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PMID: 18802064 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Induction of a VLA-2 (CD49b)-expressing effector T cell population by a cell-based neuroblastoma vaccine expressing CD137L.

Journal of immunology (Baltimore, Md. : 1950) ·Vol. 181 ·No. 7 ·2008-10-01 ·Pages 4621-31

Yan X, Johnson BD, Orentas RJ

Abstract

In malignancies where no universally expressed dominant Ag exists, the use of tumor cell-based vaccines has been proposed. We have modified a mouse neuroblastoma cell line to express either CD80 (B7.1), CD137L (4-1BBL), or both receptors on the tumor cell surface. Vaccines expressing both induce a strong T cell response that is unique in that among responding CD8 T cells, a T effector memory cell (T(EM)) response arises in which a large number of the T(EM) express the alpha-chain of VLA-2, CD49b. We demonstrate using both in vitro and in vivo assays that the CD49b(+) CD8 T cell population is a far more potent antitumor effector cell population than nonfractionated CD8 or CD49b(-) CD8 T cells and that CD49b on vaccine-induced CD8 T cells mediates invasion of a collagen matrix. In in vivo rechallenge studies, CD49b(+) T cells no longer expanded, indicating that CD49b T(EM) expansion is restricted to the initial response to vaccine. To demonstrate a mechanistic link between the expression of costimulatory molecules on the vaccine and CD49b on responding T cells, we stimulated naive T cells in vitro with artificial APC expressing different combinations of anti-CD3, anti-CD28, and CD137L. Although some mRNA encoding CD49b was induced by combining anti-CD3 with anti-CD28 or CD137L, the highest level was induced when all three signals were present. This indicates that CD49b expression results from additive costimulation and that the level of CD49b message serves as an indicator of the effectiveness of T cell activation by a cell-based vaccine.

