Comparison of cytotoxic potency between freshly cultured and freshly thawed cytokine-induced killer cells from human umbilical cord blood.

Cytokine induced killer cells Immunotherapy UCB-CIK Umbilical cord blood Umbilical cord blood derived cytokine induced killer cells

Journal

Cell and tissue banking
ISSN: 1573-6814
Titre abrégé: Cell Tissue Bank
Pays: Netherlands
ID NLM: 100965121

Informations de publication

Date de publication:
Mar 2023
Historique:
received: 31 07 2021
accepted: 19 06 2022
pubmed: 7 7 2022
medline: 15 3 2023
entrez: 6 7 2022
Statut: ppublish

Résumé

Immune cell therapy has been incorporated into cancer therapy over the past few years. Chimeric antigen receptor T cells (Car-T cells) transplantation is a novel and promising therapy for cancer treatment and introduces a new age of immune cell therapy. However, the expensive nature of genetic modification procedures limits the accessibility of Car-T cells for cancer treatment. Cytokine-induced killer cells (CIKs) can kill the target cells in an MHC-non-restricted manner; these cells can be developed to "off-the-shelf" immune cell products for cancer treatment. However, the anti-tumor potency of freshly thawed CIKs is not well documented. This study aimed to fill this gap, evaluating the anti-tumor potency of freshly thawed CIKs compared to that of freshly cultured CIKs. CIKs were produced from the human umbilical cord blood in accordance with published protocols. CIKs were cryopreserved in xeno-free cryomedium that contains 5% DMSO, 10% human serum in phosphate buffer saline at - 86 °C. These cells were thawed and immediately utilized in assays (called freshly thawed CIKs) with freshly cultured cells are control. The expression of the surface markers of CIKs, cytokine production, and in vitro anti-tumor cytotoxic cells of freshly thawed CIKs were evaluated and compared to freshly cultured CIKs. Additionally, the freshly thawed CIKs were injected into the breast of tumor-bearing mice to assess the anti-tumor potency in vivo. The results obtained in freshly thawed CIKs and freshly cultured CIKs demonstrated that the expression of CD3, and CD56 were comparable in both cases. The production of TNF-α, IFN-γ, and IL-10 was slightly reduced in freshly thawed cells compared to the freshly cultured cells. The in vitro lysis toward MCF-7 cancer cells was similar between freshly thawed and freshly cultured CIKs. Moreover, the freshly thawed CIKs displayed anti-breast tumor activity in the breast tumor-bearing mice. The volume of tumors significantly reduced in the mice grafted with freshly thawed CIKs while, conversely, the tumor volume in mice of the placebo group gradually increased. This study substantiated that freshly thawed CIKs preserved their anti-tumor potency in both in vitro and in vivo conditions. The results initially revealed the great potential of UCB-CIKs for "off-the-shelf" CIK product manufacturing. However, further studies on the effects of cryomedia, freezing rate, and thawing procedure should be undertaken before freshly thawed off-the-shelf UCB-CIKs are utilized in clinical trials.

Identifiants

pubmed: 35792988
doi: 10.1007/s10561-022-10022-8
pii: 10.1007/s10561-022-10022-8
doi:

Types de publication

Comparative Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

139-152

Subventions

Organisme : viet nam national university ho chi minh city
ID : C2020-18-26

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature B.V.

