333
Views
2
CrossRef citations to date
0
Altmetric
Original Research

Development and Characterization of 3D Hybrid Spheroids for the Investigation of the Crosstalk Between B-Cell Non-Hodgkin Lymphomas and Mesenchymal Stromal Cells

ORCID Icon, & ORCID Icon
Pages 683-697 | Published online: 17 Jun 2022

References

  • Swerdlow SH, Campo E, Pileri SA, et al. The 2016 revision of the World Health Organization classification of lymphoid neoplasms. Blood. 2016;127(20):2375–2390. doi:10.1182/blood-2016-01-643569
  • Said JW. Aggressive B-cell lymphomas: how many categories do we need? Mod Pathol. 2013;26 Suppl 1(01):S42–S56. doi:10.1038/modpathol.2012.178
  • Campbell J, Seymour JF, Matthews J, et al. The prognostic impact of bone marrow involvement in patients with diffuse large cell lymphoma varies according to the degree of infiltration and presence of discordant marrow involvement. Eur J Haematol. 2006;76(6):473–480. doi:10.1111/j.1600-0609.2006.00644.x
  • Chung R, Lai R, Wei P, et al. Concordant but not discordant bone marrow involvement in diffuse large B-cell lymphoma predicts a poor clinical outcome independent of the International Prognostic Index. Blood. 2007;110(4):1278–1282. doi:10.1182/blood-2007-01-070300
  • Yao Z, Deng L, Xu-Monette ZY, et al. Concordant bone marrow involvement of diffuse large B-cell lymphoma represents a distinct clinical and biological entity in the era of immunotherapy. Leukemia. 2018;32(2):353–363. doi:10.1038/leu.2017.222
  • Crippa S, Santi L, Bosotti R, et al. Bone marrow-derived mesenchymal stromal cells: a novel target to optimize hematopoietic stem cell transplantation protocols in hematological malignancies and rare genetic disorders. J Clin Med. 2019;9(1):2. doi:10.3390/jcm9010002
  • Méndez-Ferrer S, Michurina TV, Ferraro F, et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature. 2012;466(7308):829–834. doi:10.1038/nature09262
  • Kidd S, Caldwell L, Dietrich M, et al. Mesenchymal stromal cells alone or expressing interferon-β suppress pancreatic tumors in vivo, an effect countered by anti-inflammatory treatment. Cytotherapy. 2011;13:498.
  • He N, Kong Y, Lei X, et al. MSCs inhibit tumor progression and enhance radiosensitivity of breast cancer cells by down-regulating Stat3 signaling pathway. Cell Death Dis. 2018;9(10):1026. doi:10.1038/s41419-018-0949-3
  • De Araújo Farias V, O’Valle F, Lerma BA, et al. Human mesenchymal stem cells enhance the systemic effects of radiotherapy. Oncotarget. 2015;6(31):31164–31180. doi:10.18632/oncotarget.5216
  • Otsu K, Das S, Houser SD, et al. Concentration-dependent inhibition of angiogenesis by mesenchymal stem cells. Blood. 2009;113(18):4197–4205. doi:10.1182/blood-2008-09-176198
  • Dasari VR, Velpula KK, Kaur K, et al. Cord blood stem cell-mediated induction of apoptosis in glioma downregulates X-linked inhibitor of apoptosis protein (XIAP). PLoS One. 2010;5(7):e11813. doi:10.1371/journal.pone.0011813
  • Suzuki K, Sun R, Origuchi M, et al. Mesenchymal stromal cells promote tumor growth through the enhancement of neovascularization. Mol Med. 2011;17(7–8):579–587. doi:10.2119/molmed.2010.00157
  • Karnoub AE, Dash AB, Vo AP, et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature. 2007;449(7162):557–563. doi:10.1038/nature06188
  • Bussard KM, Mutkus L, Stumpf K, et al. Tumor-associated stromal cells as key contributors to the tumor microenvironment. Breast Cancer Res. 2016;18(1):84. doi:10.1186/s13058-016-0740-2
  • Le Naour A, Prat M, Thibault B, et al. Tumor cells educate mesenchymal stromal cells to release chemoprotective and immunomodulatory factors. J Mol Cell Biol. 2020;12(3):202–215. doi:10.1093/jmcb/mjz090
  • Hussain S, Peng B, Cherian M, et al. The roles of stroma-derived chemokine in different stages of cancer metastases. Front Immunol. 2020;11:598532. doi:10.3389/fimmu.2020.598532
