Recreating the extracellular matrix: novel 3D cell culture platforms in cancer research.
3-dimensional matrix
cancer
cell culture systems
extracellular matrix
tumour microenvironment
Journal
The FEBS journal
ISSN: 1742-4658
Titre abrégé: FEBS J
Pays: England
ID NLM: 101229646
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
revised:
23
02
2023
received:
22
12
2022
accepted:
15
03
2023
medline:
16
11
2023
pubmed:
18
3
2023
entrez:
17
3
2023
Statut:
ppublish
Résumé
Cancer initiation and progression heavily rely on microenvironmental cues derived from various components of the niche including the extracellular matrix (ECM). ECM is a complex macromolecular network that governs cell functionality. Although the two-dimensional (2D) cell culture systems provide useful information at the molecular level and preclinical testing, they could not accurately represent the in vivo matrix microenvironmental architecture. Hence, it is no surprise that researchers in the last decade have focussed their efforts on establishing novel advanced in vitro culture models that mimic tumour and tissue-specific niches and interactions. These numerous three-dimensional (3D) culture systems that are now widely available, as well as those still under development, grant researchers with new, improved tools to study cancer progression and to explore innovative therapeutic options. Herein, we report on the emerging methods and cutting-edge technologies in 3D cell culture platforms and discuss their potential use in unveiling tumour microenvironmental cues, drug screening and personalized treatment.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
5238-5247Informations de copyright
© 2023 The Authors. The FEBS Journal published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
Iozzo RV, Theocharis AD, Neill T & Karamanos NK (2020) Complexity of matrix phenotypes. Matrix Biol Plus 6-7, 100038.
Karamanos NK, Theocharis AD, Piperigkou Z, Manou D, Passi A, Skandalis SS, Vynios DH, Orian-Rousseau V, Ricard-Blum S, Schmelzer CEH et al. (2021) A guide to the composition and functions of the extracellular matrix. FEBS J 288, 6850-6912.
Karamanos NK, Piperigkou Z, Passi A, Götte M, Rousselle P & Vlodavsky I (2021) Extracellular matrix-based cancer targeting. Trends Mol Med 27, 1000-1013.
Manou D, Caon I, Bouris P, Triantaphyllidou I-E, Giaroni C, Passi A, Karamanos NK, Vigetti D & Theocharis AD (2019) The complex interplay between extracellular matrix and cells in tissues. Methods Mol Biol 1952, 1-20.
Piperigkou Z, Kyriakopoulou K, Koutsakis C, Mastronikolis S & Karamanos NK (2021) Key matrix remodeling enzymes: functions and targeting in cancer. Cancers (Basel) 13, 1441.
Vlodavsky I, Singh P, Boyango I, Gutter-Kapon L, Elkin M, Sanderson RD & Ilan N (2016) Heparanase: from basic research to therapeutic applications in cancer and inflammation. Drug Resist Updat 29, 54-75.
Manou D, Karamanos NK & Theocharis AD (2020) Tumorigenic functions of serglycin: regulatory roles in epithelial to mesenchymal transition and oncogenic signaling. Semin Cancer Biol 62, 108-115.
Kokoretsis D, Maniaki E, Kyriakopoulou K, Koutsakis C, Piperigkou Z & Karamanos NK (2022) Hyaluronan as “Agent Smith” in cancer extracellular matrix pathobiology: regulatory roles in immune response, cancer progression and targeting. IUBMB Life 74, 943-954.
Tavianatou AG, Caon I, Franchi M, Piperigkou Z, Galesso D & Karamanos NK (2019) Hyaluronan: molecular size-dependent signaling and biological functions in inflammation and cancer. FEBS J 286, 2883-2908.
Caon I, Parnigoni A, Viola M, Karousou E, Passi A & Vigetti D (2021) Cell energy metabolism and hyaluronan synthesis. J Histochem Cytochem 69, 35-47.
Turtoi M, Anghelache M, Bucatariu S-M, Deleanu M, Voicu G, Safciuc F, Manduteanu I, Fundueanu G, Simionescu M & Calin M (2021) A novel platform for drug testing: biomimetic three-dimensional hyaluronic acid-based scaffold seeded with human hepatocarcinoma cells. Int J Biol Macromol 185, 604-619.
Ström A, Larsson A & Okay O (2015) Preparation and physical properties of hyaluronic acid-based cryogels. J Appl Polym Sci 132, doi: 10.1002/app.42194
Patterson J, Siew R, Herring SW, Lin ASP, Guldberg R & Stayton PS (2010) Hyaluronic acid hydrogels with controlled degradation properties for oriented bone regeneration. Biomaterials 31, 6772-6781.
Fisher SA, Anandakumaran PN, Owen SC & Shoichet MS (2015) Tuning the microenvironment: click-crosslinked hyaluronic acid-based hydrogels provide a platform for studying breast cancer cell invasion. Adv Funct Mater 25, 7163-7172.
Franchi M, Masola V, Bellin G, Onisto M, Karamanos K & Piperigkou Z (2019) Collagen fiber array of peritumoral stroma influences epithelial-to-mesenchymal transition and invasive potential of mammary cancer cells. J Clin Med 8, 213.
