2,473
Views
39
CrossRef citations to date
0
Altmetric
Original Research

Tumor-infiltrating Tim-3+ T cells proliferate avidly except when PD-1 is co-expressed: Evidence for intracellular cross talk

, , , , , , , & show all
Article: e1200778 | Received 16 May 2016, Accepted 06 Jun 2016, Published online: 11 Oct 2016

References

  • Ferris RL. Immunology and Immunotherapy of Head and Neck Cancer. J Clin Oncol 2015; 33:3293-304; PMID:26351330; http://dx.doi.org/10.1200/JCO.2015.61.1509
  • Li J, Jie HB, Lei Y, Gildener-Leapman N, Trivedi S, Green T, Kane LP, Ferris RL. PD-1/SHP-2 inhibits Tc1/Th1 phenotypic responses and the activation of T cells in the tumor microenvironment. Cancer Res 2015; 75:508-18; PMID:25480946; http://dx.doi.org/10.1158/0008-5472.CAN-14-1215
  • Strauss L, Bergmann C, Gooding W, Johnson JT, Whiteside TL. 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 2007; 13:6301-11; PMID:17975141; http://dx.doi.org/10.1158/1078-0432.CCR-07-1403
  • Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 12:253-68; PMID:22437938; http://dx.doi.org/10.1038/nri3175
  • Li J, Srivastava RM, Ettyreddy A, Ferris RL. Cetuximab ameliorates suppressive phenotypes of myeloid antigen presenting cells in head and neck cancer patients. J Immunother Cancer 2015; 3:54; PMID:26579227; http://dx.doi.org/10.1186/s40425-015-0097-6
  • Jie HB, Schuler PJ, Lee SC, Srivastava RM, Argiris A, Ferrone S, Whiteside TL, Ferris RL. CTLA-4(+) Regulatory T Cells Increased in Cetuximab-Treated Head and Neck Cancer Patients Suppress NK Cell Cytotoxicity and Correlate with Poor Prognosis. Cancer Res 2015; 75:2200-10; PMID:25832655; http://dx.doi.org/10.1158/0008-5472.CAN-14-2788
  • Wherry EJ, Ha SJ, Kaech SM, Haining WN, Sarkar S, Kalia V, Subramaniam S, Blattman JN, Barber DL, Ahmed R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007; 27:670-84; PMID:17950003; http://dx.doi.org/10.1016/j.immuni.2007.09.006
  • Blackburn SD, Shin H, Haining WN, Zou T, Workman CJ, Polley A, Betts MR, Freeman GJ, Vignali DA, Wherry EJ. Coregulation of CD8(+) T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 2009; 10:29-37; PMID:19043418; http://dx.doi.org/10.1038/ni.1679
  • Jie HB, Gildener-Leapman N, Li J, Srivastava RM, Gibson SP, Whiteside TL, Ferris RL. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer 2013; 109:2629-35; PMID:24169351; http://dx.doi.org/10.1038/bjc.2013.645
  • Lyford-Pike S, Peng S, Young GD, Taube JM, Westra WH, Akpeng B, Bruno TC, Richmon JD, Wang H, Bishop JA et al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 2013; 73:1733-41; PMID:23288508; http://dx.doi.org/10.1158/0008-5472.CAN-12-2384
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12:252-64; PMID:22437870; http://dx.doi.org/10.1038/nrc3239
  • Lipson EJ, Drake CG. Ipilimumab: an anti-CTLA-4 antibody for metastatic melanoma. Clin Cancer Res 2011; 17:6958-62; PMID:21900389; http://dx.doi.org/10.1158/1078-0432.CCR-11-1595
  • Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
  • Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-33; PMID:23724867; http://dx.doi.org/10.1056/NEJMoa1302369
  • Fourcade J, Sun Z, Benallaoua M, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Kuchroo V, Zarour HM. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med 2010; 207:2175-86; PMID:20819923; http://dx.doi.org/10.1084/jem.20100637
