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Annual Review of Cancer Biology

Volume 7, 2023

Engineering the Immune Microenvironment into Organoid Models

Abstract

Organoid models have revolutionized cancer research through their ability to capture the cellular heterogeneity and spatial organization of a tumor in 3D culture. Patient-derived organoids can also mirror responses to therapy in vitro, opening the doors to personalized medicine that can direct clinical decision-making. As cancer immunotherapy has flourished and efforts to develop novel immunotherapies have increased, models that incorporate immune cells into organoid coculture to recapitulate the complexity of the tumor microenvironment faithfully are in high demand. To this end, a wide variety of organoid immune coculture methods have been developed, each differing in the source of immune cells used, types of immune cells maintained in culture, and their specific utility. This review aims to organize these methods into a framework that will aid researchers in choosing the appropriate system for their experimental needs. We also highlight several nonimmune cell types that have been successfully incorporated into organoid culture and the biology these coculture models are poised to interrogate.

Keyword(s): coculture organoids, coculture system, immune cells, patient-derived organoids, tumor immune microenvironment, tumor organoids
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/content/journals/10.1146/annurev-cancerbio-061421-040659
2023-04-11
2024-04-19
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Literature Cited

  1. Aisenbrey EA, Murphy WL. 2020. Synthetic alternatives to Matrigel. Nat. Rev. Mater. 5:539–51
     [Google Scholar]
  2. Aref AR, Campisi M, Ivanova E, Portell A, Larios D et al. 2018. 3D microfluidic ex vivo culture of organotypic tumor spheroids to model immune checkpoint blockade. Lab Chip 18:203129–43
     [Google Scholar]
  3. Azar J, Bahmad HF, Daher D, Moubarak MM, Hadadeh O et al. 2021. The use of stem cell-derived organoids in disease modeling: an update. Int. J. Mol. Sci. 14:7667
     [Google Scholar]
  4. Bar-Ephraim YE, Kretzschmar K, Clevers H. 2020. Organoids in immunological research. Nat. Rev. Immunol.5279–93
     [Google Scholar]
  5. Beaurivage C, Kanapeckaite A, Loomans C, Erdmann KS, Stallen J, Janssen RA. 2020. Development of a human primary gut-on-a-chip to model inflammatory processes. Sci. Rep. 10:21475
     [Google Scholar]
  6. Bein A, Shin W, Jalili-Firoozinezhad S, Park MH, Sontheimer-Phelps A et al. 2018. Microfluidic organ-on-a-chip models of human intestine. Cell. Mol. Gastroenterol. Hepatol. 5:4659–68
     [Google Scholar]
  7. Below CR, Kelly J, Brown A, Humphries JD, Hutton C, Xu J et al. 2022. A microenvironment-inspired synthetic three-dimensional model for pancreatic ductal adenocarcinoma organoids. Nat. Mater. 21:110–19
     [Google Scholar]
  8. Chakrabarti J, Holokai L, Syu L, Steele N, Chang J et al. 2018. Mouse-derived gastric organoid and immune cell co-culture for the study of the tumor microenvironment. In Epithelial Cell Culture M Baratta 157–68. New York: Humana
     [Google Scholar]
  9. Chalabi M, Fanchi LF, Dijkstra KK, Van den Berg JG, Aalbers AG et al. 2020. Neoadjuvant immunotherapy leads to pathological responses in MMR-proficient and MMR-deficient early-stage colon cancers. Nat. Med. 26:4566–76
     [Google Scholar]
  10. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L. 2009. Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27:3275–80
     [Google Scholar]
  11. Chan IS, Ewald AJ 2022. Organoid co-culture methods to capture cancer cell–natural killer cell interactions. Natural Killer (NK) Cells N Shimasaki 235–50. New York: Humana