Unnikrishnan K, Thomas LV & Ram Kumar RM (2021) Advancement of scaffold-based 3D cellular models in cancer tissue engineering: an update. Front Oncol 11, 733652.
Guo J, Zhao C, Yao R, Sui A, Sun L, Liu X, Wu S, Su Z, Li T, Liu S et al. (2019) 3D culture enhances chemoresistance of ALL Jurkat cell line by increasing DDR1 expression. Exp Ther Med 17, 1593-1600.
Murakami S, Mukaisho K, Iwasa T, Kawabe M, Yoshida S, Taniura N, Nakayama T, Noi M, Yamamoto G & Sugihara H (2020) Application of “tissueoid cell culture system” using a silicate fiber scaffold for cancer research. Pathobiology 87, 291-301.
Jensen C, Shay C & Teng Y (2022) The new frontier of three-dimensional culture models to scale-up cancer research. Methods Mol Biol 2343, 3-18.
Kapałczyńska M, Kolenda T, Przybyła W, Zajączkowska M, Teresiak A, Filas V, Ibbs M, Bliźniak R, Łuczewski Ł & Lamperska K (2016) 2D and 3D cell cultures - a comparison of different types of cancer cell cultures. Arch Med Sci 14, 910-919.
Langhans SA (2018) Three-dimensional in vitro cell culture models in drug discovery and drug repositioning. Front Pharmacol 9, 6.
Ho WJ, Pham EA, Kim JW, Ng CW, Kim JH, Kamei DT & Wu BM (2010) Incorporation of multicellular spheroids into 3-D polymeric scaffolds provides an improved tumor model for screening anticancer drugs. Cancer Sci 101, 2637-2643.
Habanjar O, Diab-Assaf M, Caldefie-Chezet F & Delort L (2021) 3D cell culture systems: tumor application, advantages, and disadvantages. Int J Mol Sci 22, 12200.
Xu J, Qi G, Wang W & Sun XS (2021) Advances in 3D peptide hydrogel models in cancer research. NPJ Sci Food 5, 14.
Nezhad-Mokhtari P, Ghorbani M, Roshangar L & Soleimani Rad J (2019) A review on the construction of hydrogel scaffolds by various chemically techniques for tissue engineering. Eur Polym J 117, 64-76.
Cavo M, Fato M, Peñuela L, Beltrame F, Raiteri R & Scaglione S (2016) Microenvironment complexity and matrix stiffness regulate breast cancer cell activity in a 3D in vitro model. Sci Rep 6, 35367.
Puls TJ, Tan X, Whittington CF & Voytik-Harbin SL (2017) 3D collagen fibrillar microstructure guides pancreatic cancer cell phenotype and serves as a critical design parameter for phenotypic models of EMT. PLoS One 12, e0188870.
Suo A, Xu W, Wang Y, Sun T, Ji L & Qian J (2019) Dual-degradable and injectable hyaluronic acid hydrogel mimicking extracellular matrix for 3D culture of breast cancer MCF-7 cells. Carbohydr Polym 211, 336-348.
Zhang Y, Tang C, Span PN, Rowan AE, Aalders TW, Schalken JA, Adema GJ, Kouwer PHJ, Zegers MMP & Ansems M (2020) Polyisocyanide hydrogels as a tunable platform for mammary gland organoid formation. Adv Sci 7, 2001797.
Yang D (2022) Recent advances in hydrogels. Chem Mater 34, 1987-1989.
Balion Z, Sipailaite E, Stasyte G, Vailionyte A, Mazetyte-Godiene A, Seskeviciute I, Bernotiene R, Phopase J & Jekabsone A (2020) Investigation of cancer cell migration and proliferation on synthetic extracellular matrix peptide hydrogels. Front Bioeng Biotechnol 8, 773.
Ryu N-E, Lee S-H & Park H (2019) Spheroid culture system methods and applications for mesenchymal stem cells. Cells 8, 1620.
Zhu Q, Hamilton M, Vasquez B & He M (2019) 3D-printing enabled micro-assembly of a microfluidic electroporation system for 3D tissue engineering. Lab Chip 19, 2362-2372.
Tu J, Luo X, Liu H, Zhang J & He M (2021) Cancer spheroids derived exosomes reveal more molecular features relevant to progressed cancer. Biochem Biophys Rep 26, 101026.
Bahcecioglu G, Basara G, Ellis BW, Ren X & Zorlutuna P (2020) Breast cancer models: engineering the tumor microenvironment. Acta Biomater 106, 1-21.
Türker E, Demirçak N & Arslan-Yildiz A (2018) Scaffold-free three-dimensional cell culturing using magnetic levitation. Biomater Sci 6, 1745-1753.
Huber JM, Amann A, Koeck S, Lorenz E, Kelm JM, Obexer P, Zwierzina H & Gamerith G (2016) Evaluation of assays for drug efficacy in a three-dimensional model of the lung. J Cancer Res Clin Oncol 142, 1955-1966.
