Reprogramming tumor-infiltrating dendritic cells for CD103+CD8+ Mucosal T-cell differentiation and breast cancer rejection

Cancer Immunology Research

Volumn 2, Issue 5, 2014, Pages 487-500

  Wu, Te Chia ^a,d   Xu, Kangling ^a,d   Banchereau, Romain ^a   Marches, Florentina ^a   Yu, Chun I ^a   Martinek, Jan ^a   Anguiano, Esperanza ^a   Pedroza Gonzalez, Alexander ^a   Snipes, G Jackson ^b   O'Shaughnessy, Joyce ^c   Nishimura, Stephen ^e   Liu, Yong Jun ^a   Pascual, Virginia ^a   Banchereau, Jacques ^a   Oh, Sangkon ^a   Palucka, Karolina ^a,f  

^a BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

^b BAYLOR UNIVERSITY MEDICAL CENTER   (United States)

^c TEXAS ONCOLOGY   (United States)

^d BAYLOR UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; CURDLAN; DECTIN 1; LECTIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; BREAST TUMOR; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CYTOLOGY; DENDRITIC CELL; DISEASE MODEL; DRUG EFFECTS; FEMALE; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; MUCOSA; PATHOLOGY; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; TH2 CELL; TUMOR CELL LINE;

ANIMALS; BETA-GLUCANS; BREAST NEOPLASMS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LECTINS, C-TYPE; MICE; MUCOUS MEMBRANE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TH2 CELLS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84905820953     PISSN: 23266066     EISSN: 23266074     Source Type: Journal    
DOI: 10.1158/2326-6066.CIR-13-0217     Document Type: Article

References (50)

