B7 Family Molecules as Regulators of the Maternal Immune System in Pregnancy

American Journal of Reproductive Immunology

Volumn 63, Issue 6, 2010, Pages 506-519

  Petroff, Margaret G ^a   Perchellet, Antoine ^a  

^a UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Fetus; Maternal fetal interface; Placenta; Tolerance

Indexed keywords

B7 ANTIGEN; B7 H2 ANTIGEN; B7 H3 ANTIGEN; B7 H4 ANTIGEN; B7 H6 ANTIGEN; CD86 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FETAL ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; UNCLASSIFIED DRUG;

ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; CYTOKINE PRODUCTION; DECIDUA; FETUS GROWTH; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INTRACELLULAR SIGNALING; MOTHER FETUS RELATIONSHIP; NONHUMAN; PLACENTA; PLACENTA DEVELOPMENT; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; REVIEW; T LYMPHOCYTE ACTIVATION; TROPHOBLAST; ANIMAL; C57BL MOUSE; CBA MOUSE; CYTOLOGY; FEMALE; FETOMATERNAL TRANSFUSION; FETUS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; METABOLISM; MOUSE; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD80; DECIDUA; FEMALE; FETUS; HUMANS; IMMUNE SYSTEM; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; PLACENTA; PREGNANCY; T-LYMPHOCYTES;

EID: 77953965808     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2010.00841.x     Document Type: Review

References (103)

1. Erlebacher A, Vencato D, Price KA, Zhang D, Glimcher LH. Constraints in antigen presentation severely restrict T cell recognition of the allogeneic fetus. J Clin Invest 2007, 117:1399-1411.
2. Moldenhauer LM, Hayball JD, Robertson SA. Conceptus antigens activate the maternal immune response in pregnancy utilising maternal antigen presenting cells. J Immunol 2009, 71:148.
3. Taglauer ES, Adams Waldorf KM, Petroff MG. The hidden maternal-fetal interface: events involving the lymphoid organs in maternal-fetal tolerance. Int J Dev Biol 2010, 54:421-430.
4. Adams Waldorf KM, Yan Z, Stevens AM, Nelson JL. The changing maternal " self" hypothesis: a mechanism for maternal tolerance of the fetus. Placenta 2007, 28:378-382.
5. Jenkins MK, Pardoll DM, Mizuguchi J, Quill H, Schwartz RH. T-cell unresponsiveness in vivo and in vitro: fine specificity of induction and molecular characterization of the unresponsive state. Immunol Rev 1987, 95:113-135.
6. Gimmi C, Freeman G, Gribben J, Sugita K, Freedman A, Morimoto C, Nadler L. B-cell surface antigen B7 provides a costimulatory signal that induces T cells to proliferate and secrete interleukin 2. Proc Natl Acad Sci U S A 1991, 88:6575-6579.
7. Gimmi CD, Freeman GJ, Gribben JG, Gray G, Nadler LM. Human T-cell clonal anergy is induced by antigen presentation in the absence of B7 costimulation. Proc Natl Acad Sci U S A 1993, 90:6586-6590.
8. van der Merwe PA, Bodian DL, Daenke S, Linsley P, Davis SJ. CD80 (B7-1) binds both CD28 and CTLA-4 with a low affinity and very fast kinetics. J Exp Med 1997, 185:393-403.
9. Ostrov DA, Shi W, Schwartz JC, Almo SC, Nathenson SG. Structure of murine CTLA-4 and its role in modulating T cell responsiveness. Science 2000, 290:816-819.
10. Walunas TL, Bakker CY, Bluestone JA. CTLA-4 ligation blocks CD28-dependent T cell activation. J Exp Med 1996, 183:2541-2550.
11. Krummel MF, Allison JP. CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells. J Exp Med 1996, 183:2533-2540.
12. Bachmann MF, Kohler G, Ecabert B, Mak TW, Kopf M. Cutting edge: lymphoproliferative disease in the absence of CTLA-4 is not T cell autonomous. J Immunol 1999, 163:1128-1131.
13. Friedline RH, Brown DS, Nguyen H, Kornfeld H, Lee J, Zhang Y, Appleby M, Der SD, Kang J, Chambers CA. CD4+ regulatory T cells require CTLA-4 for the maintenance of systemic tolerance. J Exp Med 2009, 206:421-434.
14. Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, Nomura T, Sakaguchi S. CTLA-4 control over Foxp3+ regulatory T cell function. Science 2008, 322:271-275.
15. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev 2008, 224:166-182.
16. Powell J, Ragheb J, Kitagawa-Sakakida S, Schwartz R. Molecular regulation of interleukin-2 expression by CD28 co-stimulation and anergy. Immunol Rev 1998, 165:287-300.
17. Olivares EG, Montes MJ, Oliver C, Galindo JA, Ruiz C. Cultured human decidual stromal cells express B7-1 (CD80) and B7-2 (CD86) and stimulate allogeneic T cells. Biol Reprod 1997, 57:609-615.
18. Miyazaki S, Tsuda H, Sakai M, Hori S, Sasaki Y, Futatani T, Miyawaki T, Saito S. Predominance of Th2-promoting dendritic cells in early human pregnancy decidua. J Leukoc Biol 2003, 74:514-522.
19. Breburda EE, Dambaeva SV, Slukvin II, Golos TG. Selective distribution and pregnancy-specific expression of DC-SIGN at the maternal-fetal interface in the rhesus macaque: DC-SIGN is a putative marker of the recognition of pregnancy. Placenta 2006, 27:11-21.
20. Gardner L, Moffett A. Dendritic cells in the human decidua. Biol Reprod 2003, 69:1438-1446.
21. Blois SM, Kammerer U, Soto CA, Tometten MC, Shaikly V, Barrientos G, Jurd R, Rukavina D, Thomson AW, Klapp BF, Fernandez N, Arck PC. Dendritic cells: key to fetal tolerance? Biol Reprod 2007, 77:590-598.
22. Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O. Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 2003, 131:498-505.
23. Shortman K, Liu YJ. Mouse and human dendritic cell subtypes. Nat Rev Immunol 2002, 2:151-161.
24. Collins MK, Tay CS, Erlebacher A. Dendritic cell entrapment within the pregnant uterus inhibits immune surveillance of the maternal/fetal interface in mice. J Clin Invest 2009, 119:2062-2073.
25. Petroff MG, Chen L, Phillips TA, Azzola D, Sedlmayr P, Hunt JS. B7 family molecules are favorably positioned at the human maternal-fetal interface. Biol Reprod 2003, 68:1496-1504.
26. Sutton L, Gadd M, Mason DY, Redman CW. Cells bearing class II MHC antigens in the human placenta. Immunology 1986, 58:23-29.
27. Labarrere CA, Faulk WP. Maternal cells in chorionic villi from placentae of normal and abnormal human pregnancies. Am J Reprod Immunol 1995, 33:54-59.
28. Redline RW, Patterson P. Villitis of unknown etiology is associated with major infiltration of fetal tissue by maternal inflammatory cells. Am J Pathol 1993, 143:473-479.
29. Kim J-S, Romero R, Kim MR, Kim YM, Friel L, Espinoza J, Kim CJ. Involvement of Hofbauer cells and maternal T cells in villitis of unknown aetiology. Histopathology 2008, 52:457-464.
30. Kapur P, Rakheja D, Gomez AM, Sheffield J, Sanchez P, Rogers BB. Characterization of inflammation in syphilitic villitis and in villitis of unknown etiology. Pediatr Dev Pathol 2004, 7:453-458.
31. Brito H, Juliano P, Altemani C, Altemani A. Is the immunohistochemical study of the inflammatory infiltrate helpful in distinguishing villitis of unknown etiology from non-specific infection villitis? Placenta 2005, 26:839-841.
32. Grohmann U, Orabona C, Fallarino F, Vacca C, Calcinaro F, Falorni A, Candeloro P, Belladonna ML, Bianchi R, Fioretti MC, Puccetti P. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 2002, 3:1097-1101.
33. Munn DH, Zhou M, Attwood JT, Bondarev I, Conway SJ, Marshall B, Brown C, Mellor AL. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 1998, 281:1191-1193.
34. Baban B, Chandler P, McCool D, Marshall B, Munn DH, Mellor AL. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J Reprod Immunol 2004, 61:67-77.
35. Miwa N, Hayakawa S, Miyazaki S, Myojo S, Sasaki Y, Sakai M, Takikawa O, Saito S. IDO expression on decidual and peripheral blood dendritic cells and monocytes/macrophages after treatment with CTLA-4 or interferon-γ increase in normal pregnancy but decrease in spontaneous abortion. Mol Hum Reprod 2005, 11:865-870.
36. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S. Decidual and peripheral blood CD4+ CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 2004, 10:347-353.
37. Kaufman KA, Bowen JA, Tsai AF, Bluestone JA, Hunt JS, Ober C. The CTLA-4 gene is expressed in placental fibroblasts. Mol Hum Reprod 1999, 5:84-87.
38. Jin L-P, Zhou Y-H, Wang M-Y, Zhu X-Y, Li D-J. Blockade of CD80 and CD86 at the time of implantation inhibits maternal rejection to the allogeneic fetus in abortion-prone matings. J Reprod Immunol 2005, 65:133-146.
39. Jin L-P, Li D-J, Zhang J-P, Wang M-Y, Zhu X-Y, Zhu Y, Meng Y, Yuan M-M. Adoptive transfer of paternal antigen-hyporesponsive T cells induces maternal tolerance to the allogeneic fetus in abortion-prone matings. J Immunol 2004, 173:3612-3619.
40. Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, Yagita H, Noelle RJ, Coyle A, Mellor AL, Khoury SJ, Sayegh MH. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 2005, 202:231-237.
41. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T cell proliferation and interleukin 10 secretion. Nat Med 1999, 5:1365-1369.
42. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton HF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T. Engagement of the PD-1 Immunoinhibitory Receptor by a Novel B7 Family Member Leads to Negative Regulation of Lymphocyte Activation. J Exp Med 2000, 192:1027-1034.
43. Wang S, Bajorath J, Flies DB, Dong H, Honjo T, Chen L. Molecular modeling and functional mapping of B7-H1 and B7-DC uncouple costimulatory function from PD-1 interaction. J Exp Med 2003, 197:1083-1091.
44. Holets LM, Carletti MZ, Kshirsagar SK, Christenson LK, Petroff MG. Differentiation-induced post- transcriptional control of B7-H1 in human trophoblast cells. Placenta 2009, 30:48-55.
45. Gong A-Y, Zhou R, Hu G, Li X, Splinter PL, O'Hara SP, LaRusso NF, Soukup GA, Dong H, Chen X-M. MicroRNA-513 regulates B7-H1 translation and is involved in IFN-γ-induced B7-H1 expression in cholangiocytes. J Immunol 2009, 182:1325-1333.
46. Dong H, Zhu G, Tamada K, Flies DB, van Deursen JMA, Chen L. B7-H1 determines accumulation and deletion of intrahepatic CD8+ T lymphocytes. Immunity 2004, 20:327-336.
47. Youngnak P, Kozono Y, Kozono H, Iwai H, Otsuki N, Jin H, Omura K, Yagita H, Pardoll DM, Chen L, Azuma M. Differential binding properties of B7-H1 and B7-DC to programmed death-1. Biochem Biophys Res Commun 2003, 307:672-677.
48. Liang SC, Latchman YE, Buhlmann JE, Tomczak MF, Horwitz BH, Freeman GJ, Sharpe AH. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur J Immunol 2003, 33:2706-2716.
49. Latchman Y, Wood CR, Chernova T, Chaudhary D, Borde M, Chernova I, Iwai Y, Long AJ, Brown JA, Nunes R, Greenfield EA, Bourque K, Boussiotis VA, Carter LL, Carreno BM, Malenkovich N, Nishimura H, Okazaki T, Honjo T, Sharpe AH, Freeman GJ. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001, 2:261-268.
50. Tseng S-Y, Otsuji M, Gorski K, Huang X, Slansky JE, Pai SI, Shalabi A, Shin T, Pardoll DM, Tsuchiya H. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J Exp Med 2001, 193:839-846.
51. Yamazaki T, Akiba H, Iwai H, Matsuda H, Aoki M, Tanno Y, Shin T, Tsuchiya H, Pardoll DM, Okumura K, Azuma M, Yagita H. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 2002, 169:5538-5545.
52. Okazaki T. PD-1 immunoreceptor inhibits B cell receptor-mediated signaling by recruiting src homology 2-domain-containing tyrosine phosphatase 2 to phosphotyrosine. Proc Natl Acad Sci USA 2001, 98:13866-13871.
53. Chemnitz JM, Parry RV, Nichols KE, June CH, Riley JL. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol 2004, 173:945-954.
