Antigen Presenting Cell-Mediated Expansion of Human Umbilical Cord Blood Yields Log-Scale Expansion of Natural Killer Cells with Anti-Myeloma Activity

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Shah, Nina ^a   Martin Antonio, Beatriz ^a   Yang, Hong ^a   Ku, Stephanie ^b   Lee, Dean A ^a   Cooper, Laurence J N ^a   Decker, William K ^b,c   Li, Sufang ^a   Robinson, Simon N ^a   Sekine, Takuya ^a   Parmar, Simrit ^a   Gribben, John ^d   Wang, Michael ^a   Rezvani, Katy ^a   Yvon, Eric ^a   Najjar, Amer ^a   Burks, Jared ^a   Kaur, Indreshpal ^a   Champlin, Richard E ^a   Bollard, Catherine M ^b   Shpall, Elizabeth J ^a   more..

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

^b CENTER FOR CELL AND GENE THERAPY   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD56 ANTIGEN; CD94 ANTIGEN; EOMESODERMIN; INTERLEUKIN 2; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2C; TRANSCRIPTION FACTOR T BET; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL EXPANSION; CELL FUNCTION; CELL THERAPY; CONTROLLED STUDY; CRYOPRESERVATION; CYTOTOXICITY; FEEDER CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL SYNAPSE; IN VIVO STUDY; MOUSE; MULTIPLE MYELOMA; NATURAL KILLER CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; TUMOR XENOGRAFT; UMBILICAL CORD BLOOD;

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD3; ANTIGENS, CD56; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOTOXICITY, IMMUNOLOGIC; FETAL BLOOD; HUMANS; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; INTERLEUKIN-2; K562 CELLS; KILLER CELLS, NATURAL; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MICROSCOPY, CONFOCAL; MULTIPLE MYELOMA; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84885723035     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076781     Document Type: Article

References (52)