     [Google Scholar]
  12. Cherne MD, Sidar B, Sebrell TA, Sanchez HS, Heaton K et al. 2021. A synthetic hydrogel, VitroGel® ORGANOID-3, improves immune cell-epithelial interactions in a tissue chip co-culture model of human gastric organoids and dendritic cells. Front. Pharmacol. 12:707891
     [Google Scholar]
  13. Courau T, Bonnereau J, Chicoteau J, Bottois H, Remark R et al. 2019. Cocultures of human colorectal tumor spheroids with immune cells reveal the therapeutic potential of MICA/B and NKG2A targeting for cancer treatment. J. Immunother. Cancer 7:74
     [Google Scholar]
  14. Cremonesi E, Governa V, Garzon JF, Mele V, Amicarella F et al. 2018. Gut microbiota modulate T cell trafficking into human colorectal cancer. Gut 67:111984–94
     [Google Scholar]
  15. Dao V, Yuki K, Lo YH, Nakano M, Kuo CJ et al. 2022. Immune organoids: from tumor modeling to precision oncology. Trends Cancer 8:10870–80
     [Google Scholar]
  16. Dekkers JF, Alieva M, Cleven A, Keramati F, Wezenaar AK et al. 2023. Uncovering the mode of action of engineered T cells in patient cancer organoids. Nat. Biotechnol. 41:60–69
     [Google Scholar]
  17. del Río EP, Santos F, Rodriguez XR, Martínez-Miguel M, Roca-Pinilla R et al. 2020. CCL21-loaded 3D hydrogels for T cell expansion and differentiation. Biomaterials 259:120313
     [Google Scholar]
  18. Deng J, Wang ES, Jenkins RW, Li S, Dries R et al. 2018. CDK4/6 inhibition augments antitumor immunity by enhancing T-cell activation. Cancer Discov 8:2216–33
     [Google Scholar]
  19. Dijkstra KK, Cattaneo CM, Weeber F, Chalabi M, van de Haar J et al. 2018. Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell 174:61586–98
     [Google Scholar]
  20. Ding S, Hsu C, Wang Z, Natesh NR, Millen R et al. 2022. Patient-derived micro-organospheres enable clinical precision oncology. Cell Stem Cell 29:6905–17
     [Google Scholar]
  21. du Bois H, Heim TA, Lund AW. 2021. Tumor-draining lymph nodes: at the crossroads of metastasis and immunity. Sci. Immunol. 6:63eabg3551
     [Google Scholar]
  22. Eicher AK, Kechele DO, Sundaram N, Berns HM, Poling HM et al. 2022. Functional human gastrointestinal organoids can be engineered from three primary germ layers derived separately from pluripotent stem cells. Cell Stem Cell 29:36–51
     [Google Scholar]
  23. Feig C, Gopinathan A, Neesse A, Chan DS, Cook N, Tuveson DA 2012. The pancreas cancer microenvironment. Clin. Cancer Res. 18:164266–76
     [Google Scholar]
  24. Fernando K, Kwang LG, Lim JT, Fong EL. 2021. Hydrogels to engineer tumor microenvironments in vitro. Biomater. Sci. 9:72362–83
     [Google Scholar]
  25. Fofanova TY, Stewart CJ, Auchtung JM, Wilson RL, Britton RA et al. 2019. A novel human enteroid-anaerobe co-culture system to study microbial-host interaction under physiological hypoxia. bioRxiv 555755. https://doi.org/10.1101/555755
  26. Ganesh K, Wu C, O'Rourke KP, Szeglin BC, Zheng Y et al. 2019. A rectal cancer organoid platform to study individual responses to chemoradiation. Nat. Med. 25:101607–14
     [Google Scholar]
  27. Garner H, de Visser KE. 2020. Immune crosstalk in cancer progression and metastatic spread: a complex conversation. Nat. Rev. Immunol. 20:8483–97
     [Google Scholar]
  28. Genshaft AS, Ziegler CG, Tzouanas CN, Mead BE, Jaeger AM et al. 2021. Live cell tagging tracking and isolation for spatial transcriptomics using photoactivatable cell dyes. Nat. Commun. 12:4995
     [Google Scholar]
  29. Harney AS, Arwert EN, Entenberg D, Wang Y, Guo P et al. 2015. Real-time imaging reveals local, transient vascular permeability, and tumor cell intravasation stimulated by TIE2hi macrophage–derived VEGFA. Cancer Discov 5:9932–43