54. Riley JL. PD-1 signaling in primary T cells. Immunol Rev 2009, 229:114-125.
55. Probst HC, McCoy K, Okazaki T, Honjo T, van den Broek M. Resting dendritic cells induce peripheral CD8+ T cell tolerance through PD-1 and CTLA-4. Nat Immunol 2005, 6:280-286.
56. Keir ME, Freeman GJ, Sharpe AH. PD-1 regulates self-reactive CD8+ T cell responses to antigen in lymph nodes and tissues. J Immunol 2007, 179:5064-5070.
57. Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, Sasayama S, Mizoguchi A, Hiai H, Minato N, Honjo T. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001, 291:319-322.
58. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999, 11:141-151.
59. Ansari MJI, Salama AD, Chitnis T, Smith RN, Yagita H, Akiba H, Yamazaki T, Azuma M, Iwai H, Khoury SJ, Auchincloss H, Sayegh MH. The programmed death-1 (PD-1) pathway regulates autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 2003, 198:63-69.
60. Salama AD, Chitnis T, Imitola J, Ansari MJI, Akiba H, Tushima F, Azuma M, Yagita H, Sayegh MH, Khoury SJ. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J Exp Med 2003, 198:71-78.
61. Latchman YE, Liang SC, Wu Y, Chernova T, Sobel RA, Klemm M, Kuchroo VK, Freeman GJ, Sharpe AH. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. PNAS 2004, 101:10691-10696.
62. Shin H, Wherry EJ. CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol 2007, 19:408-415.
63. Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK, Sharpe AH. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med 2009, 206:3015-3029.
64. Wang L, Pino-Lagos K, de Vries VC, Guleria I, Sayegh MH, Noelle RJ. Programmed death 1 ligand signaling regulates the generation of adaptive Foxp3+CD4+ regulatory T cells. Proc Natl Acad Sci U S A 2008, 105:9331-9336.
65. Azuma T, Yao S, Zhu G, Flies AS, Flies SJ, Chen L. B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. Blood 2008, 111:3635-3643.
66. Nguyen LT, Radhakrishnan S, Ciric B, Tamada K, Shin T, Pardoll DM, Chen L, Rodriguez M, Pease LR. Cross-linking the B7 family molecule B7-DC directly activates immune functions of dendritic cells. J Exp Med 2002, 196:1393-1398.
67. Kuipers H, Muskens F, Willart M, Hijdra D, Assema Friso BJv, Coyle Anthony J, Hoogsteden Henk C, Lambrecht Bart N. Contribution of the PD-1 ligands/PD-1 signaling pathway to dendritic cell-mediated CD4+ T cell activation. Eur J Immunol 2006, 36:2472-2482.
68. Nagamatsu T, Schust DJ, Sugimoto J, Barrier BF. Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions. Hum Reprod 2009, 24:3160-3171.
69. Petroff MG, Chen L, Phillips TA, Hunt JS. B7 family molecules: novel immunomodulators at the maternal-fetal interface. Placenta 2002, 23(Suppl. A):S95-S101.
70. Holets LM, Hunt JS, Petroff MG. Trophoblast CD274 (B7-H1) is differentially expressed across gestation: influence of oxygen concentration. Biol Reprod 2006, 74:352-358.
71. Taglauer ES, Trikhacheva AS, Slusser JG, Petroff MG. Expression and function of PDCD1 at the human maternal-fetal interface. Biol Reprod 2008, 79:562-569.
72. Bennett F, Luxenberg D, Ling V, Wang IM, Marquette K, Lowe D, Khan N, Veldman G, Jacobs KA, Valge-Archer VE, Collins M, Carreno BM. Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokine-driven proliferation: attenuation of ICOS, IL-4, and IL-21, but not CD28, IL-7, and IL-15 responses. J Immunol 2003, 170:711-718.
73. Habicht A, Dada S, Jurewicz M, Fife BT, Yagita H, Azuma M, Sayegh MH, Guleria I. A link between PDL1 and T regulatory cells in fetomaternal tolerance. J Immunol 2007, 179:5211-5219.
74. Taglauer ES, Yankee TM, Petroff MG. Maternal PD-1 regulates accumulation of fetal antigen- specific CD8+ T cells in pregnancy. J Reprod Immunol 2009, 80:12-21.
