Endogenous tumor-reactive CD8+ T cells are differentiated effector cells expressing high levels of CD11a and PD-1 but are unable to control tumor growth

OncoImmunology

Volumn 2, Issue 6, 2013, Pages

  Liu, Xin ^a   Gibbons, Rachel M ^b   Harrington, Susan M ^a   Krco, Christopher J ^a   Markovic, Svetomir N ^a   Kwon, Eugene D ^a,b   Dong, Haidong ^a,b  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

Antitumor immunity; CD11a; PD 1; T cell marker

Indexed keywords

CD11B ANTIGEN; CD18 ANTIGEN; CD3 ANTIGEN; CD31 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; FINGOLIMOD; GAMMA INTERFERON; GLYCOPROTEIN P 15095; HLA A2 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; KI 67 ANTIGEN; L SELECTIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MELAN A; PROGRAMMED DEATH 1 RECEPTOR; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGEN SPECIFICITY; ARTICLE; BREAST TUMOR; CANCER CONTROL; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL SURFACE; CELLULAR DISTRIBUTION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; DRUG MECHANISM; EFFECTOR CELL; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; IMMUNOLOGICAL MONITORING; IMMUNOPHENOTYPING; IMMUNOREACTIVITY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LYMPH NODE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTE SUBPOPULATION; MEMORY T LYMPHOCYTE; METASTASIS; MOUSE; NON DRAINING LYMPH NODE; NONHUMAN; PRIMARY TUMOR; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; TUMOR DRAINING LYMPH NODE; TUMOR IMMUNITY; UPREGULATION;

EID: 84886943680     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.23972     Document Type: Article

References (49)