     [Google Scholar]
  30. Holloway EM, Wu JH, Czerwinski M, Sweet CW, Wu A et al. 2020. Differentiation of human intestinal organoids with endogenous vascular endothelial cells. Dev. Cell 54:4516–28
     [Google Scholar]
  31. Holokai L, Chakrabarti J, Broda T, Chang J, Hawkins JA et al. 2019. Increased programmed death-ligand 1 is an early epithelial cell response to Helicobacter pylori infection. PLOS Pathog 15:e1007468
     [Google Scholar]
  32. Holokai L, Chakrabarti J, Lundy J, Croagh D, Adhikary P et al. 2020. Murine- and human-derived autologous organoid/immune cell co-cultures as pre-clinical models of pancreatic ductal adenocarcinoma. Cancers 12:123816
     [Google Scholar]
  33. Hughes CS, Postovit LM, Lajoie GA. 2010. Matrigel: a complex protein mixture required for optimal growth of cell culture. Proteomics 10:91886–90
     [Google Scholar]
  34. Ingber DE. 2022. Human organs-on-chips for disease modelling, drug development and personalized medicine. Nat. Rev. Genet. 23:467–91
     [Google Scholar]
  35. Jain T, Sharma P, Are AC, Vickers SM, Dudeja V. 2021. New insights into the cancer–microbiome–immune axis: decrypting a decade of discoveries. Front. Immunol. 12:622064
     [Google Scholar]
  36. Jalili-Firoozinezhad S, Gazzaniga FS, Calamari EL, Camacho DM, Fadel CW et al. 2019. A complex human gut microbiome cultured in an anaerobic intestine-on-a-chip. Nat. Biomed. Eng. 3:7520–31
     [Google Scholar]
  37. Jenkins RW, Aref AR, Lizotte PH, Ivanova E, Stinson S et al. 2018. Ex vivo profiling of PD-1 blockade using organotypic tumor spheroids. Cancer Discov 8:2196–215
     [Google Scholar]
  38. Jin Y, Kim J, Lee JS, Min S, Kim S et al. 2018. Vascularized liver organoids generated using induced hepatic tissue and dynamic liver-specific microenvironment as a drug testing platform. Adv. Funct. Mater. 28:371801954
     [Google Scholar]
  39. Karin M, Clevers H. 2016. Reparative inflammation takes charge of tissue regeneration. Nature 529:7586307–15
     [Google Scholar]
  40. Kasendra M, Tovaglieri A, Sontheimer-Phelps A, Jalili-Firoozinezhad S, Bein A et al. 2018. Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids. Sci. Rep. 8:2871
     [Google Scholar]
  41. Kaur S, Kaur I, Rawal P, Tripathi DM, Vasudevan A. 2021. Non-matrigel scaffolds for organoid cultures. Cancer Lett 504:58–66
     [Google Scholar]
  42. Koh V, Chakrabarti J, Torvund M, Steele N, Hawkins JA et al. 2021. Hedgehog transcriptional effector GLI mediates mTOR-induced PD-L1 expression in gastric cancer organoids. Cancer Lett 518:59–71
     [Google Scholar]
  43. Kong J, Guerra GR, Millen RM, Roth S, Xu H et al. 2018. Tumor-infiltrating lymphocyte function predicts response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. JCP Precis. Oncol. 2: https://doi.org/10.1200/PO.18.00075
    [Google Scholar]
  44. Kozlowski MT, Crook CJ, Ku HT. 2021. Towards organoid culture without Matrigel. Commun. Biol. 4:1387
     [Google Scholar]
  45. Kuol N, Stojanovska L, Apostolopoulos V, Nurgali K. 2018. Crosstalk between cancer and the neuro-immune system. J. Neuroimmunol. 315:15–23
     [Google Scholar]
  46. Li X, Nadauld L, Ootani A, Corney DC et al. 2014. Oncogenic transformation of diverse gastrointestinal tissues in primary organoid culture. Nat. Med. 20:7769–77
     [Google Scholar]
  47. Liang W, Ferrara N. 2016. The complex role of neutrophils in tumor angiogenesis and metastasis. Cancer Immunol. Res. 4:283–91
     [Google Scholar]
  48. Lucca LE, Axisa PP, Lu B, Harnett B, Jessel S et al. 2021. Circulating clonally expanded T cells reflect functions of tumor-infiltrating T cells. J. Exp. Med. 218:4e20200921
