T-cell immunoglobulin mucin 3 blockade drives an antitumor immune response in head and neck cancer

Molecular Oncology

Volumn 11, Issue 2, 2017, Pages 235-247

  Liu, Jian Feng ^a   Ma, Si Rui ^a   Mao, Liang ^a   Bu, Lin Lin ^a   Yu, Guang Tao ^a   Li, Yi Cun ^a   Huang, Cong Fa ^a   Deng, Wei Wei ^a   Kulkarni, Ashok B ^b   Zhang, Wen Feng ^a   Sun, Zhi Jun ^a  

^a WUHAN UNIVERSITY   (China)

^b NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

effector T cells; head and neck squamous cell carcinoma; immunotherapy; myeloid derived suppressor cells; T cell immunoglobulin mucin 3

Indexed keywords

MUCIN 3; TUMOR PROTEIN;

ANIMAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; EXPERIMENTAL NEOPLASM; FEMALE; HEAD AND NECK TUMOR; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; MOUSE; MYELOID-DERIVED SUPPRESSOR CELL; PATHOLOGY;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNITY, CELLULAR; MALE; MICE; MICE, KNOCKOUT; MUCIN-3; MYELOID-DERIVED SUPPRESSOR CELLS; NEOPLASM PROTEINS; NEOPLASMS, EXPERIMENTAL;

EID: 85021409000     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1002/1878-0261.12029     Document Type: Article

References (48)

1. Anderson AC, Anderson DE, Bregoli L, Hastings WD, Kassam N, Lei C, Chandwaskar R, Karman J, Su EW, Hirashima M et al. (2007) Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318, 1141–1143.
2. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P et al. (2007) Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13, 1050– 1059.
3. Argiris A, Karamouzis MV, Raben D, Ferris RL (2008) Head and neck cancer. Lancet 371, 1695–1709.
4. Baruah P, Lee M, Odutoye T, Williamson P, Hyde N, Kaski JC and Dumitriu IE (2012) Decreased levels of alternative co-stimulatory receptors OX40 and 4-1BB characterise T cells from head and neck cancer patients. Immunobiology 217, 669–675.
5. Bauernhofer T, Kuss I, Henderson B, Baum AS and Whiteside TL (2003) Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur J Immunol 33, 119–124.
6. Bian Y, Hall B, Sun ZJ, Molinolo A, Chen W, Gutkind JS, Waes CV and Kulkarni AB (2012) Loss of TGF-beta signaling and PTEN promotes head and neck squamous cell carcinoma through cellular senescence evasion and cancer-related inflammation. Oncogene 31, 3322–3332.
7. Bronte V, Brandau S, Chen SH, Colombo MP, Frey AB, Greten TF, Mandruzzato S, Murray PJ, Ochoa A, Ostrand-Rosenberg S et al. (2016) Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun 7, 12150.
8. Camus M, Tosolini M, Mlecnik B, Pages F, Kirilovsky A, Berger A, Costes A, Bindea G, Charoentong P, Bruneval P et al. (2009) Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res 69, 2685–2693.
9. Cao B, Zhu L, Zhu S, Li D, Zhang C, Xu C and Zhang S (2010) Genetic variations and haplotypes in TIM-3 gene and the risk of gastric cancer. Cancer Immunol Immunother 59, 1851–1857.
10. De Costa AM, Schuyler CA, Walker DD and Young MR (2012) Characterization of the evolution of immune phenotype during the development and progression of squamous cell carcinoma of the head and neck. Cancer Immunol Immunother 61, 927–939.
11. Eisen MB, Spellman PT, Brown PO and Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. P Natl Acad Sci USA 95, 14863–14868.
12. Farren MR, Mace T, Geyer S, Mikhail S, Wu C, Ciombor KK, Tahiri S, Ahn D, Noonan AM, Villalona-Calero MA et al. (2016) Systemic immune activity predicts overall survival in treatment naive patients with metastatic pancreatic cancer. Clini Cancer Res 22, 2565–2574.
13. Ferris RL (2015) Immunology and immunotherapy of head and neck cancer. J Clin Oncol 33, 3293–3304.
14. Ferris RL, Whiteside TL and Ferrone S (2006) Immune escape associated with functional defects in antigen-processing machinery in head and neck cancer. Clin Cancer Res 12, 3890–3895.
15. Finn OJ (2012) Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann Oncol 23(Suppl 8), viii6–viii9.
16. Fourcade J, Sun Z, Benallaoua M, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Kuchroo V and Zarour HM (2010) Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med 207, 2175–2186.
17. Freeman GJ, Casasnovas JM, Umetsu DT and DeKruyff RH (2010) TIM genes: a family of cell surface phosphatidylserine receptors that regulate innate and adaptive immunity. Immunol Rev 235, 172–189.
18. Gabrilovich DI and Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9, 162–174.
19. ´-fluoro oligonucleotide aptamer by HT-SELEX for cancer immunotherapy. Oncotarget 7, 4522–4530.
20. Huang YH, Zhu C, Kondo Y, Anderson AC, Gandhi A, Russell A, Dougan SK, Petersen BS, Melum E, Pertel T et al. (2015) CEACAM1 regulates TIM-3-mediated tolerance and exhaustion. Nature 517, 386–390.
21. Kloss S, Chambron N, Gardlowski T, Arseniev L, Koch J, Esser R, Glienke W, Seitz O and Kohl U (2015) Increased sMICA and TGFbeta levels in HNSCC patients impair NKG2D-dependent functionality of activated NK cells. Oncoimmunology 4, e1055993.
22. Koyama S, Akbay EA, Li YY, Herter-Sprie GS, Buczkowski KA, Richards WG, Gandhi L, Redig AJ, Rodig SJ, Asahina H et al. (2016) Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat Commun 7, 10501.
23. Leemans CR, Braakhuis BJ and Brakenhoff RH (2011) The molecular biology of head and neck cancer. Nat Rev Cancer 11, 9–22.
24. Lopez-Albaitero A, Nayak JV, Ogino T, Machandia A, Gooding W, DeLeo AB, Ferrone S, Ferris RL (2006) Role of antigen-processing machinery in the in vitro resistance of squamous cell carcinoma of the head and neck cells to recognition by CTL. J Immunol, 176, 3402–3409.
25. Marur S, D’Souza G, Westra WH and Forastiere AA (2010) HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol 11, 781–789.
26. Monney L, Sabatos CA, Gaglia JL, Ryu A, Waldner H, Chernova T, Manning S, Greenfield EA, Coyle AJ, Sobel RA et al. (2002) Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415, 536–541.
27. Napolitano M, D’Alterio C, Cardone E, Trotta AM, Pecori B, Rega D, Pace U, Scala D, Scognamiglio G, Tatangelo F et al. (2015) Peripheral myeloid-derived suppressor and T regulatory PD-1 positive cells predict response to neoadjuvant short-course radiotherapy in rectal cancer patients. Oncotarget 6, 8261–8270.
28. Ngiow SF, Teng MW and Smyth MJ (2011a) Prospects for TIM3-targeted antitumor immunotherapy. Cancer Res 71, 6567–6571.
29. Ngiow SF, von Scheidt B, Akiba H, Yagita H, Teng MW and Smyth MJ (2011b) Anti-TIM3 antibody promotes T cell IFN-gamma-mediated antitumor immunity and suppresses established tumors. Cancer Res 71, 3540– 3551.
30. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, Barrette TR, Anstet MJ, Kincead-Beal C, Kulkarni P et al. (2007) Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 9, 166–180.
31. Sabatos CA, Chakravarti S, Cha E, Schubart A, Sanchez-Fueyo A, Zheng XX, Coyle AJ, Strom TB, Freeman GJ and Kuchroo VK (2003) Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol 4, 1102–1110.
32. Sakuishi K, Ngiow SF, Sullivan JM, Teng MW, Kuchroo VK, Smyth MJ and Anderson AC (2013) TIM3FOXP3 regulatory T cells are tissue-specific promoters of T-cell dysfunction in cancer. Oncoimmunology 2, e23849.
33. Saldanha AJ (2004) Java Treeview–extensible visualization of microarray data. Bioinformatics 20, 3246–3248.
34. Sathyanarayanan V and Neelapu SS (2015) Cancer immunotherapy: strategies for personalization and combinatorial approaches. Mol Oncol 9, 2043–2053.
35. Sharma P and Allison JP (2015) Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 161, 205–214.
36. Siegel R, Ma J, Zou Z and Jemal A (2014) Cancer statistics, 2014. CA Cancer J Clin 64, 9–29.
37. Sobin LH and Witteking C (2002) UICC TNM classification of malignant tumours. 6th edn. Wiley-Blackwell, Oxford.
38. Strauss L, Bergmann C, Gooding W, Johnson JT and Whiteside TL (2007) The frequency and suppressor function of CD4+CD25highFoxp3+ T cells in the circulation of patients with squamous cell carcinoma of the head and neck. Clin Cancer Res 13, 6301–6311.
39. Sun ZJ, Zhang L, Hall B, Bian Y, Gutkind JS and Kulkarni AB (2012) Chemopreventive and chemotherapeutic actions of mTOR inhibitor in genetically defined head and neck squamous cell carcinoma mouse model. Clin Cancer Res 18, 5304– 5313.
40. Trellakis S, Bruderek K, Hutte J, Elian M, Hoffmann TK, Lang S and Brandau S (2013) Granulocytic myeloid-derived suppressor cells are cryosensitive and their frequency does not correlate with serum concentrations of colony-stimulating factors in head and neck cancer. Innate Immun 19, 328–336.
41. Ugel S, Delpozzo F, Desantis G, Papalini F, Simonato F, Sonda N, Zilio S and Bronte V (2009) Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol 9, 470–481.
42. Vacchelli E, Aranda F, Eggermont A, Galon J, Sautes-Fridman C, Zitvogel L, Kroemer G and Galluzzi L (2014) Trial watch: tumor-targeting monoclonal antibodies in cancer therapy. Oncoimmunology 3, e27048.
43. Weed DT, Vella JL, Reis IM, De la Fuente AC, Gomez C, Sargi Z, Nazarian R, Califano J, Borrello I and Serafini P (2015) Tadalafil reduces myeloid-derived suppressor cells and regulatory T cells and promotes tumor immunity in patients with head and neck squamous cell carcinoma. Clin Cancer Res 21, 39–48.
44. Welsh JW, Seyedin SN, Cortez MA, Maity A and Hahn SM (2014) Galectin-1 and immune suppression during radiotherapy. Clin Cancer Res 20, 6230–6232.
45. Whiteside TL (2005) Immunobiology of head and neck cancer. Cancer Metastasis Rev 24, 95–105.
46. Yu GT, Bu LL, Zhao YY, Mao L, Deng WW, Wu TF, Zhang WF and Sun ZJ (2016) CTLA4 blockade reduces immature myeloid cells in head and neck squamous cell carcinoma. Oncoimmunology 5, e1151594.
47. Zheng H, Guo X, Tian Q, Li H and Zhu Y (2015) Distinct role of Tim-3 in systemic lupus erythematosus and clear cell renal cell carcinoma. Int J Clin Exp Med 8, 7029–7038.
48. Zhu C, Anderson AC, Schubart A, Xiong H, Imitola J, Khoury SJ, Zheng XX, Strom TB and Kuchroo VK (2005) The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6, 1245–1252.