1. Vesely MD, Kershaw MH, Schreiber RD, Smyth MJ. Natural innate and adaptive immunity to cancer. Annu Rev Immunol 2011; 29:235-71; PMID:21219185; http://dx.doi.org/10.1146/annurevimmunol- 031210-101324
2. Altman JD, Moss PA, Goulder PJ, Barouch DH, McHeyzer-Williams MG, Bell JI, et al. Phenotypic analysis of antigen-specific T lymphocytes. Science 1996; 274:94-6; PMID:8810254; http://dx.doi. org/10.1126/science.274.5284.94
3. Blohm U, Roth E, Brommer K, Dumrese T, Rosenthal FM, Pircher H. Lack of effector cell function and altered tetramer binding of tumor-infiltrating lymphocytes. J Immunol 2002; 169:5522-30; PMID:12421928
4. Pardoll DM. Immunology beats cancer: a blueprint for successful translation. Nat Immunol 2012; 13:1129-32; PMID:23160205; http://dx.doi.org/10.1038/ni.2392
5. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http://dx.doi.org/10.1056/NEJMoa1200694
6. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, 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
7. Evans R, Patzak I, Svensson L, De Filippo K, Jones K, McDowall A, et al. Integrins in immunity. J Cell Sci 2009; 122:215-25; PMID:19118214; http://dx.doi. org/10.1242/jcs.019117
8. Anikeeva N, Somersalo K, Sims TN, Thomas VK, Dustin ML, Sykulev Y. Distinct role of lymphocyte function-associated antigen-1 in mediating effective cytolytic activity by cytotoxic T lymphocytes. Proc Natl Acad Sci U S A 2005; 102:6437-42; PMID:15851656; http://dx.doi.org/10.1073/pnas.0502467102
9. Seki N, Brooks AD, Carter CR, Back TC, Parsoneault EM, Smyth MJ, et al. Tumor-specific CTL kill murine renal cancer cells using both perforin and Fas ligandmediated lysis in vitro, but cause tumor regression in vivo in the absence of perforin. J Immunol 2002; 168:3484-92; PMID:11907109
10. Lunsford KE, Koester MA, Eiring AM, Horne PH, Gao D, Bumgardner GL. Targeting LFA-1 and cd154 suppresses the in vivo activation and development of cytolytic (cd4-Independent) CD8+ T cells. J Immunol 2005; 175:7855-66; PMID:16339521
11. Schmits R, Kündig TM, Baker DM, Shumaker G, Simard JJ, Duncan G, et al. LFA-1-deficient mice show normal CTL responses to virus but fail to reject immunogenic tumor. J Exp Med 1996; 183:1415-26; PMID:8666900; http://dx.doi.org/10.1084/jem.183.4.1415
12. Rai D, Pham NL, Harty JT, Badovinac VP. Tracking the total CD8 T cell response to infection reveals substantial discordance in magnitude and kinetics between inbred and outbred hosts. J Immunol 2009; 183:7672-81; PMID:19933864; http://dx.doi.org/10.4049/jimmunol. 0902874
13. Smith C, Martinez M, Peet J, Khanna R. Differential outcome of IL-2/anti-IL-2 complex therapy on effector and memory CD8+ T cells following vaccination with an adenoviral vector encoding EBV epitopes. J Immunol 2011; 186:5784-90; PMID:21482735; http://dx.doi.org/10.4049/jimmunol.1003394
14. Schmidt NW, Butler NS, Badovinac VP, Harty JT. Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog 2010; 6:e1000998; PMID:20657824; http://dx.doi. org/10.1371/journal.ppat.1000998
15. Baitsch L, Baumgaertner P, Devêvre E, Raghav SK, Legat A, Barba L, et al. Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients. J Clin Invest 2011; 121:2350-60; PMID:21555851; http://dx.doi.org/10.1172/JCI46102
16. Barber DL, Wherry EJ, Masopust D, Zhu B, Allison JP, Sharpe AH, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006; 439:682-7; PMID:16382236; http://dx.doi. org/10.1038/nature04444
17. Thompson RH, Dong H, Lohse CM, Leibovich BC, Blute ML, Cheville JC, et al. PD-1 is expressed by tumor-infiltrating immune cells and is associated with poor outcome for patients with renal cell carcinoma. Clin Cancer Res 2007; 13:1757-61; PMID:17363529; http://dx.doi.org/10.1158/1078-0432.CCR-06-2599
18. Zhang L, Gajewski TF, Kline J. PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 2009; 114:1545-52; PMID:19417208; http://dx.doi.org/10.1182/blood-2009-03-206672
19. Mumprecht S, Schürch C, Schwaller J, Solenthaler M, Ochsenbein AF. Programmed death 1 signaling on chronic myeloid leukemia-specific T cells results in T-cell exhaustion and disease progression. Blood 2009; 114:1528-36; PMID:19420358; http://dx.doi. org/10.1182/blood-2008-09-179697
20. Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood 2009; 114:1537-44; PMID:19423728; http://dx.doi.org/10.1182/blood-2008-12-195792
21. Mueller KL, Daniels MA, Felthauser A, Kao C, Jameson SC, Shimizu Y. Cutting edge: LFA-1 integrindependent T cell adhesion is regulated by both ag specificity and sensitivity. J Immunol 2004; 173:2222-6; PMID:15294931
22. Crispe IN. Hepatic T cells and liver tolerance. Nat Rev Immunol 2003; 3:51-62; PMID:12511875; http://dx.doi.org/10.1038/nri981
23. Dong H, Zhu G, Tamada K, Flies DB, van Deursen JM, Chen L. B7-H1 determines accumulation and deletion of intrahepatic CD8(+) T lymphocytes. Immunity 2004; 20:327-36; PMID:15030776; http://dx.doi.org/10.1016/S1074-7613(04)00050-0
24. Brinkmann V, Pinschewer DD, Feng L, Chen S. FTY720: altered lymphocyte traffic results in allograft protection. Transplantation 2001; 72:764-9; PMID:11571432; http://dx.doi.org/10.1097/00007890-200109150-00002
25. Lewis JD, Shearer MH, Kennedy RC, Bright RK. Surrogate tumor antigen vaccination induces tumor-specific immunity and the rejection of spontaneous metastases. Cancer Res 2005; 65:2938-46; PMID:15805297; http://dx.doi.org/10.1158/0008-5472.CAN-04-2874