     [Google Scholar]
  49. Mak IW, Evaniew N, Ghert M. 2014. Lost in translation: animal models and clinical trials in cancer treatment. Am. J. Transl. Res. 6:2114–18
     [Google Scholar]
  50. Mäkinen L, Vähä-Koskela M, Juusola M, Mustonen H, Wennerberg K et al. 2022. Pancreatic cancer organoids in the field of precision medicine: a review of literature and experience on drug sensitivity testing with multiple readouts and synergy scoring. Cancers 14:3525
     [Google Scholar]
  51. Mazzocchi AR, Rajan SA, Votanopoulos KI, Hall AR, Skardal A. 2018. In vitro patient-derived 3D mesothelioma tumor organoids facilitate patient-centric therapeutic screening. Sci. Rep. 8:2886
     [Google Scholar]
  52. Medetgul-Ernar K, Davis MM. 2022. Standing on the shoulders of mice. Immunity 55:81343–53
     [Google Scholar]
  53. Mestas J, Hughes CC. 2004. Of mice and not men: differences between mouse and human immunology. J. Immunol. 172:52731–38
     [Google Scholar]
  54. Miron-Mendoza M, Seemann J, Grinnell F. 2010. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 31:256425–35
     [Google Scholar]
  55. Mullard A. 2016. Parsing clinical success rates. Nat. Rev. Drug Discov. 15:7447–8
     [Google Scholar]
  56. Nashimoto Y, Hayashi T, Kunita I, Nakamasu A, Torisawa YS et al. 2017. Integrating perfusable vascular networks with a three-dimensional tissue in a microfluidic device. Integr. Biol. 9:6506–18
     [Google Scholar]
  57. Neal JT, Li X, Zhu J, Giangarra V, Grzeskowiak CL et al. 2018. Organoid modeling of the tumor immune microenvironment. Cell 175:71972–88
     [Google Scholar]
  58. Nissen MD, Sloan EK, Mattarollo SR. 2018. β-Adrenergic signaling impairs antitumor CD8+ T-cell responses to B-cell lymphoma immunotherapy. Cancer Immunol. Res. 6:98–109
     [Google Scholar]
  59. Ooft SN, Weeber F, Schipper L, Dijkstra KK, McLean CM et al. 2021. Prospective experimental treatment of colorectal cancer patients based on organoid drug responses. ESMO Open 6:3100103
     [Google Scholar]
  60. Ootani A, Li X, Sangiorgi E, Ho QT, Ueno H et al. 2009. Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat. Med. 15:6701–6
     [Google Scholar]
  61. Park CS, Nguyen LP, Yong D 2020. Development of colonic organoids containing enteric nerves or blood vessels from human embryonic stem cells. Cells 9:102209
     [Google Scholar]
  62. Park NY, Koh A. 2022. From the dish to the real world: modeling interactions between the gut and microorganisms in gut organoids by tailoring the gut milieu. Int. J. Stem Cells 15:70–84
     [Google Scholar]
  63. Park SE, Georgescu A, Huh D. 2019. Organoids-on-a-chip. Science 364:6444960–65
     [Google Scholar]
  64. Pham MT, Pollock KM, Rose MD, Cary WA, Stewart HR et al. 2018. Generation of human vascularized brain organoids. Neuroreport 29:7588–93
     [Google Scholar]
  65. Pleguezuelos-Manzano C, Puschhof J, Rosendahl Huber A, van Hoeck A, Wood HM et al. 2020. Mutational signature in colorectal cancer caused by genotoxic pks+E. coli. Nature 580:7802269–73
     [Google Scholar]
  66. Postow MA, Callahan MK, Wolchok JD. 2015. Immune checkpoint blockade in cancer therapy. J. Clin. Oncol. 33:171974–82
     [Google Scholar]
  67. Potente M, Carmeliet P. 2017. The link between angiogenesis and endothelial metabolism. Annu. Rev. Physiol. 79:43–66
     [Google Scholar]
  68. Rajasekar S, Lin DS, Abdul L, Liu A, Sotra A et al. 2020. IFlowPlate—a customized 384-well plate for the culture of perfusable vascularized colon organoids. Adv. Mater. 32:462002974
     [Google Scholar]