1. Raab MS, Podar K, Breitkreutz I, Richardson PG, Anderson KC, (2009) Multiple myeloma. Lancet 374: 324-339.
2. Harousseau JL, Moreau P, (2009) Autologous hematopoietic stem-cell transplantation for multiple myeloma. N Engl J Med 360: 2645-2654.
3. Alici E, Konstantinidis KV, Sutlu T, Aints A, Gahrton G, et al. (2007) Anti-myeloma activity of endogenous and adoptively transferred activated natural killer cells in experimental multiple myeloma model. Exp Hematol 35: 1839-1846.
4. Garg TK, Szmania SM, Khan JA, Hoering A, Malbrough PA, et al. (2012) Highly activated and expanded natural killer cells for multiple myeloma immunotherapy. Haematologica 97: 1348-1356.
5. Sawanobori M, Suzuki K, Nakagawa Y, Inoue Y, Utsuyama M, et al. (1997) Natural killer cell frequency and serum cytokine levels in monoclonal gammopathies: correlation of bone marrow granular lymphocytes to prognosis. Acta Haematol 98: 150-154.
6. Jurisic V, Srdic T, Konjevic G, Markovic O, Colovic M, (2007) Clinical stage-depending decrease of NK cell activity in multiple myeloma patients. Med Oncol 24: 312-317.
7. Passweg JR, Stern M, Koehl U, Uharek L, Tichelli A, (2005) Use of natural killer cells in hematopoetic stem cell transplantation. Bone Marrow Transplant 35: 637-643.
8. Ruggeri L, Capanni M, Mancusi A, Urbani E, Perruccio K, et al. (2004) Alloreactive natural killer cells in mismatched hematopoietic stem cell transplantation. Blood Cells Mol Dis 33: 216-221.
9. Hsu KC, Gooley T, Malkki M, Pinto-Agnello C, Dupont B, et al. (2006) KIR ligands and prediction of relapse after unrelated donor hematopoietic cell transplantation for hematologic malignancy. Biol Blood Marrow Transplant 12: 828-836.
10. Kroger N, Zabelina T, Berger J, Duske H, Klyuchnikov E, et al. (2011) Donor KIR haplotype B improves progression-free and overall survival after allogeneic hematopoietic stem cell transplantation for multiple myeloma. Leukemia 25: 1657-1661.
11. Willemze R, Ruggeri A, Purtill D, Rodrigues CA, Gluckman E, et al. (2010) Is there an impact of killer cell immunoglobulin-like receptors and KIR-ligand incompatibilities on outcomes after unrelated cord blood stem cell transplantation? Best Pract Res Clin Haematol 23: 283-290.
12. Brunstein CG, Wagner JE, Weisdorf DJ, Cooley S, Noreen H, et al. (2009) Negative effect of KIR alloreactivity in recipients of umbilical cord blood transplant depends on transplantation conditioning intensity. Blood 113: 5628-5634.
13. Miller JS, Cooley S, Parham P, Farag SS, Verneris MR, et al. (2007) Missing KIR ligands are associated with less relapse and increased graft-versus-host disease (GVHD) following unrelated donor allogeneic HCT. Blood 109: 5058-5061.
14. Kanga U, Mourya M, Seth T, George J, Sood P, et al. (2012) Role of killer immunoglobulin-like receptor-ligand interactions in human leukocyte antigen-matched sibling hematopoietic stem cell transplantation. Transplant Proc 44: 919-921.
15. Fauriat C, Mallet F, Olive D, Costello RT, (2006) Impaired activating receptor expression pattern in natural killer cells from patients with multiple myeloma. Leukemia 20: 732-733.
16. Ghiringhelli F, Menard C, Terme M, Flament C, Taieb J, et al. (2005) CD4+CD25+ regulatory T cells inhibit natural killer cell functions in a transforming growth factor-beta-dependent manner. J Exp Med 202: 1075-1085.
17. Tanner J, Tosato G, (1991) Impairment of natural killer functions by interleukin 6 increases lymphoblastoid cell tumorigenicity in athymic mice. J Clin Invest 88: 239-247.
18. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, et al. (1993) Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 178: 1041-1048.
19. Tinhofer I, Marschitz I, Henn T, Egle A, Greil R, (2000) Expression of functional interleukin-15 receptor and autocrine production of interleukin-15 as mechanisms of tumor propagation in multiple myeloma. Blood 95: 610-618.
20. Godfrey J, Benson DM Jr, (2012) The role of natural killer cells in immunity against multiple myeloma. Leuk Lymphoma 53: 1666-1676.
21. Alici E, Sutlu T, Bjorkstrand B, Gilljam M, Stellan B, et al. (2008) Autologous antitumor activity by NK cells expanded from myeloma patients using GMP-compliant components. Blood 111: 3155-3162.
22. Katodritou E, Terpos E, North J, Kottaridis P, Verrou E, et al. (2011) Tumor-primed natural killer cells from patients with multiple myeloma lyse autologous, NK-resistant, bone marrow-derived malignant plasma cells. Am J Hematol 86: 967-973.
23. Carbone E, Neri P, Mesuraca M, Fulciniti MT, Otsuki T, et al. (2005) HLA class I, NKG2D, and natural cytotoxicity receptors regulate multiple myeloma cell recognition by natural killer cells. Blood 105: 251-258.
24. Xing D RA, Gribben JG, Decker WK, Burks JK, Li S, et al. (2010) Cord Blood Natural Killer Cells Exhibit Defective Lytic Immunological Synapse Formation that is Reversed with IL-2 Ex Vivo Expansion. J Immunother 33(7): 684-96.
25. Lapteva N, Durett AG, Sun J, Rollins LA, Huye LL, et al. (2012) Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. Cytotherapy 14: 1131-1143.
26. Denman CJ, Senyukov VV, Somanchi SS, Phatarpekar PV, Kopp LM, et al. (2012) Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One 7: e30264.