  • Hill BS, Sarnella A, D’Avino G, et al. Recruitment of stromal cells into tumour microenvironment promote the metastatic spread of breast cancer. Semin Cancer Biol. 2020;60:202–213. doi:10.1016/j.semcancer.2019.07.028
  • Kumar A, Bhattacharyya J, Jaganathan BG. Adhesion to stromal cells mediates imatinib resistance in chronic myeloid leukemia through ERK and BMP signaling pathways. Sci Rep. 2017;7(1):9535. doi:10.1038/s41598-017-10373-3
  • Mraz M, Zent CS, Church AK, et al. Bone marrow stromal cells protect lymphoma B-cells from rituximab-induced apoptosis and targeting integrin α-4-β-1 (VLA-4) with natalizumab can overcome this resistance. Br J Haematol. 2011;155(1):53–64. doi:10.1111/j.1365-2141.2011.08794.x
  • Janssens R, Struyf S, Proost P. The unique structural and functional features of CXCL12. Cell Mol Immunol. 2018;15(4):299–311. doi:10.1038/cmi.2017.107
  • Lwin T, Crespo LA, Wu A, et al. Lymphoma cell adhesion-induced expression of B cell-activating factor of the TNF family in bone marrow stromal cells protects non-Hodgkin’s B lymphoma cells from apoptosis. Leukemia. 2009;23(1):170–177. doi:10.1038/leu.2008.266
  • Breslin S, O’Driscoll L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov Today. 2013;18(5–6):240–249. doi:10.1016/j.drudis.2012.10.003
  • Edmondson R, Broglie JJ, Adcock AF, et al. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12(4):207–218. doi:10.1089/adt.2014.573
  • Zoetemelk M, Rausch M, Colin DJ, et al. Short-term 3D culture systems of various complexity for treatment optimization of colorectal carcinoma. Sci Rep. 2019;9:7103.
  • Powley IR, Patel M, Miles G, et al. Patient-derived explants (PDEs) as a powerful preclinical platform for anti-cancer drug and biomarker discovery. Br J Cancer. 2020;122(6):735–744. doi:10.1038/s41416-019-0672-6
  • Unger FT, Witte I, David KA. Prediction of individual response to anticancer therapy: historical and future perspectives. Cell Mol Life Sci. 2015;72(4):729–757. doi:10.1007/s00018-014-1772-3
  • Imamura Y, Mukohara T, Shimono Y, et al. Comparison of 2D- and 3D-culture models as drug-testing platforms in breast cancer. Oncol Rep. 2015;33(4):1837–1843. doi:10.3892/or.2015.3767
  • Tung YC, Hsiao AY, Allen SG, et al. High-throughput 3D spheroid culture and drug testing using a 384 hanging drop array. Analyst. 2011;136(3):473–478. doi:10.1039/C0AN00609B
  • Benelli R, Zocchi MR, Poggi A. Three-Dimensional (3D) culture models in cancer investigation, drug testing and immune response evaluation. Int J Mol Sci. 2020;22(1):150. doi:10.3390/ijms22010150
  • Brüningk SC, Rivens I, Box C, et al. 3D tumour spheroids for the prediction of the effects of radiation and hyperthermia treatments. Sci Rep. 2020;10(1):1653. doi:10.1038/s41598-020-58569-4
  • Luca AC, Mersch S, Deenen R, et al. Impact of the 3D microenvironment on phenotype, gene expression, and EGFR inhibition of colorectal cancer cell lines. PLoS One. 2013;8(3):e59689. doi:10.1371/journal.pone.0059689
  • Goers L, Freemont P, Polizzi KM. Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface. 2014;11(96):20140065. doi:10.1098/rsif.2014.0065
  • Vis MAM, Ito K, Hofmann S. Impact of culture medium on cellular interactions in in vitro co-culture systems. Front Bioeng Biotechnol. 2020;8:911. doi:10.3389/fbioe.2020.00911
  • Mannino RG, Santiago-Miranda AN, Pradhan P, et al. 3D microvascular model recapitulates the diffuse large B-cell lymphoma tumor microenvironment in vitro. Lab Chip. 2017;17(3):407–414. doi:10.1039/C6LC01204C
  • Foxall R, Narang P, Glaysher B, et al. Developing a 3D B cell lymphoma culture system to model antibody therapy. Front Immunol. 2021;11:605231. doi:10.3389/fimmu.2020.605231