75. Yoshinaga SK, Whoriskey JS, Khare SD, Sarmiento U, Guo J, Horan T, Shih G, Zhang M, Coccia MA, Kohno T, Tafuri-Bladt A, Brankow D, Campbell P, Chang D, Chiu L, Dai T, Duncan G, Elliott GS, Hui A, McCabe SM, Scully S, Shahinian A, Shaklee CL, Van G, Mak TW, Senaldi G. T-cell co- stimulation through B7RP-1 and ICOS. Nature 1999, 402:827-832.
76. Coyle AJ, Lehar S, Lloyd C, Tian J, Delaney T, Manning S, Nguyen T, Burwell T, Schneider H, Gonzalo JA, Gosselin M, Owen LR, Rudd CE, Gutierrez-Ramos JC. The CD28-related molecule ICOS is required for effective T cell-dependent immune responses. Immunity 2000, 13:95-105.
77. McAdam AJ, Greenwald RJ, Levin MA, Chernova T, Malenkovich N, Ling V, Freeman GJ, Sharpe AH. ICOS is critical for CD40-mediated antibody class switching. Nature 2001, 409:102-105.
78. Tafuri A, Shahinian A, Bladt F, Yoshinaga SK, Jordana M, Wakeham A, Boucher LM, Bouchard D, Chan VS, Duncan G, Odermatt B, Ho A, Itie A, Horan T, Whoriskey JS, Pawson T, Penninger JM, Ohashi PS, Mak TW. ICOS is essential for effective T-helper-cell responses. Nature 2001, 409:105-109.
79. Hutloff A, Dittrich AM, Beier KC, Eljaschewitsch B, Kraft R, Anagnostopoulos I, Kroczek RA. ICOS is an inducible T-cell co-stimulator structurally and functionally related to CD28. Nature 1999, 397:263-266.
80. McAdam AJ, Chang TT, Lumelsky AE, Greenfield EA, Boussiotis VA, Duke-Cohan JS, Chernova T, Malenkovich N, Jabs C, Kuchroo VK, Ling V, Collins M, Sharpe AH, Freeman GJ. Mouse inducible costimulatory molecule (ICOS) expression Is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. J Immunol 2000, 165:5035-5040.
81. Tuettenberg A, Huter E, Hubo M, Horn J, Knop J, Grimbacher B, Kroczek RA, Stoll S, Jonuleit H. The role of ICOS in directing T cell responses: ICOS-dependent induction of T cell anergy by tolerogenic dendritic cells. J Immunol 2009, 182:3349-3356.
82. Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, Sharpe AH, Berry G, DeKruyff RH, Umetsu DT. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med 2002, 8:1024-1032.
83. Vermeiren J, Ceuppens JL, Van Ghelue M, Witters P, Bullens D, Mages HW, Kroczek RA, Van Gool SW. Human T cell activation by costimulatory signal-deficient allogeneic cells induces inducible costimulator-expressing anergic T cells with regulatory cell activity. J Immunol 2004, 172:5371-5378.
84. Ogasawara K, Yoshinaga SK, Lanier LL. Inducible costimulator costimulates cytotoxic activity and IFN-gamma production in activated murine NK cells. J Immunol 2002, 169:3676-3685.
85. Ling V, Wu PW, Finnerty HF, Bean KM, Spaulding V, Fouser LA, Leonard JP, Hunter SE, Zollner R, Thomas JL, Miyashiro JS, Jacobs KA, Collins M. Cutting Edge: identification of GL50, a novel B7- like protein that functionally binds to ICOS receptor. J Immunol 2000, 164:1653-1657.
86. Petroff MG, Kharatyan E, Torry DS, Holets L. The immunomodulatory proteins B7-DC, B7-H2, and B7-H3 are differentially expressed across gestation in the human placenta. Am J Pathol 2005, 167:465-473.
87. Chapoval AI, Ni J, Lau JS, Wilcox RA, Flies DB, Liu D, Dong H, Sica GL, Zhu G, Tamada K, Chen L. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol 2001, 2:269-274.
88. Prasad DV, Nguyen T, Li Z, Yang Y, Duong J, Wang Y, Dong C. Murine B7-H3 is a negative regulator of T cells. J Immunol 2004, 173:2500-2506.
89. Sun M, Richards S, Prasad DV, Mai XM, Rudensky A, Dong C. Characterization of mouse and human B7-H3 genes. J Immunol 2002, 168:6294-6297.
90. Ling V, Wu PW, Spaulding V, Kieleczawa J, Luxenberg D, Carreno BM, Collins M. Duplication of primate and rodent B7-H3 immunoglobulin V- and C-like domains: divergent history of functional redundancy and exon loss. Genomics 2003, 82:365-377.
91. Suh WK, Gajewska BU, Okada H, Gronski MA, Bertram EM, Dawicki W, Duncan GS, Bukczynski J, Plyte S, Elia A, Wakeham A, Itie A, Chung S, Da Costa J, Arya S, Horan T, Campbell P, Gaida K, Ohashi PS, Watts TH, Yoshinaga SK, Bray MR, Jordana M, Mak TW. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol 2003, 4:899-906.
92. Steinberger P, Majdic O, Derdak SV, Pfistershammer K, Kirchberger S, Klauser C, Zlabinger G, Pickl WF, Stockl J, Knapp W. Molecular characterization of human 4Ig-B7-H3, a member of the B7 family with four Ig-like domains. J Immunol 2004, 172:2352-2359.
93. Hashiguchi M, Kobori H, Ritprajak P, Kamimura Y, Kozono H, Azuma M. Triggering receptor expressed on myeloid cell-like transcript 2 (TLT-2) is a counter-receptor for B7-H3 and enhances T cell responses. Proc Natl Acad Sci U S A 2008, 105:10495-10500.
94. Leitner J, Klauser C, Pickl WF, Stöckl J, Majdic O, Bardet AF, Kreil DP, Dong C, Yamazaki T, Zlabinger G, Pfistershammer K, Steinberger P. B7-H3 is a potent inhibitor of human T-cell activation: no evidence for B7-H3 and TREML2 interaction. Eur J Immunol 2009, 39:1754-1764.
95. Suh WK, Wang SX, Jheon AH, Moreno L, Yoshinaga SK, Ganss B, Sodek J, Grynpas MD, Mak TW. The immune regulatory protein B7-H3 promotes osteoblast differentiation and bone mineralization. Proc Natl Acad Sci U S A 2004, 101:12969-12973.
96. Sica GL, Choi IH, Zhu G, Tamada K, Wang SD, Tamura H, Chapoval AI, Flies DB, Bajorath J, Chen L. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 2003, 18:849-861.
97. Prasad DV, Richards S, Mai XM, Dong C. B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 2003, 18:863-873.
98. Sedy JR, Gavrieli M, Potter KG, Hurchla MA, Lindsley RC, Hildner K, Scheu S, Pfeffer K, Ware CF, Murphy TL, Murphy KM. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol 2005, 6:90-98.
99. Suh WK, Wang S, Duncan GS, Miyazaki Y, Cates E, Walker T, Gajewska BU, Deenick E, Dawicki W, Okada H, Wakeham A, Itie A, Watts TH, Ohashi PS, Jordana M, Yoshida H, Mak TW. Generation and characterization of B7-H4/B7S1/B7x-deficient mice. Mol Cell Biol 2006, 26:6403-6411.
100. Zhu G, Augustine MM, Azuma T, Luo L, Yao S, Anand S, Rietz AC, Huang J, Xu H, Flies AS, Flies SJ, Tamada K, Colonna M, van Deursen JM, Chen L. B7-H4-deficient mice display augmented neutrophil-mediated innate immunity. Blood 2009, 113:1759-1767.
101. Song H, Park G, Kim YS, Hur I, Kim H, Ryu JW, Lee HK, Cho DH, Choi IH, Lee WJ, Hur DY. B7-H4 reverse signaling induces the apoptosis of EBV-transformed B cells through Fas ligand up- regulation. Cancer Lett 2008, 266:227-237.
102. Galazka K, Wicherek L, Pitynski K, Kijowski J, Zajac K, Bednarek W, Dutsch-Wicherek M, Rytlewski K, Kalinka J, Basta A, Majka M. Changes in the subpopulation of CD25+CD4+ and FOXP3+ regulatory T cells in decidua with respect to the progression of labor at term and the lack of analogical changes in the subpopulation of suppressive B7-H4+ macrophages - a preliminary report. Am J Reprod Immunol 2009, 61:136-146.
103. Brandt CS, Baratin M, Yi EC, Kennedy J, Gao Z, Fox B, Haldeman B, Ostrander CD, Kaifu T, Chabannon C, Moretta A, West R, Xu W, Vivier E, Levin SD. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med 2009, 206:1495-1503.