27. Hoyos V, Savoldo B, Quintarelli C, Mahendravada A, Zhang M, et al. (2010) Engineering CD19-specific T lymphocytes with interleukin-15 and a suicide gene to enhance their anti-lymphoma/leukemia effects and safety. Leukemia 24: 1160-1170.
28. Savoldo B, Rooney CM, Di Stasi A, Abken H, Hombach A, et al. (2007) Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 110: 2620-2630.
29. Yang J, Cao Y, Hong S, Li H, Qian J, et al. (2009) Human-like mouse models for testing the efficacy and safety of anti-beta2-microglobulin monoclonal antibodies to treat myeloma. Clin Cancer Res 15: 951-959.
30. Feinman R, Koury J, Thames M, Barlogie B, Epstein J, et al. (1999) Role of NF-kappaB in the rescue of multiple myeloma cells from glucocorticoid-induced apoptosis by bcl-2. Blood 93: 3044-3052.
31. Ramsay AG, Johnson AJ, Lee AM, Gorgun G, Le Dieu R, et al. (2008) Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug. J Clin Invest 118: 2427-2437.
32. Gill S, Vasey AE, De Souza A, Baker J, Smith AT, et al. (2012) Rapid development of exhaustion and down-regulation of eomesodermin limit the antitumor activity of adoptively transferred murine natural killer cells. Blood 119: 5758-5768.
33. Intlekofer AM, Takemoto N, Wherry EJ, Longworth SA, Northrup JT, et al. (2005) Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat Immunol 6: 1236-1244.
34. Stinchcombe JC, Bossi G, Booth S, Griffiths GM, (2001) The immunological synapse of CTL contains a secretory domain and membrane bridges. Immunity 15: 751-761.
35. Orange JS, (2008) Formation and function of the lytic NK-cell immunological synapse. Nat Rev Immunol 8: 713-725.
36. Bjorkstrand B, Iacobelli S, Hegenbart U, Gruber A, Greinix H, et al. (2011) Tandem autologous/reduced-intensity conditioning allogeneic stem-cell transplantation versus autologous transplantation in myeloma: long-term follow-up. J Clin Oncol 29: 3016-3022.
37. Krishnan A, Pasquini MC, Logan B, Stadtmauer EA, Vesole DH, et al. (2011) Autologous haemopoietic stem-cell transplantation followed by allogeneic or autologous haemopoietic stem-cell transplantation in patients with multiple myeloma (BMT CTN 0102): a phase 3 biological assignment trial. Lancet Oncol 12: 1195-1203.
38. Rosinol L, Perez-Simon JA, Sureda A, de la Rubia J, de Arriba F, et al. (2008) A prospective PETHEMA study of tandem autologous transplantation versus autograft followed by reduced-intensity conditioning allogeneic transplantation in newly diagnosed multiple myeloma. Blood 112: 3591-3593.
39. Giaccone L, Storer B, Patriarca F, Rotta M, Sorasio R, et al. (2011) Long-term follow-up of a comparison of nonmyeloablative allografting with autografting for newly diagnosed myeloma. Blood 117: 6721-6727.
40. Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, et al. (2002) Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295: 2097-2100.
41. Lundqvist A, McCoy JP, Samsel L, Childs R, (2007) Reduction of GVHD and enhanced antitumor effects after adoptive infusion of alloreactive Ly49-mismatched NK cells from MHC-matched donors. Blood 109: 3603-3606.
42. Shi J, Tricot G, Szmania S, Rosen N, Garg TK, et al. (2008) Infusion of haplo-identical killer immunoglobulin-like receptor ligand mismatched NK cells for relapsed myeloma in the setting of autologous stem cell transplantation. Br J Haematol 143: 641-653.
43. Roda-Navarro P, Vales-Gomez M, Chisholm SE, Reyburn HT, (2006) 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 103: 11258-11263.
44. Paley MA, Gordon SM, Bikoff EK, Robertson EJ, Wherry EJ, et al. (2012) Technical Advance: Fluorescent reporter reveals insights into eomesodermin biology in cytotoxic lymphocytes. J Leukoc Biol.
45. Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, et al. (2004) T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20: 477-494.
46. Spanholtz J, Tordoir M, Eissens D, Preijers F, van der Meer A, et al. (2010) High log-scale expansion of functional human natural killer cells from umbilical cord blood CD34-positive cells for adoptive cancer immunotherapy. PLoS One 5: e9221.
47. Spanholtz J, Preijers F, Tordoir M, Trilsbeek C, Paardekooper J, et al. (2011) Clinical-grade generation of active NK cells from cord blood hematopoietic progenitor cells for immunotherapy using a closed-system culture process. PLoS One 6: e20740.
48. Beck RC, Padival M, Yeh D, Ralston J, Cooke KR, et al. (2009) The Notch ligands Jagged2, Delta1, and Delta4 induce differentiation and expansion of functional human NK cells from CD34+ cord blood hematopoietic progenitor cells. Biol Blood Marrow Transplant 15: 1026-1037.
49. Rocha V, Labopin M, Sanz G, Arcese W, Schwerdtfeger R, et al. (2004) Transplants of umbilical-cord blood or bone marrow from unrelated donors in adults with acute leukemia. N Engl J Med 351: 2276-2285.
50. Laughlin MJ, Eapen M, Rubinstein P, Wagner JE, Zhang MJ, et al. (2004) Outcomes after transplantation of cord blood or bone marrow from unrelated donors in adults with leukemia. N Engl J Med 351: 2265-2275.
51. Anasetti C, Aversa F, Brunstein CG, (2012) Back to the future: mismatched unrelated donor, haploidentical related donor, or unrelated umbilical cord blood transplantation? Biol Blood Marrow Transplant 18: S161-165.
52. Gluckman E, Ruggeri A, Volt F, Cunha R, Boudjedir K, et al. (2011) Milestones in umbilical cord blood transplantation. Br J Haematol 154: 441-447.