Références

Alsherbiny MA, Bhuyan DJ, Radwan I, Chang D, Li CG (2021) Metabolomic identification of anticancer metabolites of australian propolis and proteomic elucidation of its synergistic mechanisms with doxorubicin in the MCF7 cells. Int J Mol Sci 22:7840
pubmed: 34360606 pmcid: 8346082 doi: 10.3390/ijms22157840
Arunachalam PS, Wimmers F, Mok CKP, Perera R, Scott M, Hagan T, Sigal N, Feng Y, Bristow L, Tak-Yin Tsang O, Wagh D, Coller J, Pellegrini KL, Kazmin D, Alaaeddine G, Leung WS, Chan JMC, Chik TSH, Choi CYC, Huerta C, Paine McCullough M, Lv H, Anderson E, Edupuganti S, Upadhyay AA, Bosinger SE, Maecker HT, Khatri P, Rouphael N, Peiris M, Pulendran B (2020) Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans. Science (new York, NY) 369:1210–1220
doi: 10.1126/science.abc6261
Bastard P, Rosen LB, Zhang Q, Michailidis E, Hoffmann HH, Zhang Y, Dorgham K, Philippot Q, Rosain J, Béziat V, Manry J, Shaw E, Haljasmägi L, Peterson P, Lorenzo L, Bizien L, Trouillet-Assant S, Dobbs K, de Jesus AA, Belot A, Kallaste A, Catherinot E, Tandjaoui-Lambiotte Y, Le Pen J, Kerner G, Bigio B, Seeleuthner Y, Yang R, Bolze A, Spaan AN, Delmonte OM, Abers MS, Aiuti A, Casari G, Lampasona V, Piemonti L, Ciceri F, Bilguvar K, Lifton RP, Vasse M, Smadja DM, Migaud M, Hadjadj J, Terrier B, Duffy D, Quintana-Murci L, van de Beek D, Roussel L, Vinh DC, Tangye SG, Haerynck F, Dalmau D, Martinez-Picado J, Brodin P, Nussenzweig MC, Boisson-Dupuis S, Rodríguez-Gallego C, Vogt G, Mogensen TH, Oler AJ, Gu J, Burbelo PD, Cohen JI, Biondi A, Bettini LR, D'Angio M, Bonfanti P, Rossignol P, Mayaux J, Rieux-Laucat F, Husebye ES, Fusco F, Ursini MV, Imberti L, Sottini A, Paghera S, Quiros-Roldan E, Rossi C, Castagnoli R, Montagna D, Licari A, Marseglia GL, Duval X, Ghosn J, Tsang JS, Goldbach-Mansky R, Kisand K, Lionakis MS, Puel A, Zhang SY, Holland SM, Gorochov G, Jouanguy E, Rice CM, Cobat A, Notarangelo LD, Abel L, Su HC, Casanova JL (2020) Autoantibodies against type I IFNs in patients with life-threatening COVID-19. Science (New York, NY) 370(6515): eabd4585
Cany J, van der Waart AB, Tordoir M, Franssen GM, Hangalapura BN, de Vries J, Boerman O, Schaap N, van der Voort R, Spanholtz J, Dolstra H (2013) Natural killer cells generated from cord blood hematopoietic progenitor cells efficiently target bone marrow-residing human leukemia cells in NOD/SCID/IL2Rg(null) mice. PLoS ONE 8:e64384
pubmed: 23755121 pmcid: 3673996 doi: 10.1371/journal.pone.0064384
Capellero S, Erriquez J, Melano C, Mesiano G, Genta S, Pisacane A, Mittica G, Ghisoni E, Olivero M, Di Renzo MF, Aglietta M, Sangiolo D, Valabrega G (2020) Preclinical immunotherapy with cytokine-induced killer lymphocytes against epithelial ovarian cancer. Sci Rep 10:6478
pubmed: 32296104 pmcid: 7160190 doi: 10.1038/s41598-020-63634-z
Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH (2000) Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1:119–126
pubmed: 11248803 doi: 10.1038/77793
Edinger M, Cao YA, Verneris MR, Bachmann MH, Contag CH, Negrin RS (2003) Revealing lymphoma growth and the efficacy of immune cell therapies using in vivo bioluminescence imaging. Blood 101:640–648
pubmed: 12393519 doi: 10.1182/blood-2002-06-1751
Franceschetti M, Pievani A, Borleri G, Vago L, Fleischhauer K, Golay J, Introna M (2009) Cytokine-induced killer cells are terminally differentiated activated CD8 cytotoxic T-EMRA lymphocytes. Exp Hematol 37:616-628.e612
pubmed: 19375652 doi: 10.1016/j.exphem.2009.01.010
Garofano F, Gonzalez-Carmona MA, Skowasch D, Schmidt-Wolf R, Abramian A, Hauser S, Strassburg CP, Schmidt-Wolf IGH (2019) Clinical trials with combination of cytokine-induced killer cells and dendritic cells for cancer therapy. Int J Mol Sci 20:4307