  69. Reticker-Flynn NE, Zhang W, Belk JA, Basto PA, Escalante NK et al. 2022. Lymph node colonization induces tumor-immune tolerance to promote distant metastasis. Cell 185:111924–42
     [Google Scholar]
  70. Roberts KJ, Kershner AM, Beachy PA. 2017. The stromal niche for epithelial stem cells: a template for regeneration and a brake on malignancy. Cancer Cell 32:4404–10
     [Google Scholar]
  71. Rooks MG, Garrett WS. 2016. Gut microbiota, metabolites and host immunity. Nat. Rev. Immunol. 16:6341–52
     [Google Scholar]
  72. Sachs N, Papaspyropoulos A, Zomer-van Ommen DD, Heo I, Böttinger L et al. 2019. Long-term expanding human airway organoids for disease modeling. EMBO J 38:4e100300
     [Google Scholar]
  73. Sahai E, Astsaturov I, Cukierman E, DeNardo DG, Egeblad M et al. 2020. A framework for advancing our understanding of cancer-associated fibroblasts. Nat. Rev. Cancer 20:3174–86
     [Google Scholar]
  74. Sasaki N, Miyamoto K, Maslowski KM, Ohno H, Kanai T, Sato T. 2020. Development of a scalable coculture system for gut anaerobes and human colon epithelium. Gastroenterology 159:388–90
     [Google Scholar]
  75. Sato T, Vries RG, Snippert HJ, van De Wetering M, Barker N et al. 2009. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459:7244262–65
     [Google Scholar]
  76. Schlieve CR, Fowler KL, Thornton M, Huang S, Hajjali I et al. 2017. Neural crest cell implantation restores enteric nervous system function and alters the gastrointestinal transcriptome in human tissue-engineered small intestine. Stem Cell Rep 9:3883–96
     [Google Scholar]
  77. Schnalzger TE, de Groot MH, Zhang C, Mosa MH, Michels BE et al. 2019. 3D model for CAR-mediated cytotoxicity using patient-derived colorectal cancer organoids. EMBO J 38:12e100928
     [Google Scholar]
  78. Schreurs RR, Baumdick ME, Sagebiel AF, Kaufmann M, Mokry M et al. 2019. Human fetal TNF-α-cytokine-producing CD4+ effector memory T cells promote intestinal development and mediate inflammation early in life. Immunity 50:2462–76
     [Google Scholar]
  79. Scognamiglio G, De Chiara A, Parafioriti A, Armiraglio E, Fazioli F et al. 2019. Patient-derived organoids as a potential model to predict response to PD-1/PD-L1 checkpoint inhibitors. Br. J. Cancer 121:11979–82
     [Google Scholar]
  80. Shanti A, Hallfors N, Petroianu GA, Planelles L, Stefanini C. 2021. Lymph nodes-on-chip: promising immune platforms for pharmacological and toxicological applications. Front. Pharmacol. 12:711307
     [Google Scholar]
  81. Shim S, Belanger MC, Harris AR, Munson JM, Pompano RR. 2019. Two-way communication between ex vivo tissues on a microfluidic chip: application to tumor–lymph node interaction. Lab Chip 19:61013–26
     [Google Scholar]
  82. Shurin MR, Shurin GV, Zlotnikov SB, Bunimovich YL. 2020. The neuroimmune axis in the tumor microenvironment. J. Immunol. 204:2280–85
     [Google Scholar]
  83. Singh N, Gurav A, Sivaprakasam S, Brady E, Padia R et al. 2014. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40:128–39
     [Google Scholar]
  84. Sloan EK, Priceman SJ, Cox BF, Yu S, Pimentel MA et al. 2010. The sympathetic nervous system induces a metastatic switch in primary breast cancer. Cancer Res 70:187042–52
     [Google Scholar]
  85. Sontheimer-Phelps A, Hassell BA, Ingber DE. 2019. Modelling cancer in microfluidic human organs-on-chips. Nat. Rev. Cancer 19:265–81
     [Google Scholar]
  86. Tsai S, McOlash L, Palen K, Johnson B, Duris C et al. 2018. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer 18:335
     [Google Scholar]
  87. Tuveson D, Clevers H. 2019. Cancer modeling meets human organoid technology. Science 364:6444952–55
     [Google Scholar]