MeSH Terms
4-1BB Ligand/administration & dosage,biosynthesis,genetics,immunology Animals CD4-Positive T-Lymphocytes/immunology,metabolism CD8-Positive T-Lymphocytes/cytology,immunology,transplantation Cancer Vaccines/administration & dosage,biosynthesis,genetics,immunology Cell Differentiation/immunology Cell Line, Tumor Cell Proliferation Coculture Techniques Humans Immunotherapy, Adoptive Integrin alpha2/biosynthesis,genetics K562 Cells Lymphocyte Activation/immunology Mice Mice, Inbred A Neuroblastoma/metabolism,prevention & control T-Lymphocyte Subsets/cytology,immunology,metabolism,transplantation Tumor Necrosis Factor Receptor Superfamily, Member 9/metabolism
Chemicals
4-1BB Ligand Cancer Vaccines Integrin alpha2 Tumor Necrosis Factor Receptor Superfamily, Member 9
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Yan Xiaocai
Department of Pediatrics, Section of Hematology-Oncology, Medical College of Wisconsin Milwaukee, WI 53226, USA.
Johnson Bryon D
Orentas Rimas J
References (51)
51 references, click to expand
  1. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children's Cancer Group.
    N Engl J Med. 1999 Oct 14;341(16):1165-73 PMID: 10519894
  2. Biochemical characterization of VLA-1 and VLA-2. Cell surface heterodimers on activated T cells.
    J Biol Chem. 1985 Dec 5;260(28):15246-52 PMID: 2415516
  3. Integrin alpha(2)beta(1) (VLA-2) is a principal receptor used by neutrophils for locomotion in extravascular tissue.
    Blood. 2000 Mar 1;95(5):1804-9 PMID: 10688841
  4. Distinct recognition of collagen subtypes by alpha(1)beta(1) and alpha(2)beta(1) integrins. Alpha(1)beta(1) mediates cell adhesion to type XIII collagen.
    J Biol Chem. 2000 Mar 17;275(11):8255-61 PMID: 10713152
  5. Regulation of inflammation by collagen-binding integrins alpha1beta1 and alpha2beta1 in models of hypersensitivity and arthritis.
    J Clin Invest. 2000 Mar;105(6):721-9 PMID: 10727440
  6. Potent costimulation of effector T lymphocytes by human collagen type I.
    J Immunol. 2000 Nov 1;165(9):4935-40 PMID: 11046019
  7. Differential effects of CD18, CD29, and CD49 integrin subunit inhibition on neutrophil migration in pulmonary inflammation.
    J Immunol. 2001 Mar 1;166(5):3484-90 PMID: 11207307
  8. Characterization of Inherited Differences in Transcription of the Human Integrin alpha 2 Gene.
    J Biol Chem. 2001 Jun 29;276(26):23518-24 PMID: 11313353
  9. Expression of the DX5 antigen on CD8+ T cells is associated with activation and subsequent cell death or memory during influenza virus infection.
    Eur J Immunol. 2001 May;31(5):1523-30 PMID: 11465109
  10. 4-1BB ligand induces cell division, sustains survival, and enhances effector function of CD4 and CD8 T cells with similar efficacy.
    J Immunol. 2001 Aug 1;167(3):1313-24 PMID: 11466348
  11. 4-1BBL enhances anti-tumor responses in the presence or absence of CD28 but CD28 is required for protective immunity against parental tumors.
    Cell Immunol. 2001 May 25;210(1):56-65 PMID: 11485353
  12. Provision of antigen and CD137 signaling breaks immunological ignorance, promoting regression of poorly immunogenic tumors.
    J Clin Invest. 2002 Mar;109(5):651-9 PMID: 11877473
  13. Signaling through NK cell-associated CD137 promotes both helper function for CD8+ cytolytic T cells and responsiveness to IL-2 but not cytolytic activity.
    J Immunol. 2002 Oct 15;169(8):4230-6 PMID: 12370353
  14. High-risk neuroblastoma in Ontario: a report of experience from 1989 to 1995.
    J Pediatr Hematol Oncol. 2003 Jan;25(1):8-13 PMID: 12544767
  15. Dual expression of CD80 and CD86 produces a tumor vaccine superior to single expression of either molecule.
    Cell Immunol. 2003 Mar;222(1):15-26 PMID: 12798304
  16. Graft-versus-tumor effect in a patient with advanced neuroblastoma who received HLA haplo-identical bone marrow transplantation.
    Bone Marrow Transplant. 2003 Jul;32(1):103-6 PMID: 12815485
  17. 4-1BB enhances CD8+ T cell expansion by regulating cell cycle progression through changes in expression of cyclins D and E and cyclin-dependent kinase inhibitor p27kip1.
    Eur J Immunol. 2003 Aug;33(8):2133-41 PMID: 12884287
  18. Expression and functional importance of collagen-binding integrins, alpha 1 beta 1 and alpha 2 beta 1, on virus-activated T cells.
    J Immunol. 2003 Sep 15;171(6):2804-11 PMID: 12960301
  19. Ligation of CD137 receptor prevents and reverses established anergy of CD8+ cytolytic T lymphocytes in vivo.
    Blood. 2004 Jan 1;103(1):177-84 PMID: 12969968
  20. Mast cell-mediated inflammatory responses require the alpha 2 beta 1 integrin.
    Blood. 2004 Mar 15;103(6):2214-20 PMID: 14645004
  21. Genetic variation responsible for mouse strain differences in integrin alpha 2 expression is associated with altered platelet responses to collagen.
    Blood. 2004 May 1;103(9):3396-402 PMID: 14739220
  22. Murine CD8 lymphocyte expansion in vitro by artificial antigen-presenting cells expressing CD137L (4-1BBL) is superior to CD28, and CD137L expressed on neuroblastoma expands CD8 tumour-reactive effector cells in vivo.