Wu C-G, Chiovaro F, Curioni-Fontecedro A, Casanova R & Soltermann A (2020) In vitro cell culture of patient derived malignant pleural and peritoneal effusions for personalised drug screening. J Transl Med 18, 163.
Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ et al. (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265.
Sachs N, de Ligt J, Kopper O, Gogola E, Bounova G, Weeber F, Balgobind AV, Wind K, Gracanin A, Begthel H et al. (2018) A living biobank of breast cancer organoids captures disease heterogeneity. Cell 172, 373-386.e10.
Serra D, Mayr U, Boni A, Lukonin I, Rempfler M, Challet Meylan L, Stadler MB, Strnad P, Papasaikas P, Vischi D et al. (2019) Self-organization and symmetry breaking in intestinal organoid development. Nature 569, 66-72.
Driehuis E, van Hoeck A, Moore K, Kolders S, Francies HE, Gulersonmez MC, Stigter ECA, Burgering B, Geurts V, Gracanin A et al. (2019) Pancreatic cancer organoids recapitulate disease and allow personalized drug screening. Proc Natl Acad Sci USA 116, 26580-26590.
Kondo J, Ekawa T, Endo H, Yamazaki K, Tanaka N, Kukita Y, Okuyama H, Okami J, Imamura F, Ohue M et al. (2019) High-throughput screening in colorectal cancer tissue-originated spheroids. Cancer Sci 110, 345-355.
Randriamanantsoa S, Papargyriou A, Maurer HC, Peschke K, Schuster M, Zecchin G, Steiger K, Öllinger R, Saur D, Scheel C et al. (2022) Spatiotemporal dynamics of self-organized branching in pancreas-derived organoids. Nat Commun 13, 5219.
Tang X-Y, Wu S, Wang D, Chu C, Hong Y, Tao M, Hu H, Xu M, Guo X & Liu Y (2022) Human organoids in basic research and clinical applications. Signal Transduct Target Ther 7, 168.
Prince E, Cruickshank J, Ba-Alawi W, Hodgson K, Haight J, Tobin C, Wakeman A, Avoulov A, Topolskaia V, Elliott MJ et al. (2022) Biomimetic hydrogel supports initiation and growth of patient-derived breast tumor organoids. Nat Commun 13, 1466.
Mao B, Xu X, Sheng G, Qian W & Li HQ (2020) Transcriptome comparison among patients, PDX, PDO, PDXO, PDXC and cell lines. Eur J Cancer 138, S31.
Granat LM, Kambhampati O, Klosek S, Niedzwecki B, Parsa K & Zhang D (2019) The promises and challenges of patient-derived tumor organoids in drug development and precision oncology. Animal Model Exp Med 2, 150-161.
Yu J, Berthier E, Craig A, de Groot TE, Sparks S, Ingram PN, Jarrard DF, Huang W, Beebe DJ & Theberge AB (2019) Reconfigurable open microfluidics for studying the spatiotemporal dynamics of paracrine signalling. Nat Biomed Eng 3, 830-841.
Kim H, Chung H, Kim J, Choi D, Shin Y, Kang YG, Kim B, Seo S, Chung S & Seok SH (2019) Macrophages-triggered sequential remodeling of endothelium-interstitial matrix to form pre-metastatic niche in microfluidic tumor microenvironment. Adv Sci 6, 1900195.
Torabi S, Li L, Grabau J, Sands M, Berron BJ, Xu R & Trinkle CA (2019) Cassie-Baxter surfaces for reversible, barrier-free integration of microfluidics and 3D cell culture. Langmuir 35, 10299-10308.
Khoo BL, Grenci G, Jing T, Lim YB, Lee SC, Thiery JP, Han J & Lim CT (2016) Liquid biopsy and therapeutic response: circulating tumor cell cultures for evaluation of anticancer treatment. Sci Adv 2, e1600274.
Dankó T, Petővári G, Raffay R, Sztankovics D, Moldvai D, Vetlényi E, Krencz I, Rókusz A, Sipos K, Visnovitz T et al. (2022) Characterisation of 3D bioprinted human breast cancer model for in vitro drug and metabolic targeting. Int J Mol Sci 23, 7444.
Almela T, Al-Sahaf S, Brook IM, Khoshroo K, Rasoulianboroujeni M, Fahimipour F, Tahriri M, Dashtimoghadam E, Bolt R, Tayebi L et al. (2018) 3D printed tissue engineered model for bone invasion of oral cancer. Tissue Cell 52, 71-77.
Mondal A, Gebeyehu A, Miranda M, Bahadur D, Patel N, Ramakrishnan S, Rishi AK & Singh M (2019) Characterization and printability of sodium alginate -gelatin hydrogel for bioprinting NSCLC co-culture. Sci Rep 9, 19914.
Kääriäinen A, Pesola V, Dittmann A, Kontio J, Koivunen J, Pihlajaniemi T & Izzi V (2020) Machine learning identifies robust matrisome markers and regulatory mechanisms in cancer. Int J Mol Sci 21, 8837.