본문 바로가기
KERD
논문KCI 등재

The CD28-B7 Family in Anti-Tumor Immunity: Emerging Concepts in Cancer Immunotherapy

Woong-Kyung Suh|Joanne Leung
대한면역학회 (The Korean Association of Immunologists)|2014.12|Immune Network|제14권 제6호|pp. 265-276

2

조회

0

다운로드

1

인용

0

참고문헌

키워드

Cancer immunotherapyImmune evasionB7 familyCD28 familyCo-stimulationCo-inhibition

초록

The interactions between B7 molecules and CD28-family receptorsare crucial in the regulation of adaptive cellularimmunity. In cancer, the aberrant expression of co-inhibitoryB7 molecules has been attributed to reduced anti-tumor immunityand cancer immune evasion, prompting the developmentof cancer therapeutics that can restore T cell function. Murine tumor models have provided significant support forthe targeting of multiple immune checkpoints involvingCTLA-4, PD-1, ICOS, B7-H3 and B7-H4 during tumorgrowth, and clinical studies investigating the therapeutic effectsof CTLA-4 and PD-1 blockade have shown exceptionallypromising results in patients with advanced melanomaand other cancers. The expression pattern of co-inhibitoryB7 ligands in the tumor microenvironment has also beenlargely correlated with poor patient prognosis, and recentevidence suggests that the presence of several B7 moleculesmay predict the responsiveness of immunotherapies that relyon pre-existing tumor-associated immune responses. Whilemonotherapies blocking T cell co-inhibition have beneficialeffects in reducing tumor burden, combinatorial immunotherapytargeting multiple immune checkpoints involved invarious stages of the anti-tumor response has led to themost substantial impact on tumor reduction. In this review,we will examine the contributions of B7- and CD28-familymembers in the context of cancer development, and discussthe implications of current human findings in cancer immunotherapy.

Abstract

The interactions between B7 molecules and CD28-family receptorsare crucial in the regulation of adaptive cellularimmunity. In cancer, the aberrant expression of co-inhibitoryB7 molecules has been attributed to reduced anti-tumor immunityand cancer immune evasion, prompting the developmentof cancer therapeutics that can restore T cell function. Murine tumor models have provided significant support forthe targeting of multiple immune checkpoints involvingCTLA-4, PD-1, ICOS, B7-H3 and B7-H4 during tumorgrowth, and clinical studies investigating the therapeutic effectsof CTLA-4 and PD-1 blockade have shown exceptionallypromising results in patients with advanced melanomaand other cancers. The expression pattern of co-inhibitoryB7 ligands in the tumor microenvironment has also beenlargely correlated with poor patient prognosis, and recentevidence suggests that the presence of several B7 moleculesmay predict the responsiveness of immunotherapies that relyon pre-existing tumor-associated immune responses. Whilemonotherapies blocking T cell co-inhibition have beneficialeffects in reducing tumor burden, combinatorial immunotherapytargeting multiple immune checkpoints involved invarious stages of the anti-tumor response has led to themost substantial impact on tumor reduction. In this review,we will examine the contributions of B7- and CD28-familymembers in the context of cancer development, and discussthe implications of current human findings in cancer immunotherapy.

참고문헌 (98)

