Intrinsically de-sialylated CD103+ CD8 T cells mediate beneficial anti-glioma immune responses

Cancer Immunology, Immunotherapy

Volumn 63, Issue 9, 2014, Pages 911-924

  Jouanneau, Emmanuel ^a,b   Black, Keith L ^a   Veiga, Lucia ^a   Cordner, Ryan ^a   Goverdhana, Shyam ^a   Zhai, Yuying ^a   Zhang, Xiao Xue ^a   Panwar, Akanksha ^a   Mardiros, Armen ^a,c   Wang, Hongqiang ^a   Gragg, Ashley ^a   Zandian, Mandana ^a   Irvin, Dwain K ^a   Wheeler, Christopher J ^a  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

Anti tumor T cell; Cancer immunotherapy; DC vaccine; Glioma; Sialylation

Indexed keywords

CANCER VACCINE; GALACTOSYL(BETA 1,3) N ACETYLGALACTOSAMINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; N ACETYLGALACTOSAMINE; SIALIC ACID; SIALIDASE; UNCLASSIFIED DRUG; ALPHA E INTEGRINS; ALPHA INTEGRIN; BETA-GALACTOSIDE ALPHA-2,3-SIALYLTRANSFERASE; LEUKOCYTE ANTIGEN; SIALYLTRANSFERASE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER SURVIVAL; CD103+T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG RESPONSE; FEMALE; FLOW CYTOMETRY; GLIOMA; HISTOCOMPATIBILITY COMPLEX; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IN VITRO STUDY; INTRINSIC ACTIVITY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIALYLATION; T LYMPHOCYTE; TUMOR INVASION; VACCINE FAILURE; ADOPTIVE IMMUNOTHERAPY; ANIMAL; BRAIN NEOPLASMS; C57BL MOUSE; CLINICAL TRIAL; DENDRITIC CELL; GLIOBLASTOMA; IMMUNOLOGY; METABOLISM; PHASE 1 CLINICAL TRIAL; PHASE 2 CLINICAL TRIAL; PROCEDURES;

ANIMALS; ANTIGENS, CD; BRAIN NEOPLASMS; CANCER VACCINES; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; FEMALE; GLIOBLASTOMA; GLIOMA; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTEGRIN ALPHA CHAINS; MICE; MICE, INBRED C57BL; NEURAMINIDASE; SIALYLTRANSFERASES;

EID: 84906937482     PISSN: 03407004     EISSN: 14320851     Source Type: Journal    
DOI: 10.1007/s00262-014-1559-2     Document Type: Article

References (43)