pubmed: 31484350 pmcid: 6747410 doi: 10.3390/ijms20174307
Golay J, Martinelli S, Alzani R, Cribioli S, Albanese C, Gotti E, Pasini B, Mazzanti B, Saccardi R, Rambaldi A, Introna M (2018) Cord blood-derived cytokine-induced killer cells combined with blinatumomab as a therapeutic strategy for CD19(+) tumors. Cytotherapy 20:1077–1088
pubmed: 30093325 doi: 10.1016/j.jcyt.2018.06.003
Hanley PJ (2019) Fresh versus Frozen: Effects of Cryopreservation on CAR T Cells. Mol Ther J Am Soc Gene Ther 27:1213–1214
doi: 10.1016/j.ymthe.2019.06.001
Introna M (2017) CIK as therapeutic agents against tumors. J Autoimmun 85:32–44
pubmed: 28679475 doi: 10.1016/j.jaut.2017.06.008
Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH (2002) The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17:19–29
pubmed: 12150888 doi: 10.1016/S1074-7613(02)00333-3
Jiang J, Wu C, Lu B (2013) Cytokine-induced killer cells promote antitumor immunity. J Transl Med 11:83
pubmed: 23536996 pmcid: 3617047 doi: 10.1186/1479-5876-11-83
Khan JF, Khan AS, Brentjens RJ (2019) Application of CAR T cells for the treatment of solid tumors. Prog Mol Biol Transl Sci 164:293–327
pubmed: 31383408 doi: 10.1016/bs.pmbts.2019.07.004
Lapteva N, Durett AG, Sun J, Rollins LA, Huye LL, Fang J, Dandekar V, Mei Z, Jackson K, Vera J, Ando J, Ngo MC, Coustan-Smith E, Campana D, Szmania S, Garg T, Moreno-Bost A, Vanrhee F, Gee AP, Rooney CM (2012) Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. Cytotherapy 14:1131–1143
pubmed: 22900959 pmcid: 4787300 doi: 10.3109/14653249.2012.700767
Li Y, Schmidt-Wolf IG, Wu YF, Huang SL, Wei J, Fang J, Huang K, Zhou DH (2010) Optimized protocols for generation of cord blood-derived cytokine-induced killer/natural killer cells. Anticancer Res 30:3493–3499
pubmed: 20944128
Lin SJ, Kuo ML (2011) Cytotoxic function of umbilical cord blood natural killer cells: relevance to adoptive immunotherapy. Pediatr Hematol Oncol 28:640–646
pubmed: 21970456 doi: 10.3109/08880018.2011.613092
Lv Y, Wang Y (2021) Chemical constituents from Oldenlandia diffusa and their cytotoxic effects on human cancer cell lines. Nat Prod Res. https://doi.org/10.1080/14786419.2021.1974434
doi: 10.1080/14786419.2021.1974434 pubmed: 34963387
Marofi F, Motavalli R, Safonov VA, Thangavelu L, Yumashev AV, Alexander M, Shomali N, Chartrand MS, Pathak Y, Jarahian M, Izadi S, Hassanzadeh A, Shirafkan N, Tahmasebi S, Khiavi FM (2021) CAR T cells in solid tumors: challenges and opportunities. Stem Cell Res Ther 12:81
pubmed: 33494834 pmcid: 7831265 doi: 10.1186/s13287-020-02128-1
Miller JS, Rooney CM, Curtsinger J, McElmurry R, McCullar V, Verneris MR, Lapteva N, McKenna D, Wagner JE, Blazar BR, Tolar J (2014) Expansion and homing of adoptively transferred human natural killer cells in immunodeficient mice varies with product preparation and in vivo cytokine administration: implications for clinical therapy. Biol Blood Marrow Transplant J Am Soc Blood Marrow Transplant 20:1252–1257
doi: 10.1016/j.bbmt.2014.05.004
Mirabdollahi M, Haghjooyjavanmard S, Sadeghi-aliabadi H (2019) An anticancer effect of umbilical cord-derived mesenchymal stem cell secretome on the breast cancer cell line. Cell Tissue Bank 20:423–434
pubmed: 31338647 doi: 10.1007/s10561-019-09781-8
Mu Y, Wang WH, Xie JP, Zhang YX, Yang YP, Zhou CH (2016) Efficacy and safety of cord blood-derived dendritic cells plus cytokine-induced killer cells combined with chemotherapy in the treatment of patients with advanced gastric cancer: a randomized phase II study. Onco Targets Ther 9:4617–4627
pubmed: 27524915 pmcid: 4966574 doi: 10.2147/OTT.S107745