1. DeNardo DG, Andreu P, Coussens LM. Interactions between lymphocytes and myeloid cells regulate proversus anti-tumor immunity. Cancer Metastasis Rev 2010; 29:309-16.
2. + T cells that facilitate tumor development. J Exp Med 2007; 204:1037-47.
3. Pedroza-Gonzalez A, Xu K, Wu TC, Aspord C, Tindle S, Marches F, et al. Thymic stromal lymphopoietin fosters human breast tumor growth by promoting type 2 inflammation. J Exp Med 2011; 208:479-90.
4. Teschendorff AE, Gomez S, Arenas A, El-Ashry D, Schmidt M, Gehrmann M, et al. Improved prognostic classification of breast cancer defined by antagonistic activation patterns of immune response pathway modules. BMC Cancer 2010; 10:604.
5. Kristensen VN, Vaske CJ, Ursini-Siegel J, Van Loo P, Nordgard SH, Sachidanandam R, et al. Integrated molecular profiles of invasive breast tumors and ductal carcinoma in situ (DCIS) reveal differential vascular and interleukin signaling. Proc Natl Acad Sci U S A 2012; 109:2802-7.
6. De Monte L, Reni M, Tassi E, Clavenna D, Papa I, Recalde H, et al. Intratumor T helper type 2 cell infiltrate correlates with cancer-associated fibroblast thymic stromal lymphopoietin production and reduced survival in pancreatic cancer. J Exp Med 2011; 208:469-78.
7. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009; 16:91-102.
8. Terabe M, Berzofsky JA. Immunoregulatory T cells in tumor immunity. Curr Opin Immunol 2004; 16:157-62.
9. Zhang WJ, Li BH, Yang XZ, Li PD, Yuan Q, Liu XH, et al. IL-4-induced Stat6 activities affect apoptosis and gene expression in breast cancer cells. Cytokine 2008; 42:39-47.
10. Denardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF, et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011; 1:54-67.
11. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313: 1960-4.
12. Olkhanud PB, Rochman Y, Bodogai M, Malchinkhuu E, Wejksza K, Xu M, et al. Thymic stromal lymphopoietin is a key mediator of breast cancer progression. J Immunol 2011; 186:5656-62.
13. Gringhuis SI, den Dunnen J, Litjens M, van der Vlist M, Wevers B, Bruijns SC, et al. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat Immunol 2009; 10:203-13.
14. Baran J, Allendorf DJ, Hong F, Ross GD. Oral beta-glucan adjuvant therapy converts nonprotective Th2 response to protective Th1 cellmediated immune response in mammary tumor-bearing mice. Folia Histochem Cytobiol 2007; 45:107-14.
15. Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ, et al. Activation of the innate immunereceptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature 2011; 472:471-5.
16. + T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med 2013; 5:172ra20.
17. Obermoser G, Presnell S, Domico K, Xu H, Wang Y, Anguiano E, et al. Systems scale interactive exploration reveals quantitative and qualitative differences in response to influenza and pneumococcal vaccines. Immunity 2013; 38:831-44.
18. Min L, Isa SA, Fam WN, Sze SK, Beretta O, Mortellaro A, et al. Synergism between curdlan and GM-CSF confers a strong inflammatory signature to dendritic cells. J Immunol 2012; 188:1789-98.
19. Arima K, Watanabe N, Hanabuchi S, Chang M, Sun SC, Liu YJ. Distinct signal codes generate dendritic cell functional plasticity. Sci Signal 2010; 3:ra4.
20. Markovics JA, Araya J, Cambier S, Jablons D, Hill A, Wolters PJ, et al. Transcription of the transforming growth factor beta activating integrin beta8 subunit is regulated by SP3, AP-1, and the p38 pathway. J Biol Chem 2010; 285:24695-706.
21. Bell D, Chomarat P, Broyles D, Netto G, Harb GM, Lebecque S, et al. In breast carcinoma tissue, immature dendritic cells reside within the tumor, whereas mature dendritic cells are located in peritumoral areas. J Exp Med 1999; 190:1417-26.
22. Leibundgut-Landmann S, Osorio F, Brown GD, Reise Sousa C. Stimulation of dendritic cells via the dectin-1/Syk pathway allows priming of cytotoxic T-cell responses. Blood 2008; 112:4971-80.
23. Dubsky P, Saito H, Leogier M, Dantin C, Connolly JE, Banchereau J, et al. IL-15-induced human DC efficiently prime melanoma-specific naive CD8(+) T cells to differentiate into CTL. Eur J Immunol 2007; 37:1678-90.
24. Romano E, Cotari JW, Barreira da Silva R, Betts BC, Chung DJ, Avogadri F, et al. Human Langerhans cells use an IL-15R-alpha/IL-15/pSTAT5-dependent mechanism to break T-cell tolerance against the self-differentiation tumor antigen WT1. Blood 2012; 119: 5182-90.
25. + T cells responding to antigen without requiring knowledge of epitope specificities. Blood 2007; 110:201-10.
26. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, et al. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 1994; 372:190-3.