  • An JH, Song WJ, Li Q, et al. 3D-culture models as drug-testing platforms in canine lymphoma and their cross talk with lymph node-derived stromal cells. J Vet Sci. 2021;22(3):e25. doi:10.4142/jvs.2021.22.e25
  • Białkowska K, Komorowski P, Bryszewska M, et al. Spheroids as a type of three-dimensional cell cultures-examples of methods of preparation and the most important application. Int J Mol Sci. 2020;21(17):6225. doi:10.3390/ijms21176225
  • LaBarbera DV, Reid BG, Yoo BH. The multicellular tumor spheroid model for high throughput cancer drug discovery. Expert Opin Drug Discov. 2012;7(9):819–830. doi:10.1517/17460441.2012.708334
  • Monjaret F, Fernandes M, Duchemin-Pelletier E, et al. Fully automated one-step production of functional 3D tumor spheroids for high-content screening. J Lab Autom. 2016;21(2):268–280. doi:10.1177/2211068215607058
  • Caliari SR, Burdick JA. A practical guide to hydrogels for cell culture. Nat Methods. 2016;13(5):405–414. doi:10.1038/nmeth.3839
  • Lee JM, Park DY, Yang L, et al. Generation of uniform-sized multicellular tumor spheroids using hydrogel microwells for advanced drug screening. Sci Rep. 2018;8(1):17145. doi:10.1038/s41598-018-35216-7
  • Lutolf MP, Hubbell JA. Synthetic biomaterials as instructive extracellular microenvironments for morphogenesis in tissue engineering. Nat Biotechnol. 2005;23(1):47–55. doi:10.1038/nbt1055
  • Tibbitt MW, Anseth KS. Hydrogels as extracellular matrix mimics for 3D cell culture. Biotechnol Bioeng. 2009;103(4):655–663. doi:10.1002/bit.22361
  • Determining fluorescence intensity and signal. University of Maryland, Baltimore County. Available from: https://kpif.umbc.edu/image-processing-resources/imagej-fiji/determining-fluorescence-intensity-and-positive-signal/. Accessed December 21, 2021.
  • Bio-Rad colorimetric and fluorometric calculator. Available from: https://www.bio-rad-antibodies.com/colorimetric-calculator-fluorometric-alamarblue.html. Accessed December 21, 2021.
  • Eilenberger C, Kratz SRA, Rothbauer M, et al. Optimized alamarBlue assay protocol for drug dose-response determination of 3D tumor spheroids. MethodsX. 2018;5:781–787. doi:10.1016/j.mex.2018.07.011
  • Meads MB, Hazlehurst LA, Dalton WS. The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin Cancer Res. 2008;14(9):2519–2526. doi:10.1158/1078-0432.CCR-07-2223
  • Lee MW, Ryu S, Kim DS, et al. Mesenchymal stem cells in suppression or progression of hematologic malignancy: current status and challenges. Leukemia. 2019;33(3):597–611. doi:10.1038/s41375-018-0373-9
  • Galland S, Stamenkovic I. Mesenchymal stromal cells in cancer: a review of their immunomodulatory functions and dual effects on tumor progression. J Pathol. 2020;250(5):555–572. doi:10.1002/path.5357
  • Liang W, Chen X, Zhang S, et al. Mesenchymal stem cells as a double-edged sword in tumor growth: focusing on MSC-derived cytokines. Cell Mol Biol Lett. 2021;26(1):3. doi:10.1186/s11658-020-00246-5
  • Wu YL, Li HY, Zhao XP, et al. Mesenchymal stem cell‐derived CCN2 promotes the proliferation, migration and invasion of human tongue squamous cell carcinoma cells. Cancer Sci. 2017;108(5):897–909. doi:10.1111/cas.13202
  • Yulyana Y, Ho IA, Sia KC, et al. Paracrine factors of human fetal MSCs inhibit liver cancer growth through reduced activation of IGF-1R/PI3K/Akt signaling. Mol Ther. 2015;23(4):746–756. doi:10.1038/mt.2015.13
  • Klopp AH, Gupta A, Spaeth E, et al. Concise review: dissecting a discrepancy in the literature: do mesenchymal stem cells support or suppress tumor growth? Stem Cells. 2011;29(1):11–19. doi:10.1002/stem.559
  • Li L, Tian H, Yue W, et al. Human mesenchymal stem cells play a dual role on tumor cell growth in vitro and in vivo. J Cell Physiol. 2011;226(7):1860–1867. doi:10.1002/jcp.22511