1. Stupp R, Hegi ME, Gilbert MR, Chakravarti A (2007) Chemoradiotherapy in malignant glioma: standard of care and future directions. J Clin Oncol 25:4127-4136 (Pubitemid 47492957)
2. Yu JS, Wheeler CJ, Zeltzer PM et al (2001) Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. Cancer Res 61:842-847 (Pubitemid 32175145)
3. Kikuchi T, Akasaki Y, Irie M, Homma S, Abe T, Ohno T (2001) Results of a phase I clinical trial of vaccination of glioma patients with fusions of dendritic and glioma cells. Cancer Immunol Immunother 50:337-344 (Pubitemid 32835343)
4. Yamanaka R, Abe T, Yajima N, Tsuchiya N, Homma J, Kobayashi T, Narita M, Takahashi M, Tanaka R (2003) Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial. Br J Cancer 89:1172-1179 (Pubitemid 37363398)
5. Yu JS, Liu G, Ying H, Yong WH, Black KL, Wheeler CJ (2004) Vaccination with tumor lysate-pulsed dendritic cells elicits antigen-specific cytotoxic T cells in patients with malignant glioma. Cancer Res 64:4973-4979 (Pubitemid 38924545)
6. Kikuchi T, Akasaki Y, Abe T, Fukuda T, Saotome H, Ryan JL, Kufe DW, Ohno T (2004) Vaccination of glioma patients with fusions of dendritic and glioma cells and recombinant human interleukin 12. J Immunother 27:452-459 (Pubitemid 39447353)
7. Rutkowski S, De Vleeschouwer S, Kaempgen E et al (2004) Surgery and adjuvant dendritic cell-based tumour vaccination for patients with relapsed malignant glioma, a feasibility study. Br J Cancer 91:1656-1662 (Pubitemid 39546137)
8. Yamanaka R, Homma J, Yajima N et al (2005) Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. Clin Cancer Res 11:4160-4167 (Pubitemid 40791581)
9. Liau LM, Prins RM, Kiertscher SM et al (2005) Dendritic cell vaccination in glioblastoma patients induces systemic and intracranial T-cell responses modulated by the local central nervous system tumor microenvironment. Clin Cancer Res 11: 5515-5525 (Pubitemid 41060828)
10. De Vleeschouwer S, Fieuws S, Rutkowski S et al (2008) Postoperative adjuvant dendritic cell-based immunotherapy in patients with relapsed glioblastoma multiforme. Clin Cancer Res 14:3098-3104
11. Wheeler CJ, Black KL, Liu G et al (2008) Vaccination elicits correlated immune and clinical responses in glioblastoma multiforme patients. Cancer Res 68:5955-5964
12. Wheeler CJ, Das A, Liu G, Yu JS, Black KL (2004) Clinical responsiveness of glioblastoma multiform to chemotherapy after vaccination. Clin Cancer Res 10:5316-5326 (Pubitemid 39100466)
13. Okada H, Kalinski P, Ueda R et al (2011) Induction of CD8+ T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with α-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol 29:330-336
14. Wheeler CJ, Black KL, Liu G, Ying H, Yu JS, Zhang W, Lee PK (2003) Thymic CD8+ T cell production strongly influences tumor antigen recognition and age-dependent glioma mortality. J Immunol 171:4927-4933 (Pubitemid 37310617)
15. Schon MP, Arya A, Murphy EA et al (1999) Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 162:6641-6649 (Pubitemid 29309388)
16. McFarland RD, Douek DC, Koup RA, Picker LJ (2000) Identification of a human recent thymic emigrant phenotype. Proc Natl Acad Sci USA 97:4215-4220 (Pubitemid 30226113)
17. Annunziato F, Cosmi L, Liotta F et al (2006) CXCR3 and αEβ7 integrin identify a subset of CD8+ mature thymocytes that share phenotypic and functional properties with CD8+ gut intraepithelial lymphocytes. Gut 55:961-968 (Pubitemid 43962607)
18. Scott CL, Aumeunier AM, Mowat AM (2011) Intestinal CD103+ dendritic cells: master regulators of tolerance? Trends Immunol 32:412-419. doi:10.1016/j.it.2011.06.003
19. Li L, Kim S, Herndon J et al (2012) Cross-dressed CD8α+/CD103+ dendritic cells prime CD8+ T cells following vaccination. Proc Natl Acad Sci USA 109:12716-12721
20. Sung SS, Fu SM, Rose CE Jr, Gaskin F, Ju ST, Beaty SR (2006) A major lung CD103 (alphaE)-beta7 integrin-positive epithelial dendritic cell population expressing Langerin and tight junction proteins. J Immunol 176:2161-2172 (Pubitemid 43201663)
21. Allez M, Brimnes J, Dotan I, Mayer L (2002) Expansion of CD8+ T cells with regulatory function after interaction with intestinal epithelial cells. Gastroenterology 123:1516-1526 (Pubitemid 35231652)
