Engineering lymph node homing of ex vivo-expanded human natural killer cells via trogocytosis of the chemokine receptor CCR7

Blood

Volumn 119, Issue 22, 2012, Pages 5164-5172

  Somanchi, Srinivas S ^a   Somanchi, Anitha ^a   Cooper, Laurence J N ^a,b   Lee, Dean A ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR7; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ADOPTIVE TRANSFER; ARTICLE; CELL ENGINEERING; CELL EXPANSION; CELL MIGRATION; CELL POPULATION; COCULTURE; GENE TRANSFER; HUMAN; HUMAN CELL; LYMPH NODE; LYMPH NODE HOMING; LYMPHOCYTE; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TROGOCYTOSIS;

EID: 84861906931     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-11-389924     Document Type: Article

References (50)

1. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? the example of natural killer cells. Science. 2011;331(6013):44-49.
2. Klingemann HG, Martinson J. Ex vivo expansion of natural killer cells for clinical applications. Cytotherapy. 2004;6(1):15-22.
3. Koehl U, Esser R, Zimmermann S, et al. Ex vivo expansion of highly purified NK cells for immunotherapy after haploidentical stem cell transplantation in children. Klin Padiatr. 2005;217(6):345-350.
4. Berg M, Lundqvist A, McCoy P Jr, et al. Clinical-grade ex vivo-expanded human natural killer cells up-regulate activating receptors and death receptor ligands and have enhanced cytolytic activity against tumor cells. Cytotherapy. 2009;11(3):341-355.
5. Iliopoulou EG, Kountourakis P, Karamouzis MV, et al. A phase I trial of adoptive transfer of allogeneic natural killer cells in patients with advanced non-small cell lung cancer. Cancer Immunol Immunother. 2010;59(12):1781-1789.
6. Fujisaki H, Kakuda H, Shimasaki N, et al. Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. Cancer Res. 2009;69(9): 4010-4017.
7. Somanchi SS, Senyukov VV, Denman CJ, Lee DA. Expansion, purification, and functional assessment of human peripheral blood NK cells. J Vis Exp. 2011;(48). pii:2540.
8. Denman CJ, Senyukov VV, Somanchi SS, et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One. 2012;7(1):e30264.
9. Imai C. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood. 2005;106(1):376-383.
10. Muller T, Uherek C, Maki G, et al. Expression of a CD20-specific chimeric antigen receptor enhances cytotoxic activity of NK cells and overcomes NK-resistance of lymphoma and leukemia cells. Cancer Immunol Immunother. 2008;57(3): 411-423.
11. Li L, Liu LN, Feller S, et al. Expression of chimeric antigen receptors in natural killer cells with a regulatory-compliant non-viral method. Cancer Gene Ther. 2010;17(3):147-154.
12. Rollins BJ. Inflammatory chemokines in cancer growth and progression. Eur J Cancer. 2006; 42(6):760-767.
13. Kakinuma T, Hwang ST. Chemokines, chemokine receptors, and cancer metastasis. J Leukoc Biol. 2006;79(4):639-651.
14. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer. 2004;4(7):540-550.
15. Forster R, Davalos-Misslitz AC, Rot A. CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol. 2008;8(5):362-371.
16. Pan MR, Hou MF, Chang HC, Hung WC. Cyclooxygenase-2 up-regulates CCR7 via EP2/ EP4 receptor signaling pathways to enhance lymphatic invasion of breast cancer cells. J Biol Chem. 2008;283(17):11155-11163.
17. Nakata B, Fukunaga S, Noda E, Amano R, Yamada N, Hirakawa K. Chemokine receptor CCR7 expression correlates with lymph node metastasis in pancreatic cancer. Oncology. 2008; 74(1-2):69-75.
18. Sancho M, Vieira JM, Casalou C, et al. Expression and function of the chemokine receptor CCR7 in thyroid carcinomas. J Endocrinol. 2006; 191(1):229-238.
19. Gunther K, Leier J, Henning G, et al. Prediction of lymph node metastasis in colorectal carcinoma by expressionof chemokine receptor CCR7. Int J Cancer. 2005;116(5):726-733.
20. Shang ZJ, Liu K, Shao Z. Expression of chemokine receptor CCR7 is associated with cervical lymph node metastasis of oral squamous cell carcinoma. Oral Oncol. 2009;45(6):480-485.
21. Fang L, Lee VC, Cha E, Zhang H, Hwang ST. CCR7 regulates B16 murine melanoma cell tumorigenesis in skin. J Leukoc Biol. 2008;84(4): 965-972.
22. Rehm A, Mensen A, Schradi K, et al. Cooperative function of CCR7 and lymphotoxin in the formation of a lymphoma-permissive niche within murine secondary lymphoid organs. Blood. 2011; 118(4):1020-1033.
23. Berahovich RD, Lai NL, Wei Z, Lanier LL, Schall TJ. Evidence for NK cell subsets based on chemokine receptor expression. J Immunol. 2006; 177(11):7833-7840.
24. Uherek C, Tonn T, Uherek B, et al. Retargeting of natural killer-cell cytolytic activity to ErbB2- expressing cancer cells results in efficient and selective tumor cell destruction. Blood. 2002; 100(4):1265-1273.