    Immunology. 2004 May;112(1):105-16 PMID: 15096190
  23. Endothelial cells use alpha 2 beta 1 integrin as a laminin receptor.
    J Cell Biol. 1989 Nov;109(5):2455-62 PMID: 2530239
  24. The human integrin VLA-2 is a collagen receptor on some cells and a collagen/laminin receptor on others.
    Proc Natl Acad Sci U S A. 1989 Dec;86(24):9906-10 PMID: 2557634
  25. In vitro and in vivo consequences of VLA-2 expression on rhabdomyosarcoma cells.
    Science. 1991 Mar 29;251(5001):1600-2 PMID: 2011740
  26. Functional role of alpha 2/beta 1 and alpha 4/beta 1 integrins in leukocyte intercellular adhesion induced through the common beta 1 subunit.
    Eur J Immunol. 1992 Dec;22(12):3111-9 PMID: 1446704
  27. Interaction of type IV collagen with the isolated integrins alpha 1 beta 1 and alpha 2 beta 1.
    Eur J Biochem. 1993 Jul 1;215(1):151-9 PMID: 8344274
  28. Local and systemic effects of an allogeneic tumor cell vaccine combining transgenic human lymphotactin with interleukin-2 in patients with advanced or refractory neuroblastoma.
    Blood. 2003 Mar 1;101(5):1718-26 PMID: 12406881
  29. The human alpha 2 integrin gene promoter. Identification of positive and negative regulatory elements important for cell-type and developmentally restricted gene expression.
    J Biol Chem. 1994 Jan 7;269(1):463-9 PMID: 8276836
  30. Identification of collagen and laminin receptor integrins on murine T lymphocytes.
    Eur J Immunol. 1994 Sep;24(9):2000-5 PMID: 7522156
  31. Regulation of alpha 2 integrin gene expression in cells with megakaryocytic features: a common theme of three necessary elements.
    Blood. 1995 Oct 15;86(8):3006-14 PMID: 7579393
  32. Collagens: molecular biology, diseases, and potentials for therapy.
    Annu Rev Biochem. 1995;64:403-34 PMID: 7574488
  33. Amplification of tumor immunity by gene transfer of the co-stimulatory 4-1BB ligand: synergy with the CD28 co-stimulatory pathway.
    Eur J Immunol. 1998 Mar;28(3):1116-21 PMID: 9541607
  34. CD28-independent, TRAF2-dependent costimulation of resting T cells by 4-1BB ligand.
    J Exp Med. 1998 Jun 1;187(11):1849-62 PMID: 9607925
  35. Role of the I-domain in collagen binding specificity and activation of the integrins alpha1beta1 and alpha2beta1.
    J Cell Physiol. 1998 Sep;176(3):634-41 PMID: 9699516
  36. IL-2 adenovector-transduced autologous tumor cells induce antitumor immune responses in patients with neuroblastoma.
    Blood. 1998 Sep 15;92(6):1941-9 PMID: 9731051
  37. 4-1BB costimulation promotes human T cell adhesion to fibronectin.
    Cell Immunol. 1999 Feb 25;192(1):13-23 PMID: 10066342
  38. Cutting edge: 4-1BB is a bona fide CD8 T cell survival signal.
    J Immunol. 1999 May 1;162(9):5037-40 PMID: 10227968
  39. Mouse NKR-P1B, a novel NK1.1 antigen with inhibitory function.
    J Immunol. 1999 May 15;162(10):5917-23 PMID: 10229828
  40. Immunogenicity of human neuroblastoma.
    Ann N Y Acad Sci. 2004 Dec;1028:69-80 PMID: 15650233
  41. Cross-linking of 4-1BB activates TCR-signaling pathways in CD8+ T lymphocytes.
    J Immunol. 2005 Feb 15;174(4):1898-905 PMID: 15699116
  42. Neuroblastoma cells transiently transfected to simultaneously express the co-stimulatory molecules CD54, CD80, CD86, and CD137L generate antitumor immunity in mice.
    J Immunother. 2005 Sep-Oct;28(5):449-60 PMID: 16113601
  43. Collagen type I signaling reduces the expression and the function of human receptor activator of nuclear factor-kappa B ligand (RANKL) in T lymphocytes.
    Eur J Immunol. 2005 Dec;35(12):3673-82 PMID: 16304637
  44. Integrin alpha2beta1 regulates neutrophil recruitment and inflammatory activity in experimental colitis in mice.
    Inflamm Bowel Dis. 2006 Mar;12(3):172-7 PMID: 16534417
  45. Molecular and genetic basis for strain-dependent NK1.1 alloreactivity of mouse NK cells.
    J Immunol. 2006 Jun 15;176(12):7511-24 PMID: 16751398
  46. Functional specialization of memory Th cells revealed by expression of integrin CD49b.
    J Immunol. 2006 Jul 15;177(2):968-75 PMID: 16818752
  47. CD25+ regulatory T cell inhibition enhances vaccine-induced immunity to neuroblastoma.
    J Immunother. 2007 Feb-Mar;30(2):203-14 PMID: 17471167
  48. Phase I trial of vaccination with autologous neuroblastoma tumor cells genetically modified to secrete IL-2 and lymphotactin.
    J Immunother. 2007 Feb-Mar;30(2):227-33 PMID: 17471169
  49. Neuroblastoma.
    Lancet. 2007 Jun 23;369(9579):2106-20 PMID: 17586306
  50. 4-1BB is superior to CD28 costimulation for generating CD8+ cytotoxic lymphocytes for adoptive immunotherapy.
    J Immunol. 2007 Oct 1;179(7):4910-8 PMID: 17878391
  51. NK markers are expressed on a high percentage of virus-specific CD8+ and CD4+ T cells.
    J Immunol. 2000 Feb 15;164(4):2009-15 PMID: 10657652
Article Info
Journal
Journal of immunology (Baltimore, Md. : 1950)
Abbr.
J Immunol
ISSN
1550-6606
Published
2008-10-01
Pages
4621-31
Language
English
Region
United States
NLM ID
2985117R
PMCID
PMC2975591
Subset
IM
Grants
NCI NIH HHS · R01 CA100030 · United States
NCI NIH HHS · R01 CA100030-02 · United States
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