26. Scholzen T, Gerdes J. The Ki-67 protein: from the known and the unknown. J Cell Physiol 2000; 182:311-22; PMID:10653597; http://dx.doi.org/10.1002/(SICI)1097-4652(200003)182:3<311::AIDJCP1> 3.0.CO;2-9
27. Harrington LE, Galvan M, Baum LG, Altman JD, Ahmed R. Differentiating between memory and effector CD8 T cells by altered expression of cell surface O-glycans. J Exp Med 2000; 191:1241-6; PMID:10748241; http://dx.doi.org/10.1084/jem.191.7.1241
28. Truneh A, Albert F, Golstein P, Schmitt-Verhulst AM. Early steps of lymphocyte activation bypassed by synergy between calcium ionophores and phorbol ester. Nature 1985; 313:318-20; PMID:3918270; http://dx.doi.org/10.1038/313318a0
29. Boggio K, Nicoletti G, Di Carlo E, Cavallo F, Landuzzi L, Melani C, et al. Interleukin 12-mediated prevention of spontaneous mammary adenocarcinomas in two lines of Her-2/neu transgenic mice. J Exp Med 1998; 188:589-96; PMID:9687535; http://dx.doi. org/10.1084/jem.188.3.589
30. Nava-Parada P, Forni G, Knutson KL, Pease LR, Celis E. Peptide vaccine given with a Toll-like receptor agonist is effective for the treatment and prevention of spontaneous breast tumors. Cancer Res 2007; 67:1326-34; PMID:17283170; http://dx.doi. org/10.1158/0008-5472.CAN-06-3290
31. Mace EM, Zhang J, Siminovitch KA, Takei F. Elucidation of the integrin LFA-1-mediated signaling pathway of actin polarization in natural killer cells. Blood 2010; 116:1272-9; PMID:20472831; http://dx.doi.org/10.1182/blood-2009-12-261487
32. Barber DF, Faure M, Long EO. LFA-1 contributes an early signal for NK cell cytotoxicity. J Immunol 2004; 173:3653-9; PMID:15356110
33. Melero I, Balboa MA, Alonso JL, Yagüe E, Pivel JP, Sanchez-Madrid F, et al. Signaling through the LFA-1 leucocyte integrin actively regulates intercellular adhesion and tumor necrosis factor-alpha production in natural killer cells. Eur J Immunol 1993; 23:1859-65; PMID:8344347; http://dx.doi.org/10.1002/eji.1830230819
34. Perez OD, Mitchell D, Jager GC, South S, Murriel C, McBride J, et al. Leukocyte functional antigen 1 lowers T cell activation thresholds and signaling through cytohesin-1 and Jun-activating binding protein 1. Nat Immunol 2003; 4:1083-92; PMID:14528303; http://dx.doi.org/10.1038/ni984
35. Borthwick NJ, Akbar AA, Buckley C, Pilling D, Salmon M, Jewell AP, et al. Transendothelial migration confers a survival advantage to activated T lymphocytes: role of LFA-1/ICAM-1 interactions. Clin Exp Immunol 2003; 134:246-52; PMID:14616784; http://dx.doi.org/10.1046/j.1365-2249.2003.02298.x
36. Gibbons RM, Liu X, Pulko V, Harrington SM, Krco CJ, Kwon ED, et al. B7-H1 limits the entry of effector CD8(+) T cells to the memory pool by upregulating Bim. Oncoimmunology 2012; 1:1061-73; PMID:23170254; http://dx.doi.org/10.4161/onci.20850
37. Lazarevic V, Glimcher LH. T-bet in disease. Nat Immunol 2011; 12:597-606; PMID:21685955; http://dx.doi.org/10.1038/ni.2059
38. Thompson ED, Enriquez HL, Fu YX, Engelhard VH. Tumor masses support naive T cell infiltration, activation, and differentiation into effectors. J Exp Med 2010; 207:1791-804; PMID:20660615; http://dx.doi. org/10.1084/jem.20092454
39. Fuertes MB, Kacha AK, Kline J, Woo SR, Kranz DM, Murphy KM, et al. Host type I IFN signals are required for antitumor CD8+ T cell responses through CD8alpha+ dendritic cells. J Exp Med 2011; 208:2005-16; PMID:21930765; http://dx.doi. org/10.1084/jem.20101159
40. Diamond MS, Kinder M, Matsushita H, Mashayekhi M, Dunn GP, Archambault JM, et al. Type I interferon is selectively required by dendritic cells for immune rejection of tumors. J Exp Med 2011; 208:1989-2003; PMID:21930769; http://dx.doi.org/10.1084/jem.20101158
41. Katou F, Ohtani H, Watanabe Y, Nakayama T, Yoshie O, Hashimoto K. Differing phenotypes between intraepithelial and stromal lymphocytes in early-stage tongue cancer. Cancer Res 2007; 67:11195-201; PMID:18056444; http://dx.doi.org/10.1158/0008-5472.CAN-07-2637
42. Dustin ML, Springer TA. T-cell receptor cross-linking transiently stimulates adhesiveness through LFA-1. Nature 1989; 341:619-24; PMID:2477710; http://dx.doi.org/10.1038/341619a0
43. Sheppard KA, Fitz LJ, Lee JM, Benander C, George JA, Wooters J, et al. PD-1 inhibits T-cell receptor induced phosphorylation of the ZAP70/CD3zeta signalosome and downstream signaling to PKCtheta. FEBS Lett 2004; 574:37-41; PMID:15358536; http://dx.doi. org/10.1016/j.febslet.2004.07.083
44. Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med 2002; 8:793-800; PMID:12091876
45. Dong H, Chen L. B7-H1 pathway and its role in the evasion of tumor immunity. J Mol Med (Berl) 2003; 81:281-7; PMID:12721664
46. Blank C, Brown I, Peterson AC, Spiotto M, Iwai Y, Honjo T, et al. PD-L1/B7H-1 inhibits the effector phase of tumor rejection by T cell receptor (TCR) transgenic CD8+ T cells. Cancer Res 2004; 64:1140-5; PMID:14871849; http://dx.doi.org/10.1158/0008-5472.CAN-03-3259
47. Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N. 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 2002; 99:12293-7; PMID:12218188; http://dx.doi. org/10.1073/pnas.192461099
48. Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, et al. Durable cancer regression off-treatment and effective re-induction therapy with an anti-PD-1 antibody. Clin Cancer Res 2013; 19:462-8; PMID:23169436; http://dx.doi.org/10.1158/1078-0432.CCR-12-2625
49. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, Roederer M, et al. Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 2003; 281:65-78; PMID:14580882; http://dx.doi.org/10.1016/S0022-1759(03)00265-5