Mu YX, Zhao YX, Li BY, Bao HJ, Jiang H, Qi XL, Bai LY, Wang YH, Ma ZJ, Wu XY (2019) A simple method for in vitro preparation of natural killer cells from cord blood. BMC Biotechnol 19:80
pubmed: 31752805 pmcid: 6869212 doi: 10.1186/s12896-019-0564-0
Nishimura R, Baker J, Beilhack A, Zeiser R, Olson JA, Sega EI, Karimi M, Negrin RS (2008) In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood 112:2563–2574
pubmed: 18565854 pmcid: 2532819 doi: 10.1182/blood-2007-06-092817
Niu Q, Wang W, Li Y, Qin S, Wang Y, Wan G, Guan J, Zhu W (2011) Cord blood-derived cytokine-induced killer cells biotherapy combined with second-line chemotherapy in the treatment of advanced solid malignancies. Int Immunopharmacol 11:449–456
pubmed: 21215350 doi: 10.1016/j.intimp.2010.12.014
Panch SR, Srivastava SK, Elavia N, McManus A, Liu S, Jin P, Highfill SL, Li X, Dagur P, Kochenderfer JN, Fry TJ, Mackall CL, Lee D, Shah NN, Stroncek DF (2019) Effect of cryopreservation on autologous chimeric antigen receptor T cell characteristics. Mol Ther J Am Soc Gene Ther 27:1275–1285
doi: 10.1016/j.ymthe.2019.05.015
Pievani A, Borleri G, Pende D, Moretta L, Rambaldi A, Golay J, Introna M (2011) Dual-functional capability of CD3+CD56+ CIK cells, a T-cell subset that acquires NK function and retains TCR-mediated specific cytotoxicity. Blood 118:3301–3310
pubmed: 21821703 doi: 10.1182/blood-2011-02-336321
Rettinger E, Kuçi S, Naumann I, Becker P, Kreyenberg H, Anzaghe M, Willasch A, Koehl U, Bug G, Ruthardt M, Klingebiel T, Fulda S, Bader P (2012) The cytotoxic potential of interleukin-15-stimulated cytokine-induced killer cells against leukemia cells. Cytotherapy 14:91–103
pubmed: 21973023 doi: 10.3109/14653249.2011.613931
Sangiolo D, Martinuzzi E, Todorovic M, Vitaggio K, Vallario A, Jordaney N, Carnevale-Schianca F, Capaldi A, Geuna M, Casorzo L, Nash RA, Aglietta M, Cignetti A (2008) Alloreactivity and anti-tumor activity segregate within two distinct subsets of cytokine-induced killer (CIK) cells: implications for their infusion across major HLA barriers. Int Immunol 20:841–848
pubmed: 18469328 doi: 10.1093/intimm/dxn042
Sarvaria A, Jawdat D, Madrigal JA, Saudemont A (2017) Umbilical cord blood natural killer cells, their characteristics, and potential clinical applications. Front Immunol 8:329–329
pubmed: 28386260 pmcid: 5362597 doi: 10.3389/fimmu.2017.00329
Schmidt-Wolf IG, Negrin RS, Kiem HP, Blume KG, Weissman IL (1991) Use of a SCID mouse/human lymphoma model to evaluate cytokine-induced killer cells with potent antitumor cell activity. J Exp Med 174:139–149
pubmed: 1711560 doi: 10.1084/jem.174.1.139
Smagur A, Mitrus I, Ciomber A, Panczyniak K, Fidyk W, Sadus-Wojciechowska M, Holowiecki J, Giebel S (2015) Comparison of the cryoprotective solutions based on human albumin vs. autologous plasma: its effect on cell recovery, clonogenic potential of peripheral blood hematopoietic progenitor cells and engraftment after autologous transplantation. Vox Sang 108:417–424
pubmed: 25753814 doi: 10.1111/vox.12238
Sterner RC, Sterner RM (2021) CAR-T cell therapy: current limitations and potential strategies. Blood Cancer J 11:69
pubmed: 33824268 pmcid: 8024391 doi: 10.1038/s41408-021-00459-7
Trong HN, Le Van MH, Dang VT, Nguyen NH-T, Thanh BV, Van Pham P (2020) Current strategies for adoptive immunotherapy for cancer: “Off-the-shelf” immune cells. Biomed Res Ther 7:4170–4189
doi: 10.15419/bmrat.v7i12.655
Valgardsdottir R, Capitanio C, Texido G, Pende D, Cantoni C, Pesenti E, Rambaldi A, Golay J, Introna M (2014) Direct involvement of CD56 in cytokine-induced killer-mediated lysis of CD56+ hematopoietic target cells. Exp Hematol 42:1013-1021.e1011