  • Sakuishi K, Apetoh L, Sullivan JM, Blazar BR, Kuchroo VK, Anderson AC. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 2010; 207:2187-94; PMID:20819927; http://dx.doi.org/10.1084/jem.20100643
  • Badoual C, Hans S, Merillon N, Van Ryswick C, Ravel P, Benhamouda N, Levionnois E, Nizard M, Si-Mohamed A, Besnier N et al. PD-1-expressing tumor-infiltrating T cells are a favorable prognostic biomarker in HPV-associated head and neck cancer. Cancer Res 2013; 73:128-38; PMID:23135914; http://dx.doi.org/10.1158/0008-5472.CAN-12-2606
  • Legat A, Speiser DE, Pircher H, Zehn D, Fuertes Marraco SA. Inhibitory Receptor Expression Depends More Dominantly on Differentiation and Activation than “Exhaustion” of Human CD8 T Cells. Front Immunol 2013; 4:455; PMID:24391639; http://dx.doi.org/10.3389/fimmu.2013.00455
  • Utzschneider DT, Legat A, Fuertes Marraco SA, Carrie L, Luescher I, Speiser DE, Zehn D. T cells maintain an exhausted phenotype after antigen withdrawal and population reexpansion. Nat Immunol 2013; 14:603-10; PMID:23644506; http://dx.doi.org/10.1038/ni.2606
  • Jin HT, Anderson AC, Tan WG, West EE, Ha SJ, Araki K, Freeman GJ, Kuchroo VK, Ahmed R. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci U S A 2010; 107:14733-8; PMID:20679213; http://dx.doi.org/10.1073/pnas.1009731107
  • Gros A, Robbins PF, Yao X, Li YF, Turcotte S, Tran E, Wunderlich JR, Mixon A, Farid S, Dudley ME et al. PD-1 identifies the patient-specific CD8(+) tumor-reactive repertoire infiltrating human tumors. J Clin Invest 2014; 124:2246-59; PMID:24667641; http://dx.doi.org/10.1172/JCI73639
  • Wherry EJ. T cell exhaustion. Nat Immunol 2011; 12:492-9; PMID:21739672; http://dx.doi.org/10.1038/ni.2035
  • Shin H, Blackburn SD, Intlekofer AM, Kao C, Angelosanto JM, Reiner SL, Wherry EJ. A role for the transcriptional repressor Blimp-1 in CD8(+) T cell exhaustion during chronic viral infection. Immunity 2009; 31:309-20; PMID:19664943; http://dx.doi.org/10.1016/j.immuni.2009.06.019
  • Quigley M, Pereyra F, Nilsson B, Porichis F, Fonseca C, Eichbaum Q, Julg B, Jesneck JL, Brosnahan K, Imam S et al. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat Med 2010; 16:1147-51; PMID:20890291; http://dx.doi.org/10.1038/nm.2232
  • Paley MA, Kroy DC, Odorizzi PM, Johnnidis JB, Dolfi DV, Barnett BE, Bikoff EK, Robertson EJ, Lauer GM, Reiner SL et al. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 2012; 338:1220-5; PMID:23197535; http://dx.doi.org/10.1126/science.1229620
  • Lee J, Su EW, Zhu C, Hainline S, Phuah J, Moroco JA, Smithgall TE, Kuchroo VK, Kane LP. Phosphotyrosine-dependent coupling of Tim-3 to T-cell receptor signaling pathways. Mol Cell Biol 2011; 31:3963-74; PMID:21807895; http://dx.doi.org/10.1128/MCB.05297-11
  • Li J, Jie HB, Lei Y, Gildener-Leapman N, Trivedi S, Green T, Kane LP, Ferris RL. PD-1/SHP-2 negatively regulate Tc1/Th1 phenotypic responses and activation of T cells in the tumor microenvironment. Cancer Res 2015; 75(3):508-518; PMID:25480946; http://dx.doi.org/10.1158/0008-5472.CAN-14-1215
  • Jones RB, Ndhlovu LC, Barbour JD, Sheth PM, Jha AR, Long BR, Wong JC, Satkunarajah M, Schweneker M, Chapman JM et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 2008; 205:2763-79; PMID:19001139; http://dx.doi.org/10.1084/jem.20081398
  • Kaye J, Porcelli S, Tite J, Jones B, Janeway CA, Jr. Both a monoclonal antibody and antisera specific for determinants unique to individual cloned helper T cell lines can substitute for antigen and antigen-presenting cells in the activation of T cells. J Exp Med 1983; 158:836-56; PMID:6193236; http://dx.doi.org/10.1084/jem.158.3.836
  • Agata Y, Kawasaki A, Nishimura H, Ishida Y, Tsubata T, Yagita H, Honjo T. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol 1996; 8:765-72; PMID:8671665; http://dx.doi.org/10.1093/intimm/8.5.765
  • Mujib S, Jones RB, Lo C, Aidarus N, Clayton K, Sakhdari A, Benko E, Kovacs C, Ostrowski MA. Antigen-Independent Induction of Tim-3 Expression on Human T Cells by the Common gamma-Chain Cytokines IL-2, IL-7, IL-15, and IL-21 Is Associated with Proliferation and Is Dependent on the Phosphoinositide 3-Kinase Pathway. J Immunol 2012; 188:3745-56; PMID:22422881; http://dx.doi.org/10.4049/jimmunol.1102609
  • Zajac AJ, Blattman JN, Murali-Krishna K, Sourdive DJD, Suresh M, Altman JD, Ahmed R. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med 1998; 188:2205-13; PMID:9858507; http://dx.doi.org/10.1084/jem.188.12.2205
  • Gallimore A, Glithero A, Godkin A, Tissot AC, Pluckthun A, Elliott T, Hengartner H, Zinkernagel R. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I peptide complexes. J Exp Med 1998; 187:1383-93; PMID:9565631; http://dx.doi.org/10.1084/jem.187.9.1383
  • Crawford A, Angelosanto JM, Kao C, Doering TA, Odorizzi PM, Barnett BE, Wherry EJ. Molecular and transcriptional basis of CD4(+) T cell dysfunction during chronic infection. Immunity 2014; 40:289-302; PMID:24530057; http://dx.doi.org/10.1016/j.immuni.2014.01.005
  • Blackburn SD, Shin H, Freeman GJ, Wherry EJ. Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade. Proc Natl Acad Sci U S A 2008; 105:15016-21; PMID:18809920; http://dx.doi.org/10.1073/pnas.0801497105
  • Wang SF, Fouquet S, Chapon M, Salmon H, Regnier F, Labroquere K, Badoual C, Damotte D, Validire P, Maubec E et al. Early T Cell Signalling Is Reversibly Altered in PD-1(+) T Lymphocytes Infiltrating Human Tumors. Plos One 2011; 6:e17621; PMID:21408177; http://dx.doi.org/10.1371/journal.pone.0017621
  • Yokosuka T, Takamatsu M, Kobayashi-Imanishi W, Hashimoto-Tane A, Azuma M, Saito T. Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 2012; 209:1201-17; PMID:22641383; http://dx.doi.org/10.1084/jem.20112741
  • Ferris RL, Lu B, Kane LP. Too Much of a Good Thing? Tim-3 and TCR Signaling in T Cell Exhaustion. J Immunol 2014; 193:1525-30; PMID:25086175; http://dx.doi.org/10.4049/jimmunol.1400557
  • 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; 206:3015-29; PMID:20008522; http://dx.doi.org/10.1084/jem.20090847
  • Andrade Filho PA, Lopez-Albaitero A, Gooding W, Ferris RL. Novel immunogenic HLA-A*0201-restricted epidermal growth factor receptor-specific T-cell epitope in head and neck cancer patients. J Immunother 2010; 33:83-91; PMID:19952953; http://dx.doi.org/10.1097/CJI.0b013e3181b8f421

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.