25. Altvater B, Landmeier S, Pscherer S, et al. 2B4 (CD244) signaling by recombinant antigen-specific chimeric receptors costimulates natural killer cell activation to leukemia and neuroblastoma cells. Clin Cancer Res. 2009;15(15):4857-4866.
26. Marcenaro E, Cantoni C, Pesce S, et al. Uptake of CCR7 and acquisition of migratory properties by human KIR+ NK cells interacting with monocyte- derived DC or EBV cell lines: regulation by KIR/HLA-class I interaction. Blood. 2009;114(19): 4108-4116.
27. Carlin LM, Eleme K, McCann FE, Davis DM. Intercellular transfer and supramolecular organization of human leukocyte antigen C at inhibitory natural killer cell immune synapses. J Exp Med. 2001;194(10):1507-1517.
28. Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol. 2003;4(9):815.
29. Bona C, Robineaux R, Anteunis A, Heuclin C, Astesano A. Transfer of antigen from macrophages to lymphocytes, II: immunological significance of the transfer of lipopolysaccharide. Immunology. 1973;24(5):831-840.
30. Tabiasco J, Espinosa E, Hudrisier D, Joly E, Fournie JJ, Vercellone A. Active trans-synaptic capture of membrane fragments by natural killer cells. Eur J Immunol. 2002;32(5):1502-1508.
31. HoWangYin KY, Caumartin J, Favier B, et al. Proper regrafting of Ig-like transcript 2 after trogocytosis allows a functional cell-cell transfer of sensitivity. J Immunol. 2011;186(4):2210-2218.
32. Hudrisier D, Riond J, Garidou L, Duthoit C, Joly E. T cell activation correlates with an increased proportion of antigen among the materials acquired from target cells. Eur J Immunol. 2005;35(8):2284-2294.
33. Domaica CI, Fuertes MB, Rossi LE, et al. Tumour-experienced T cells promote NK cell activity through trogocytosis of NKG2D and NKp46 ligands. EMBO Rep. 2009;10(8):908-915.
34. Roda-Navarro P, Vales-Gomez M, Chisholm SE, Reyburn HT. Transfer of NKG2D and MICB at the cytotoxic NK cell immune synapse correlates with a reduction in NK cell cytotoxic function. Proc Natl Acad Sci U S A. 2006;103(30):11258-11263.
35. Caumartin J, Favier B, Daouya M, et al. Trogocytosis-based generation of suppressive NK cells. EMBO J. 2007;26(5):1423-1433.
36. LeMaoult J, Caumartin J, Carosella ED. Exchanges of membrane patches (trogocytosis) split theoretical and actual functions of immune cells. Hum Immunol. 2007;68(4):240-243.
37. LeMaoult J, Caumartin J, Daouya M, et al. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood. 2007;109(5):2040-2048.
38. Ford McIntyre MS, Young KJ, Gao J, Joe B, Zhang L. Cutting edge: in vivo trogocytosis as a mechanism of double negative regulatory T cell-mediated antigen-specific suppression. J Immunol. 2008;181(4):2271-2275.
39. Rosenits K, Keppler SJ, Vucikuja S, Aichele P. T cells acquire cell surface determinants of APC via in vivo trogocytosis during viral infections. Eur J Immunol. 2010;40(12):3450-3457.
40. Vanherberghen B, Andersson K, Carlin LM, et al. Human and murine inhibitory natural killer cell receptors transfer from natural killer cells to target cells. Proc Natl Acad Sci U S A. 2004;101(48): 16873-16878.
41. Alegre E, HoWangYin K-Y, Favier B, et al. Membrane redistributions through multi-intercellular exchanges and serial trogocytosis. Cell Res. 2010;20(11):1239-1251.
42. Caumartin J, Lemaoult J, Carosella ED. Intercellular exchanges of membrane patches (trogocytosis) highlight the next level of immune plasticity. Transpl Immunol. 2006;17(1):20-22.
43. Roda-Navarro P, Reyburn HT. Intercellular protein transfer at the NK cell immune synapse: mechanisms and physiological significance. FASEB J. 2007;21(8):1636-1646.
44. Suhoski MM, Golovina TN, Aqui NA, et al. Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. Mol Ther. 2007;15(5):981-988.
45. Zlotnik A. Chemokines and cancer. Int J Cancer. 2006;119(9):2026-2029.
46. Mailliard RB, Alber SM, Shen H, et al. IL-18- induced CD83+CCR7+ NK helper cells. J Exp Med. 2005;202(7):941-953.
47. Riol-Blanco L, Sanchez-Sanchez N, Torres A, et al. The chemokine receptor CCR7 activates in dendritic cells two signaling modules that independently regulate chemotaxis and migratory speed. J Immunol. 2005;174(7):4070-4080.
48. Stein JV, Soriano SF, M'Rini C, et al. CCR7- mediated physiological lymphocyte homing involves activation of a tyrosine kinase pathway. Blood. 2003;101(1):38-44.
49. Guimaraes F, Guven H, Donati D, et al. Evaluation of ex vivo expanded human NK cells on anti-leukemia activity in SCID-beige mice. Leukemia. 2006;20(5):833-839.
50. Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res. 2011;17(19):6287-6297.