pubmed: 25201755 doi: 10.1016/j.exphem.2014.08.005
Van Pham P, Vu BT, Pham VQ, Le PM, Le HT, Phan NK (2015) Production of dendritic cells and cytokine-induced killer cells from banked umbilical cord blood samples. Biomed Res Ther 2:1–7
Verneris MR, Miller JS (2009) The phenotypic and functional characteristics of umbilical cord blood and peripheral blood natural killer cells. Br J Haematol 147:185–191
pubmed: 19796267 pmcid: 2770803 doi: 10.1111/j.1365-2141.2009.07768.x
Vu BT, Duong QT-N, Le PM, Van Pham P (2016) Culture and differentiation of cytokine-induced killer cells from umbilical cord blood-derived mononuclear cells. Biomed Res Ther 3:1–9
doi: 10.7603/s40730-016-0002-z
Wang R, Jaw JJ, Stutzman NC, Zou Z, Sun PD (2012) Natural killer cell-produced IFN-γ and TNF-α induce target cell cytolysis through up-regulation of ICAM-1. J Leukoc Biol 91:299–309
pubmed: 22045868 pmcid: 3290424 doi: 10.1189/jlb.0611308
Wang L, Huang S, Dang Y, Li M, Bai W, Zhong Z, Zhao H, Li Y, Liu Y, Wu M (2014) Cord blood-derived cytokine-induced killer cellular therapy plus radiation therapy for esophageal cancer: a case report. Medicine 93:e340
pubmed: 25526496 pmcid: 4603076 doi: 10.1097/MD.0000000000000340
Xu X, Huang S, Xiao X, Sun Q, Liang X, Chen S, Zhao Z, Huo Z, Tu S, Li Y (2020) Challenges and clinical strategies of CAR T-cell therapy for acute lymphoblastic leukemia: overview and developments. Front Immunol 11:569117
pubmed: 33643279 doi: 10.3389/fimmu.2020.569117
Zeisberger SM, Schulz JC, Mairhofer M, Ponsaerts P, Wouters G, Doerr D, Katsen-Globa A, Ehrbar M, Hescheler J, Hoerstrup SP, Zisch AH, Kolbus A, Zimmermann H (2011) Biological and physicochemical characterization of a serum- and xeno-free chemically defined cryopreservation procedure for adult human progenitor cells. Cell Transplant 20:1241–1257
pubmed: 21176408 doi: 10.3727/096368910X547426
Zhang Z, Wang L, Luo Z, Zhao X, Huang J, Li H, Yang S, Zhao X, Zhang L, Li L, Wang F, Huang L, Zhang Y (2015a) Efficacy and safety of cord blood-derived cytokine-induced killer cells in treatment of patients with malignancies. Cytotherapy 17:1130–1138
pubmed: 25963952 doi: 10.1016/j.jcyt.2015.04.002
Zhang Z, Zhao X, Zhang T, Wang L, Yang L, Huang L, Li F, Liu J, Yue D, Wang F, Li J, Guan F, Xu Y, Zhang B, Zhang Y (2015b) Phenotypic characterization and anti-tumor effects of cytokine-induced killer cells derived from cord blood. Cytotherapy 17:86–97
pubmed: 25457278 doi: 10.1016/j.jcyt.2014.09.006

Auteurs

Hieu Trong Ngo (HT)

Stem Cell Institute, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam.
Vietnam National University Ho Chi Minh City, Ho Chi Minh City, Viet Nam.

Vy Thanh Dang (VT)

Stem Cell Institute, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam.
Vietnam National University Ho Chi Minh City, Ho Chi Minh City, Viet Nam.

Nguyen Ho-Thao Nguyen (NH)

Stem Cell Institute, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam.
Vietnam National University Ho Chi Minh City, Ho Chi Minh City, Viet Nam.

Anh Nguyen-Tu Bui (AN)

Stem Cell Institute, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam.
Vietnam National University Ho Chi Minh City, Ho Chi Minh City, Viet Nam.

Phuc Van Pham (P)

Stem Cell Institute, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam. phucpham@sci.edu.vn.
Vietnam National University Ho Chi Minh City, Ho Chi Minh City, Viet Nam. phucpham@sci.edu.vn.
Laboratory of Stem Cell Research and Application, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam. phucpham@sci.edu.vn.
Laboratory of Cancer Research, University of Science Ho Chi Minh City, Ho Chi Minh City, Viet Nam. phucpham@sci.edu.vn.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH