cells increase during viral infection and migrate to sites of infection. Eur J Immunol 2000, 30:1797-1806.
72. Connor S.J., Paraskevopoulos N., Newman R., Cuan N., Hampartzoumian T., Lloyd A.R., et al. CCR2 expressing CD4+ T lymphocytes are preferentially recruited to the ileum in Crohn's disease. Gut 2004, 53:1287-1294.
73. Zhang H.H., Song K., Rabin R.L., Hill B.J., Perfetto S.P., Roederer M., et al. CCR2 identifies a stable population of human effector memory CD4+ T cells equipped for rapid recall response. J Immunol 2010, 185:6646-6663.
74. Moon E.K., Carpenito C., Sun J., Wang L.C., Kapoor V., Predina J., et al. Expression of a functional CCR2 receptor enhances tumor localization and tumor eradication by retargeted human T cells expressing a mesothelin-specific chimeric antibody receptor. Clin Cancer Res 2011, 17:4719-4730.
75. Berencsi K., Rani P., Zhang T., Gross L., Mastrangelo M., Meropol N.J., et al. In vitro migration of cytotoxic T lymphocyte derived from a colon carcinoma patient is dependent on CCL2 and CCR2. J Transl Med 2011, 9:33.
76. Terwey T.H., Kim T.D., Kochman A.A., Hubbard V.M., Lu S., Zakrzewski J.L., et al. CCR2 is required for CD8-induced graft-versus-host disease. Blood 2005, 106:3322-3330.
77. Zhang H., Guo C., Wu D., Zhang A., Gu T., Wang L., et al. Hydrogen sulfide inhibits the development of atherosclerosis with suppressing CX3CR1 and CX3CL1 expression. PLOS ONE 2012, 7:e41147.
78. Pachot A., Cazalis M.A., Venet F., Turrel F., Faudot C., Voirin N., et al. Decreased expression of the fractalkine receptor CX3CR1 on circulating monocytes as new feature of sepsis-induced immunosuppression. J Immunol 2008, 180:6421-6429.
79. Shimizu K., Karube K., Arakawa F., Nomura Y., Komatani H., Yamamoto K., et al. Upregulation of CC chemokine ligand 18 and downregulation of CX3C chemokine receptor 1 expression in human T-cell leukemia virus type 1-associated lymph node lesions: results of chemokine and chemokine receptor DNA chip analysis. Cancer Sci 2007, 98:1875-1880.
80. Sica A., Saccani A., Bottazzi B., Bernasconi S., Allavena P., Gaetano B., et al. Defective expression of the monocyte chemotactic protein-1 receptor CCR2 in macrophages associated with human ovarian carcinoma. J Immunol 2000, 164:733-738.
81. Molon B., Viola A., Bronte V. Smoothing T cell roads to the tumor: chemokine post-translational regulation. Oncoimmunology 2012, 1:390-392.
82. Seok S.J., Lee E.S., Kim G.T., Hyun M., Lee J.H., Chen S., et al. Blockade of CCL2/CCR2 signalling ameliorates diabetic nephropathy in db/db mice. Nephrol Dial Transplant 2013, 28:1700-1710.
83. Dimitrijevic O.B., Stamatovic S.M., Keep R.F., Andjelkovic A.V. Absence of the chemokine receptor CCR2 protects against cerebral ischemia/reperfusion injury in mice. Stroke 2007, 38:1345-1353.
84. Allen C.D., Ansel K.M., Low C., Lesley R., Tamamura H., Fujii N., et al. Germinal center dark and light zone organization is mediated by CXCR4 and CXCR5. Nat Immunol 2004, 5:943-952.
85. Bannard O., Horton R.M., Allen C.D., An J., Nagasawa T., Cyster J.G. Germinal center centroblasts transition to a centrocyte phenotype according to a timed program and depend on the dark zone for effective selection. Immunity 2013, 39:912-924.