22. Annacker O, Coombes JL, Malmstrom V, Uhlig HH, Bourne T, Johansson-Lindbom B, Agace WW, Parker CM, Powrie F (2005) Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J Exp Med 202:1051-1061 (Pubitemid 41464499)
23. Liu Y, Lan Q, Lu L et al (2014) Phenotypic and functional characteristic of a newly identified CD8+ Foxp3-CD103+ regulatory T cells. J Mol Cell Biol 6:81-92
24. Calzascia T, Masson F, Di Berardino-Besson W, Contassot E, Wilmotte R, Aurrand-Lions M, Rüegg C, Dietrich PY, Walker PR (2005) Homing phenotypes of tumor-specific CD8 T cells are predetermined at the tumor site by crosspresenting APCs. Immunity 22:175-184
25. Masson F, Calzascia T, Di Berardino-Besson W, de Tribolet N, Dietrich PY, Walker PR (2007) Brain microenvironment promotes the final functional maturation of tumor-specific effector CD8+ T cells. J Immunol 179:845-853
26. Wakim LM, Woodward-Davis A, Bevan MJ (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc Natl Acad Sci USA 107:17872-17879
27. Casey KA, Fraser KA, Schenkel JM et al (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J Immunol 188:4866-4875
28. + T lymphocyte homeostasis by modulating O-glycan biosynthesis. Immunity 12:273-283
29. Moody AM, Chui D, Reche PA, Priatel JJ, Marth JD, Reinherz EL (2001) Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell 107:501-512 (Pubitemid 33152785)
30. Daniels MA, Devine L, Miller JD, Moser JM, Lukacher AE, Altman JD, Kavathas P, Hogquist KA, Jameson SC (2001) CD8 binding to MHC class I molecules is influenced by T cell maturation and glycosylation. Immunity 15:1051-1061 (Pubitemid 34075383)
31. Brennan PJ, Saouaf SJ, Van Dyken S, Marth JD, Li B, Bhandoola A, Greene MI (2006) Sialylation regulates peripheral tolerance in CD4+ T cells. Int Immunol 18:627-635 (Pubitemid 43779052)
32. Irvin DK, Jouanneau E, Duvall G et al (2010) T cells enhance stem-like properties and conditional malignancy in gliomas. PLoSONE 5:e10974
33. Phuphanich S, Wheeler CJ, Rudnick JD et al (2013) Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma. Cancer Immunol Immunother 62:125-135
34. Prins RM, Odesa SK, Liau LM (2003) Immunotherapeutic targeting of shared melanoma-associated antigens in a murine glioma model. Cancer Res 63:8487-8491 (Pubitemid 37549505)
35. Prins RM, Incardona F, Lau R, Lee P, Claus S, Zhang W, Black KL, Wheeler CJ (2004) Characterization of defective CD4-CD8-T cells in murine tumors generated independent of antigen specificity. J Immunol 172:1602-1611 (Pubitemid 38116807)
36. Jouanneau E, Poujol D, Gulia S, Le Mercier I, Blay JY, Belin MF, Puisieux I (2006) Dendritic cells are essential for priming but inefficient for boosting antitumour immune response in an orthotopic murine glioma model. Cancer Immunol Immunother 55:254-267 (Pubitemid 41682574)
37. Shai R, Shi T, Kremen TJ, Horvath S, Liau LM, Cloughesy TF, Mischel PS, Nelson SF (2003) Gene expression profiling identifies molecular subtypes of gliomas. Oncogene 22:4918-4923 (Pubitemid 36981282)
38. Sempowski GD, Gooding ME, Liao HX, Le PT, Haynes BF (2002) T cell receptor excision circle assessment of thymopoiesis in aging mice. Mol Immunol 38:841-848 (Pubitemid 34260886)
39. Pappu BP, Shrikant PA (2004) Alteration of cell surface sialylation regulates antigen-induced naive CD8+ T cell responses. J Immunol 173:275-284 (Pubitemid 38797352)
40. Lee YC, Kojima N, Wada E, Kurosawa N, Nakaoka T, Hamamoto T, Tsuji S (1994) Cloning and expression of cDNA for a new type of Gal beta 1,3GalNAc alpha 2,3-sialyltransferase. J Biol Chem 269:10028-10033
41. Wu W, Harley PH, Punt JA, Sharrow SO, Kearse KP (1996) Identification of CD8 as a peanut agglutinin (PNA) receptor molecule on immature thymocytes. J Exp Med 184:759-764 (Pubitemid 26324131)
42. Prins RM, Graf MR, Merchant RE, Black KL, Wheeler CJ (2003) Deficits in thymic function and output of recent thymic emigrant T cells during intracranial glioma progression. J Neurooncol 64:45-54 (Pubitemid 36992459)
43. Wheeler CJ, Black KL (2011) Vaccines for glioblastoma and high-grade glioma. Expert Rev Vaccines 10:875-886