  • Wang Q, Li T, Wu W, et al. Interplay between mesenchymal stem cell and tumor and potential application. Hum Cell. 2020;33(3):444–458. doi:10.1007/s13577-020-00369-z
  • Duś-Szachniewicz K, Drobczyński S, Woźniak M, et al. Differentiation of single lymphoma primary cells and normal B-cells based on their adhesion to mesenchymal stromal cells in optical tweezers. Sci Rep. 2019;9(1):9885. doi:10.1038/s41598-019-46086-y
  • Duś-Szachniewicz K, Drobczyński S, Ziółkowski P, et al. Physiological Hypoxia (Physioxia) impairs the early adhesion of single lymphoma cell to marrow stromal cell and extracellular matrix. Optical Tweezers Study. Int J Mol Sci. 2018;19(7):1880. doi:10.3390/ijms19071880
  • Gava F, Faria C, Gravelle P, et al. 3D model characterization by 2D and 3D imaging in t(14;18)-positive B-NHL: perspectives for in vitro drug screens in follicular lymphoma. Cancers. 2021;13(7):1490. doi:10.3390/cancers13071490
  • Barbaglio F, Belloni D, Scarfò L, et al. Three-dimensional co-culture model of chronic lymphocytic leukemia bone marrow microenvironment predicts patient-specific response to mobilizing agents. Haematologica. 2021;106(9):2334–2344. doi:10.3324/haematol.2020.248112
  • Adamo A, Delfino P, Gatti A, et al. HS-5 and HS-27A stromal cell lines to study bone marrow mesenchymal stromal cell-mediated support to cancer development. Front Cell Dev Biol. 2020;8:584232. doi:10.3389/fcell.2020.584232
  • Belloni D, Heltai S, Ponzoni M, et al. Modeling multiple myeloma-bone marrow interactions and response to drugs in a 3D sur rogate microenvironment. Haematologica. 2018;103(4):707–716. doi:10.3324/haematol.2017.167486
  • Maritan SM, Lian EY, Mulligan LM. An efficient and flexible cell aggregation method for 3d spheroid production. J Vis Exp. 2017;121:55544.
  • McHowat J, Swift LM, Arutunyan A, et al. Clinical concentrations of doxorubicin inhibit activity of myocardial membrane-associated, calcium-independent phospholipase A(2). Cancer Res. 2001;61(10):4024–4029.
  • Xu P, Zuo H, Chen B, et al. Doxorubicin-loaded platelets as a smart drug delivery system: an improved therapy for lymphoma. Sci Rep. 2017;7(1):42632. Erratum in: Sci Rep. 2017;7:44974. doi:10.1038/srep42632
  • Ma J, Lu P, Guo A. Characterization of ibrutinib-sensitive and -resistant mantle lymphoma cells. Br J Haematol. 2014;166(6):849–861. doi:10.1111/bjh.12974
  • Wu W, Wang W, Franzen CA. at al. Inhibition of B-cell receptor signaling disrupts cell adhesion in mantle cell lymphoma via RAC2. Blood Adv. 2021;5(1):185–197. doi:10.1182/bloodadvances.2020001665
  • Mai Y, Yu JJ, Bartholdy B, et al. An oxidative stress-based mechanism of doxorubicin cytotoxicity suggests new therapeutic strategies in ABC-DLBCL. Blood. 2016;128(24):2797–2807. doi:10.1182/blood-2016-03-705814
  • Lamaison C, Latour S, Hélaine N, et al. A novel 3D culture model recapitulates primary FL B-cell features and promotes their survival. Blood Adv. 2021;5(23):5372–5386. doi:10.1182/bloodadvances.2020003949
  • Hou K, Yu Z, Jia Y, et al. Efficacy and safety of ibrutinib in diffuse large B-cell lymphoma: a single-arm meta-analysis. Crit Rev Oncol Hematol. 2020;152:103010. doi:10.1016/j.critrevonc.2020.103010
  • Bray LJ, Binner M, Körner Y, et al. A three-dimensional ex vivo tri-culture model mimics cell-cell interactions between acute myeloid leukemia and the vascular niche. Haematologica. 2017;102:1215–1226. doi:10.3324/haematol.2016.157883
  • Khawar IA, Park JK, Jung ES, et al. Three dimensional mixed-cell spheroids mimic stroma-mediated chemoresistance and invasive migration in hepatocellular carcinoma. Neoplasia. 2018;20(8):800–812. doi:10.1016/j.neo.2018.05.008
  • Yip D, Cho CH. A multicellular 3D heterospheroid model of liver tumor and stromal cells in collagen gel for anti-cancer drug testing. Biochem Biophys Res Commun. 2013;433(3):327–332. doi:10.1016/j.bbrc.2013.03.008