  1. Ceeraz, S., "B7 family checkpoint regulators in immune regulation and disease", Trends Immunol, 34, pp.556~563 (2013)
  2. Sharpe, A. H., "The B7-CD28 superfamily", Nat. Rev. Immunol, 2, pp.116~126 (2002)
  3. Sakaguchi, S, "Regulatory T cells: how do they suppress immune responses?", Int. Immunol, 21, pp.1105~1111 (2009)
  4. Grosso, J. F, "CTLA-4 blockade in tumor models: an overview of preclinical and translational research", Cancer Immun, 13, pp.5~ (2013)
  5. Yang, Y. F., "Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages", Cancer Res, 57, pp.4036~4041 (1997)
  6. Kwon, E. D., "Manipulation of T cell costimulatory and inhibitory signals for immunotherapy of prostate cancer", Proc. Natl. Acad. Sci. U. S. A, 94, pp.8099~8103 (1997)
  7. van, E. A., "Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte", macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation, 1999, pp.190, 355~366
  8. Demaria, S, "Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer", Clin. Cancer Res, 11, pp.728~734 (2005)
  9. Hurwitz, A. A, "CTLA-4 blockade synergizes with tumor-derived granulocyte-macrophage colony-stimulating factor for treatment of an experimental mammary carcinoma", Proc. Natl. Acad. Sci. U. S. A, 95, pp.10067~10071 (1998)
  10. Mokyr, M. B., "Realization of the therapeutic potential of CTLA-4 blockade in low-dose chemotherapy-treated tumor-bearing mice", Cancer Res, 58, pp.5301~5304 (1998)
  11. Waitz, R., "Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy", Cancer Res, 72, pp.430~439 (2012)
  12. Phan, G. Q, "Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma", Proc. Natl. Acad. Sci. U. S. A, 100, pp.8372~8377 (2003)
  13. Sanderson, K., "Autoimmunity in a phase I trial of a fully human anti-cytotoxic T-lymphocyte antigen-4 monoclonal antibody with multiple melanoma peptides and Montanide ISA 51 for patients with resected stages III and IV melanoma", J. Clin. Oncol, 23, pp.741~750 (2005)
  14. Hodi, F. S., "Improved survival with ipilimumab in patients with metastatic melanoma", N. Engl. J. Med, 363, pp.711~723 (2010)
  15. Robert, C, "Ipilimumab plus dacarbazine for previously untreated metastatic melanoma", N. Engl. J. Med, 364, pp.2517~2526 (2011)
  16. Ribas, A. 2008, "Overcoming immunologic tolerance to melanoma: targeting CTLA-4 with tremelimumab (CP-675,206)", Oncologist Suppl, 4, pp.10~15 (2008)
  17. Ribas, A., "Phase III randomized clinical trial comparing tremelimumab with standard-of-care chemotherapy in patients with advanced melanoma", J. Clin. Oncol, 31, pp.616~622 (2013)
  18. Selby, M. J., "Anti-CTLA-4 antibodies of IgG2a isotype enhance antitumor activity through reduction of intratumoral regulatory T cells", Cancer Immunol. Res, 1, pp.32~42 (2013)
  19. Yuan, J., "Integrated NY-ESO-1 antibody and CD8＋ T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab", Proc. Natl. Acad. Sci. U. S. A, 108, pp.16723~16728 (2011)
  20. Liakou, C. I., "CTLA-4 blockade increases IFNgamma-producing CD4＋ICOShi cells to shift the ratio of effector to regulatory T cells in cancer patients", Proc. Natl. Acad. Sci. U. S. A, 105, pp.14987~14992 (2008)
  21. Keir, M. E, "Tissue expression of PD-L1 mediates peripheral T cell tolerance", J. Exp. Med, 203, pp.883~895 (2006)
  22. Larsson, M., "Molecular signatures of T-cell inhibition in HIV-1 infection", Retrovirology, 10, pp.31~ (2013)
  23. Pardoll, D. M, "The blockade of immune checkpoints in cancer immunotherapy", Nat. Rev. Cancer, 12, pp.252~264 (2012)
  24. Ahmadzadeh, M, "Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired", Blood, 114, pp.1537~1544 (2009)
  25. Matsuzaki, J., "Tumor-infiltrating NY-ESO-1- specific CD8＋ T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer", Proc. Natl. Acad. Sci. U. S. A, 107, pp.7875~7880 (2010)
  26. Barber, D. L., "Restoring function in exhausted CD8 T cells during chronic viral infection", Nature, 439, pp.682~687 (2006)
  27. Dong, H, "Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion", Nat. Med, 8, pp.793~800 (2002)
  28. Iwai, Y., "Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade", Proc. Natl. Acad. Sci. U. S. A, 99, pp.12293~12297 (2002)
  29. Ghebeh, H, "The B7-H1 (PD-L1) T lymphocyte-inhibitory molecule is expressed in breast cancer patients with infiltrating ductal carcinoma: correlation with important high-risk prognostic factors", Neoplasia, 8, pp.190~198 (2006)
  30. Steidl, C., "MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers", Nature, 471, pp.377~381 (2011)
  31. Rosenwald, A., "Molecular diagnosis of primary mediastinal B cell lymphoma identifies a clinically favorable subgroup of diffuse large B cell lymphoma related to Hodgkin lymphoma", J. Exp. Med, 198, pp.851~862 (2003)
  32. Hino, R., "Tumor cell expression of programmed cell death-1 ligand 1 is a prognostic factor for malignant melanoma", Cancer, 116, pp.1757~1766 (2010)
  33. Gao, Q, "Overexpression of PD-L1 significantly associates with tumor aggressiveness and postoperative recurrence in human hepatocellular carcinoma", Clin. Cancer Res, 15, pp.971~979 (2009)
  34. Muenst, S, "Expression of programmed death ligand 1 (PD-L1) is associated with poor prognosis in human breast cancer", Breast Cancer Res. Treat, 146, pp.15~24 (2014)
  35. Taube, J. M., "Colocalization of inflammatory response with B7-h1 expression in human melanocytic lesions supports an adaptive resistance mechanism of immune escape", Sci. Transl. Med, 4, pp.127ra37~ (2012)
  36. Zheng, Z., "Level of circulating PD-L1 expression in patients with advanced gastric cancer and its clinical implications", Chin. J. Cancer Res, 26, pp.104~111 (2014)
  37. Iwai, Y., "PD-1 blockade inhibits hematogenous spread of poorly immunogenic tumor cells by enhanced recruitment of effector T cells", Int. Immunol, 17, pp.133~144 (2005)
  38. Harvey, R. D., "Immunologic and clinical effects of targeting PD-1 in lung cancer", Clin. Pharmacol. Ther, 96, pp.214~223 (2014)
  39. Okudaira, K., "Blockade of B7-H1 or B7-DC induces an anti-tumor effect in a mouse pancreatic cancer model", Int. J. Oncol, 35, pp.741~749 (2009)
  40. Liu, X, "B7DC", PDL2 promotes tumor immunity by a PD-1-independent mechanism, 2003, pp.197, 1721~1730
  41. Brahmer, J. R, "Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates", J. Clin. Oncol, 28, pp.3167~3175 (2010)
  42. Topalian, S. L, "Safety, activity, and immune correlates of anti-PD-1 antibody in cancer", N. Engl. J. Med, 366, pp.2443~2454 (2012)
  43. Hamid, O., "Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma", N. Engl. J. Med, 369, pp.134~144 (2013)
  44. Brahmer, J. R., "Safety and activity of anti-PD-L1 antibody in patients with advanced cancer", N. Engl. J. Med, 366, pp.2455~2465 (2012)
  45. Wolchok, J. D., "Nivolumab plus ipilimumab in advanced melanoma", N. Engl. J. Med, 369, pp.122~133 (2013)
  46. Spranger, S., "Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(＋) T cells", Sci. Transl. Med, 5, pp.200ra116~ (2013)
  47. Tafuri, A., "ICOS is essential for effective T-helper-cell responses", Nature, 409, pp.105~109 (2001)
  48. McAdam, A. J, "ICOS is critical for CD40-mediated antibody class switching", Nature, 409, pp.102~105 (2001)
  49. Parry, R. V, "CD28 and inducible costimulatory protein Src homology 2 binding domains show distinct regulation of phosphatidylinositol 3-kinase, Bcl-xL, and IL-2 expression in primary human CD4 T lymphocytes", J. Immunol, 171, pp.166~174 (2003)
  50. Gigoux, M, "Inducible costimulator promotes helper T-cell differentiation through phosphoinositide 3-kinase", Proc. Natl. Acad. Sci. U. S. A, 106, pp.20371~20376 (2009)
  51. Gigoux, M., "Inducible costimulator facilitates T-dependent B cell activation by augmenting IL-4 translation", Mol. Immunol, 59, pp.46~54 (2014)
  52. Rolf, J., "Signaling pathways in T follicular helper cells", J. Immunol, 184, pp.6563~6568 (2010)
  53. Greenwald, R. J, "The B7 family revisited", Annu. Rev. Immunol, 23, pp.515~548 (2005)
  54. Lee, H., "Peripheral blood gene expression of B7 and CD28 family members associated with tumor progression and microscopic lymphovascular invasion in colon cancer patients", J. Cancer Res. Clin. Oncol, 136, pp.1445~1452 (2010)
  55. Bogunovic, D., "Immune profile and mitotic index of metastatic melanoma lesions enhance clinical staging in predicting patient survival", Proc. Natl. Acad. Sci. U. S. A, 106, pp.20429~20434 (2009)
  56. Tamura, H., "Expression of functional B7-H2 and B7.2 costimulatory molecules and their prognostic implications in de novo acute myeloid leukemia", Clin. Cancer Res, 11, pp.5708~5717 (2005)
  57. Martin-Orozco, N, "Melanoma cells express ICOS ligand to promote the activation and expansion of T-regulatory cells", Cancer Res, 70, pp.9581~9590 (2010)
  58. Sim, G. C., "IL-2 therapy promotes suppressive ICOS＋ Treg expansion in melanoma patients", J. Clin. Invest, 124, pp.99~110 (2014)
  59. Carthon, B. C., "Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial", Clin. Cancer Res, 16, pp.2861~2871 (2010)
  60. Vonderheide, R. H, "Tremelimumab in combination with exemestane in patients with advanced breast cancer and treatment-associated modulation of inducible costimulator expression on patient T cells", Clin. Cancer Res, 16, pp.3485~3494 (2010)
  61. Fu, T., "The ICOS", ICOSL pathway is required for optimal antitumor responses mediated by anti-CTLA-4 therapy, 2011, pp.71, 5445~5454
  62. Guedan, S., "ICOS-based chimeric antigen receptors program bipolar TH17", TH1 cells, 2014, pp.124, 1070~1080
  63. Hashiguchi, 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, 105, pp.10495~10500 (2008)
  64. Leitner, J., "B7-H3 is a potent inhibitor of human T-cell activation: No evidence for B7-H3 and TREML2 interaction", Eur. J. Immunol, 39, pp.1754~1764 (2009)
  65. Chapoval, A. I., "B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production", Nat. Immunol, 2, pp.269~274 (2001)
  66. Suh, W. K, "The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses", Nat. Immunol, 4, pp.899~906 (2003)
  67. Wang, L, "B7-H3 promotes acute and chronic allograft rejection", Eur. J. Immunol, 35, pp.428~438 (2005)
  68. Prasad, D. V, "Murine B7-H3 is a negative regulator of T cells", J. Immunol, 173, pp.2500~2506 (2004)
  69. Collins, M., "The B7 family of immune-regulatory ligands", Genome Biol, 6, pp.223~ (2005)
  70. Loos, M, "B7-h3 and its role in antitumor immunity", Clin. Dev. Immunol, pp.683875~ (2010)
  71. Luo, L, "B7-H3 enhances tumor immunity in vivo by costimulating rapid clonal expansion of antigen-specific CD8＋ cytolytic T cells", J. Immunol, 173, pp.5445~5450 (2004)
  72. Sun, X., "Mouse B7-H3 induces antitumor immunity", Gene Ther, 10, pp.1728~1734 (2003)
  73. Loos, M, "Expression of the costimulatory molecule B7-H3 is associated with prolonged survival in human pancreatic cancer", BMC Cancer, 9, pp.463~ (2009)
  74. Wu, C. P, "Relationship between co-stimulatory molecule B7-H3 expression and gastric carcinoma histology and prognosis", World J. Gastroenterol, 12, pp.457~459 (2006)
  75. Zang, X, "B7-H3 and B7x are highly expressed in human prostate cancer and associated with disease spread and poor outcome", Proc. Natl. Acad. Sci. U. S. A, 104, pp.19458~19463 (2007)
  76. Roth, T. J., "B7-H3 ligand expression by prostate cancer: a novel marker of prognosis and potential target for therapy", Cancer Res, 67, pp.7893~7900 (2007)
  77. Sun, J., "Clinical significance and regulation of the costimulatory molecule B7-H3 in human colorectal carcinoma", Cancer Immunol. Immunother, 59, pp.1163~1171 (2010)
  78. Xu, H., "MicroRNA miR-29 modulates expression of immunoinhibitory molecule B7-H3: potential implications for immune based therapy of human solid tumors", Cancer Res, 69, pp.6275~6281 (2009)
  79. Sica, G. L, "B7-H4, a molecule of the B7 family, negatively regulates T cell immunity", Immunity, 18, pp.849~861 (2003)
  80. Choi, I. H., "Genomic organization and expression analysis of B7-H4, an immune inhibitory molecule of the B7 family", J. Immunol, 171, pp.4650~4654 (2003)
  81. Kryczek, I., "B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma", J. Exp. Med, 203, pp.871~881 (2006)
  82. Zang, X., "B7x: a widely expressed B7 family member that inhibits T cell activation", Proc. Natl. Acad. Sci. U. S. A, 100, pp.10388~10392 (2003)
  83. Ou, D., "Suppression of human T-cell responses to beta-cells by activation of B7-H4 pathway", Cell Transplant, 15, pp.399~410 (2006)
  84. Suh, W. K., "Generation and characterization of B7-H4", B7S1, Mol. Cell Biol, pp.2006, 26[DOI]
  85. Zhu, G., "B7-H4-deficient mice display augmented neutrophil- mediated innate immunity", Blood, 113, pp.1759~1767 (2009)
  86. Leung, J, "Host B7-H4 regulates antitumor T cell responses through inhibition of myeloid-derived suppressor cells in a 4T1 tumor transplantation model", J. Immunol, 190, pp.6651~6661 (2013)
  87. Cheng, L., "B7-H4 expression promotes tumorigenesis in ovarian cancer", Int. J. Gynecol. Cancer, 19, pp.1481~1486 (2009)
  88. Salceda, S, "The immunomodulatory protein B7-H4 is overexpressed in breast and ovarian cancers and promotes epithelial cell transformation", Exp. Cell Res, 306, pp.128~141 (2005)
  89. Sedy, J. R, "B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator", Nat. Immunol, 6, pp.90~98 (2005)
  90. Abadi, Y. M, "Host b7x promotes pulmonary metastasis of breast cancer", J. Immunol, 190, pp.3806~3814 (2013)
  91. He, C., "The inhibitory role of b7-h4 in antitumor immunity: association with cancer progression and survival", Clin. Dev. Immunol, pp.695834~ (2011)
  92. Tringler, B, "B7-h4 is highly expressed in ductal and lobular breast cancer", Clin. Cancer Res, 11, pp.1842~1848 (2005)
  93. Bignotti, E., "Differential gene expression profiles between tumor biopsies and short-term primary cultures of ovarian serous carcinomas: identification of novel molecular biomarkers for early diagnosis and therapy", Gynecol. Oncol, 103, pp.405~416 (2006)
  94. Le, H. K., "Gemcitabine directly inhibits myeloid derived suppressor cells in BALB", c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice, 2009, pp.9, 900~909
  95. Dangaj, D., "Novel recombinant human b7-h4 antibodies overcome tumoral immune escape to potentiate T-cell antitumor responses", Cancer Res, 73, pp.4820~4829 (2013)
  96. Le, M., "VISTA Regulates the Development of Protective Antitumor Immunity", Cancer Res, 74, pp.1933~1944 (2014)
  97. Zhao, R., "HHLA2 is a member of the B7 family and inhibits human CD4 and CD8 T-cell function", Proc. Natl. Acad. Sci. U. S. A, 110, pp.9879~9884 (2013)
  98. Brandt, C. S., "The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans", J. Exp. Med, 206, pp.1495~1503 (2009)

관련 논문AI추천

Co-Stimulatory Receptors in Cancers and Their Implications for Cancer Immunotherapy박수형, Seongju Jeong대한면역학회 · Immune Network2020 · 제20권 제1호Emerging Co-signaling Networks in T Cell Immune Regulation정근옥, 최인학대한면역학회 · Immune Network2013 · 제13권 제5호Perspectives on immune checkpoint ligands: expression, regulation, and clinical implications하상준, Jihyun Moon, Yoo Min Oh생화학분자생물학회 · BMB Reports2021 · 제54권 제8호4-1BB (CD137), an inducible costimulatory receptor, as a specific target for cancer therapy권병세, Dass S. Vinay생화학분자생물학회 · BMB Reports2014 · 제47권 제3호Updates to Clinical Information on Anticancer Immunotherapy양재욱, 최은주한국임상약학회 · 한국임상약학회지2018 · 제28권 제1호VISTA-mediated immune evasion in cancerKim Tae Kon, Zhang Raymond J.생화학분자생물학회 · Experimental and Molecular Medicine2024 · 제56권

이 간행물의 다른 논문 (6건)

Gut Microbiota-Derived Short-Chain Fatty Acids, T Cells, and Inflammation박정호, 김명후, 김창한pp. 277-288Reference Values for Peripheral Blood Lymphocyte Subsets in a Healthy Korean Population이수진, 이종균, 강용원, 이윤아, 맹형건, 최종범pp. 289-295Simultaneous Inhibition of CXCR4 and VLA-4 Exhibits Combinatorial Effect in Overcoming Stroma-Mediated Chemotherapy Resistance in Mantle Cell Lymphoma Cells김유리, 엄기성pp. 296-306Characterization of Proinflammatory Responses and Innate Signaling Activation in Macrophages Infected with Mycobacterium scrofulaceumJoy G. Lee, 박정규, 김태성, 육재민, 양미소, 김기혜, 조은경, 김진만pp. 307-320SUMO Proteins are not Involved in TGF-β1-induced, Smad3/4-mediated Germline α Transcription, but PIASy Suppresses it in CH12F3-2A B Cells박석래, 김평현, 이상훈, 오상묵, 유영춘, 박정환, 이정림pp. 321-327
원문 보기