86. Shi G.X., Harrison K., Wilson G.L., Moratz C., Kehrl J.H. RGS13 regulates germinal center B lymphocytes responsiveness to CXC chemokine ligand (CXCL)12 and CXCL13. J Immunol 2002, 169:2507-2515.
87. Wang A., Guilpain P., Chong B.F., Chouzenoux S., Guillevin L., Du Y., et al. Dysregulated expression of CXCR4/CXCL12 in subsets of patients with systemic lupus erythematosus. Arthritis Rheum 2010, 62:3436-3446.
88. Ehlin-Henriksson B., Mowafi F., Klein G., Nilsson A. Epstein-Barr virus infection negatively impacts the CXCR4-dependent migration of tonsillar B cells. Immunology 2006, 117:379-385.
89. Gazit E., Sherf M., Balbin E., Muratov A., Goldstein I., Loewenthal R. HLA-G expression is induced in Epstein-Barr virus-transformed B-cell lines by culture conditions. Hum Immunol 2007, 68:463-468.
90. Walker L.S., Gulbranson-Judge A., Flynn S., Brocker T., Raykundalia C., Goodall M., et al. Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J Exp Med 1999, 190:1115-1122.
91. Breitfeld D., Ohl L., Kremmer E., Ellwart J., Sallusto F., Lipp M., et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J Exp Med 2000, 192:1545-1552.
92. Schaerli P., Willimann K., Lang A.B., Lipp M., Loetscher P., Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J Exp Med 2000, 192:1553-1562.
93. Kim C.H., Rott L.S., Clark-Lewis I., Campbell D.J., Wu L., Butcher E.C. Subspecialization of CXCR5+ T cells: B helper activity is focused in a germinal center-localized subset of CXCR5+ T cells. J Exp Med 2001, 193:1373-1381.
94. Corcione A., Benvenuto F., Ferretti E., Giunti D., Cappiello V., Cazzanti F., et al. Human mesenchymal stem cells modulate B-cell functions. Blood 2006, 107:367-372.
95. Morandi F., Raffaghello L., Bianchi G., Meloni F., Salis A., Millo E., et al. Immunogenicity of human mesenchymal stem cells in HLA-class I-restricted T-cell responses against viral or tumor-associated antigens. Stem Cells 2008, 26:1275-1287.
96. Selmani Z., Naji A., Zidi I., Favier B., Gaiffe E., Obert L. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4+CD25highFOXP3+ regulatory T cells. Stem Cells 2008, 26:212-222.
97. Krumbholz M., Theil D., Cepok S., Hemmer B., Kivisakk P., Ransohoff R.M., et al. Chemokines in multiple sclerosis: CXCL12 and CXCL13 up-regulation is differentially linked to CNS immune cell recruitment. Brain 2006, 129:200-211.
98. Salomonsson S., Larsson P., Tengner P., Mellquist E., Hjelmstrom P., Wahren-Herlenius M. Expression of the B cell-attracting chemokine CXCL13 in the target organ and autoantibody production in ectopic lymphoid tissue in the chronic inflammatory disease Sjogren's syndrome. Scand J Immunol 2002, 55:336-342.
99. Mountz J.D., Wang J.H., Xie S., Hsu H.C. Cytokine regulation of B-cell migratory behavior favors formation of germinal centers in autoimmune disease. Discov Med 2011, 11:76-85.
100. Kearney E.R., Pape K.A., Loh D.Y., Jenkins M.K. Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994, 1:327-339.
101. Morita R., Schmitt N., Bentebibel S.E., Ranganathan R., Bourdery L., Zurawski G., et al. Human blood CXCR5(+)CD4(+) T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011, 34:108-121.
102. He J., Tsai L.M., Leong Y.A., Hu X., Ma C.S., Chevalier N., et al. Circulating precursor CCR7(lo)PD-1(hi) CXCR5(+) CD4(+) T cells indicate Tfh cell activity and promote antibody responses upon antigen reexposure. Immunity 2013, 39:770-781.