  88. van Pul KM, Fransen MF, van de Ven R, de Gruijl TD. 2021. Immunotherapy goes local: the central role of lymph nodes in driving tumor infiltration and efficacy. Front. Immunol. 12:643291
     [Google Scholar]
  89. van Riet S, van Schadewijk A, Khedoe PP, Limpens RW, Bárcena M et al. 2022. Organoid-based expansion of patient-derived primary alveolar type 2 cells for establishment of alveolus epithelial Lung-Chip cultures. Am. J. Physiol. Lung Cell. Mol. Physiol. 322:4L526–38
     [Google Scholar]
  90. Vlachogiannis G, Hedayat S, Vatsiou A, Jamin Y, Fernández-Mateos J et al. 2018. Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science 359:6378920–26
     [Google Scholar]
  91. Voabil P, de Bruijn M, Roelofsen LM, Hendriks SH, Brokamp S et al. 2021. An ex vivo tumor fragment platform to dissect response to PD-1 blockade in cancer. Nat. Med. 27:71250–61
     [Google Scholar]
  92. Votanopoulos KI, Forsythe S, Sivakumar H, Mazzocchi A, Aleman J et al. 2020. Model of patient-specific immune-enhanced organoids for immunotherapy screening: feasibility study. Ann. Surg. Oncol. 27:61956–67
     [Google Scholar]
  93. Wagar LE, Salahudeen A, Constantz CM, Wendel BS, Lyons MM et al. 2021. Modeling human adaptive immune responses with tonsil organoids. Nat. Med. 27:125–35
     [Google Scholar]
  94. Wang H, Zheng Q, Lu Z, Wang L, Ding L et al. 2021. Role of the nervous system in cancers: a review. Cell Death Discov 7:76
     [Google Scholar]
  95. Williamson IA, Arnold JW, Samsa LA, Gaynor L, DiSalvo M et al. 2018. A high-throughput organoid microinjection platform to study gastrointestinal microbiota and luminal physiology. Cell. Mol. Gastroenterol. Hepatol. 6:3301–19
     [Google Scholar]
  96. Wolchok JD, Chiarion-Sileni V, Gonzalez R, Rutkowski P, Grob JJ et al. 2017. Overall survival with combined nivolumab and ipilimumab in advanced melanoma. N. Engl. J. Med. 377:141345–56
     [Google Scholar]
  97. Workman MJ, Mahe MM, Trisno S, Poling HM, Watson CL et al. 2017. Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system. Nat. Med. 23:49–59
     [Google Scholar]
  98. Wörsdörfer P, Dalda N, Kern A, Krüger S, Wagner N et al. 2019. Generation of complex human organoid models including vascular networks by incorporation of mesodermal progenitor cells. Sci. Rep. 9:15663
     [Google Scholar]
  99. Yang J, Yan J, Liu B 2018. Targeting VEGF/VEGFR to modulate antitumor immunity. Front. Immunol. 9:978
     [Google Scholar]
  100. Yao Y, Xu X, Yang L, Zhu J, Wan J et al. 2020. Patient-derived organoids predict chemoradiation responses of locally advanced rectal cancer. Cell Stem Cell 26:117–26
     [Google Scholar]
  101. Yuki K, Cheng N, Nakano M, Kuo CJ. 2020. Organoid models of tumor immunology. Trends Immunol 41:8652–64
     [Google Scholar]
  102. Zaman MH, Trapani LM, Sieminski AL, MacKellar D, Gong H et al. 2006. Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. PNAS 103:2910889–94
     [Google Scholar]
  103. Zetter BR. 1998. Angiogenesis and tumor metastasis. Annu. Rev. Med. 49:407–24
     [Google Scholar]
  104. Zhou G, Lieshout R, van Tienderen GS, de Ruiter V, van Royen ME et al. 2022. Modelling immune cytotoxicity for cholangiocarcinoma with tumour-derived organoids and effector T cells. Br. J. Cancer 127:649–60
     [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-061421-040659
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Engineering the Immune Microenvironment into Organoid Models
Annual Review of Cancer Biology 7, 171 (2023); https://doi.org/10.1146/annurev-cancerbio-061421-040659
/content/journals/10.1146/annurev-cancerbio-061421-040659
/content/journals/10.1146/annurev-cancerbio-061421-040659
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