27. Agace WW, Higgins JM, Sadasivan B, Brenner MB, Parker CM. Tlymphocyte-epithelial-cell interactions: integrin alpha(E)(CD103) beta(7), LEEP-CAM and chemokines. Curr Opin Cell Biol 2000; 12:563-8.
28. Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW, et al. Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 1999; 162:6641-9.
29. Le Floc'h A, Jalil A, Vergnon I, Le Maux Chansac B, Lazar V, Bismuth G, et al. Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J Exp Med 2007; 204:559-70.
30. Le Floc'h A, Jalil A, Franciszkiewicz K, Validire P, Vergnon I, Mami Chouaib F. Minimal engagement of CD103 oncytotoxicTlymphocytes with an E-cadherin-Fc molecule triggers lytic granule polarization via a phospholipase Cgamma-dependent pathway. Cancer Res 2011; 71: 328-38.
31. Parker CM, Cepek KL, Russell GJ, Shaw SK, Posnett DN, Schwarting R, et al. A family of beta 7 integrins on human mucosal lymphocytes. Proc Natl Acad Sci U S A 1992; 89:1924-8.
32. Rihs S, Walker C, Virchow JC Jr, Boer C, Kroegel C, Giri SN, et al. Differential expression of alpha E beta 7 integrins on bronchoalveolar lavage T lymphocyte subsets: regulation by alpha 4 beta 1-integrin crosslinking and TGF-beta. Am J Respir Cell Mol Biol 1996; 15:600-10.
33. + regulatory T cells in human thymus and periphery. Immunity 2008; 28:870-80.
34. Kitamura H, Cambier S, Somanath S, Barker T, Minagawa S, Markovics J, et al. Mouse and human lung fibroblasts regulate dendritic cell trafficking, airway inflammation, and fibrosis through integrin alphavbeta8-mediated activation of TGF-beta. J Clin Invest 2011; 121: 2863-75.
35. Li MO, Flavell RA. TGF-beta: a master of all T cell trades. Cell 2008; 134:392-404.
36. Dragicevic A, Dzopalic T, Vasilijic S, Vucevic D, Tomic S, Bozic B, et al. Signaling through Toll-like receptor 3 and Dectin-1 potentiates the capability of human monocyte-derived dendritic cells to promote Thelper 1 and T-helper 17 immune responses. Cytotherapy 2012; 14: 598-607.
37. Lin JY, Chen JS, Chen PC, Chung MH, Liu CY, Miaw SC, et al. Concurrent exposure to a dectin-1 agonist suppresses the Th2 response to epicutaneously introduced antigen in mice. J Biomed Sci 2013; 20:1.
38. Ohshima Y, Tanaka Y, Tozawa H, Takahashi Y, Maliszewski C, Delespesse G. Expression and function of OX40 ligand on human dendritic cells. J Immunol 1997; 159:3838-48.
39. Lewis KL, Caton ML, Bogunovic M, Greter M, Grajkowska LT, Ng D, et al. Notch2 receptor signaling controls functional differentiation of dendritic cells in the spleen and intestine. Immunity 2011; 35:780-91.
40. Vigne S, Palmer G, Lamacchia C, Martin P, Talabot-Ayer D, Rodriguez E, et al. IL-36R ligands are potent regulators of dendritic and T cells. Blood 2011; 118:5813-23.
41. + T cells. Blood 2012; 120: 3478-87.
42. Gresnigt MS, Rosler B, Jacobs CW, Becker KL, Joosten LA, van der Meer JW, et al. The IL-36 receptor pathway regulates Aspergillus fumigatus-induced Th1 and Th17 responses. Eur J Immunol 2012; 43: 416-26.
43. Agrawal S, Gupta S, Agrawal A. Human dendritic cells activated via dectin-1 are efficient at priming Th17, cytotoxic CD8 T and B cell responses. PLoS ONE 2010; 5:e13418.
44. Shaw SK, Brenner MB. The beta 7 integrins in mucosal homing and retention. Semin Immunol 1995; 7:335-42.
45. Sheridan BS, Lefrancois L. Regional and mucosal memory T cells. Nat Immunol 2011; 12:485-91.
46. El-Asady R, Yuan R, Liu K, Wang D, Gress RE, Lucas PJ, et al. TGF{beta}-dependent CD103 expression by CD8(+) T cells promotes selective destruction of the host intestinal epithelium during graftversus-host disease. J Exp Med 2005; 201:1647-57.
47. Yu CI, Becker C, Wang Y, Marches F, Helft J, Leboeuf M, et al. Human CD1c(+) dendritic cells drive the differentiation of CD103(+) CD8(+) mucosal effector T cells via the cytokine TGF-beta. Immunity 2013; 38:818-30.
48. Mullins DW, Sheasley SL, Ream RM, Bullock TN, Fu YX, Engelhard VH. Route of immunization with peptide-pulsed dendritic cells controls the distribution of memory and effector T cells in lymphoid tissues and determines the pattern of regional tumor control. J Exp Med 2003; 198: 1023-34.
49. Sheasley-O'Neill SL, Brinkman CC, Ferguson AR, Dispenza MC, Engelhard VH. Dendritic cell immunization route determines integrin expression and lymphoid and nonlymphoid tissue distribution of CD8 T cells. J Immunol 2007; 178:1512-22.
50. Mora JR, Bono MR, Manjunath N, Weninger W, Cavanagh LL, Rosemblatt M, et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 2003; 424:88-93.