Personalized Vascularized Models of Breast Cancer Desmoplasia Reveal Biomechanical Determinants of Drug Delivery to the Tumor.
TGFβ mechanotherapy
hyaluronic acid
microphysiological systems
permeability
tumor vascularization
vascular glycocalyx
Journal
Advanced science (Weinheim, Baden-Wurttemberg, Germany)
ISSN: 2198-3844
Titre abrégé: Adv Sci (Weinh)
Pays: Germany
ID NLM: 101664569
Informations de publication
Date de publication:
23 Jul 2024
23 Jul 2024
Historique:
revised:
01
07
2024
received:
15
03
2024
medline:
23
7
2024
pubmed:
23
7
2024
entrez:
23
7
2024
Statut:
aheadofprint
Résumé
Desmoplasia in breast cancer leads to heterogeneity in physical properties of the tissue, resulting in disparities in drug delivery and treatment efficacy among patients, thus contributing to high disease mortality. Personalized in vitro breast cancer models hold great promise for high-throughput testing of therapeutic strategies to normalize the aberrant microenvironment in a patient-specific manner. Here, tumoroids assembled from breast cancer cell lines (MCF7, SKBR3, and MDA-MB-468) and patient-derived breast tumor cells (TCs) cultured in microphysiological systems including perfusable microvasculature reproduce key aspects of stromal and vascular dysfunction causing impaired drug delivery. Models containing SKBR3 and MDA-MB-468 tumoroids show higher stromal hyaluronic acid (HA) deposition, vascular permeability, interstitial fluid pressure (IFP), and degradation of vascular HA relative to models containing MCF7 tumoroids or models without tumoroids. Interleukin 8 (IL8) secretion is found responsible for vascular dysfunction and loss of vascular HA. Interventions targeting IL8 or stromal HA normalize vascular permeability, perfusion, and IFP, and ultimately enhance drug delivery and TC death in response to perfusion with trastuzumab and cetuximab. Similar responses are observed in patient-derived models. These microphysiological systems can thus be personalized by using patient-derived cells and can be applied to discover new molecular therapies for the normalization of the tumor microenvironment.
Identifiants
pubmed: 39041892
doi: 10.1002/advs.202402757
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2402757Subventions
Organisme : Swiss National Science Foundation
ID : P2EZP2_199914
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : P500PB_222131
Pays : Switzerland
Organisme : Swiss National Science Foundation
ID : SNSF-P400PB_186779
Pays : Switzerland
Organisme : Ludwig Center at MIT Koch Institute for Integrative Cancer Research
Organisme : NCI NIH HHS
ID : K00CA212227
Pays : United States
Organisme : NCI NIH HHS
ID : U01CA214381
Pays : United States
Organisme : NCI NIH HHS
ID : U54CA261694
Pays : United States
Organisme : Fondazione AIRC per la ricerca sul cancro ETS
ID : IG21479
Organisme : American-Italian Cancer Foundation
Organisme : Amgen
Informations de copyright
© 2024 The Author(s). Advanced Science published by Wiley‐VCH GmbH.
Références
G. Turashvili, E. Brogi, Front. Med. 2017, 4, 227.
Y. Feng, M. Spezia, S. Huang, C. Yuan, Z. Zeng, L. Zhang, X. Ji, W. Liu, B. Huang, W. Luo, B. Liu, Y. Lei, S. Du, A. Vuppalapati, H. H. Luu, R. C. Haydon, T. C. He, G. Ren, Genes Dis. 2018, 5, 77.
R. A. Walker, Breast Cancer Res. 2001, 3, 143.
J. Winkler, A. Abisoye‐Ogunniyan, K. J. Metcalf, Z. Werb, Nat. Commun. 2020, 11, 5120.
J. Alexander, E. Cukierman, Matrix Biol. 2020, 91‐92, 19.
E. Cambria, M. F. Coughlin, M. A. Floryan, G. S. Offeddu, S. E. Shelton, R. D. Kamm, Nat. Rev. Cancer 2024, 24, 216.
M. G. Rooks, W. S. Garrett, Physiol. Behav. 2017, 176, 139.
E. Henke, R. Nandigama, S. Ergün, Front. Mol. Biosci. 2020, 6, 160.
C. H. Heldin, K. Rubin, K. Pietras, A. Östman, Nat. Rev. Cancer 2004, 4, 806.
C. Sheridan, Nat. Biotechnol. 2019, 37, 829.
S. Nath, G. R. Devi, Pharmacol. Ther. 2016, 163, 94.
P. A. Mollica, E. N. Booth‐Creech, J. A. Reid, M. Zamponi, S. M. Sullivan, X. L. Palmer, P. C. Sachs, R. D. Bruno, Acta Biomater. 2019, 95, 201.
R. W. Jenkins, A. R. Aref, P. H. Lizotte, E. Ivanova, S. Stinson, C. W. Zhou, M. Bowden, J. Deng, H. Liu, D. Miao, M. X. He, W. Walker, G. Zhang, T. Tian, C. Cheng, Z. Wei, S. Palakurthi, M. Bittinger, H. Vitzthum, J. W. Kim, A. Merlino, M. Quinn, C. Venkataramani, J. A. Kaplan, A. Portell, P. C. Gokhale, B. Phillips, A. Smart, A. Rotem, R. E. Jones, et al., Cancer Discovery 2018, 8, 196.
D. F. Lee, J. Su, H. S. Kim, B. Chang, D. Papatsenko, R. Zhao, Y. Yuan, J. Gingold, W. Xia, H. Darr, R. Mirzayans, M. C. Hung, C. Schaniel, I. R. Lemischka, Cell 2015, 161, 240.
C. Moccia, K. Haase, Front. Bioeng. Biotechnol. 2021, 9, 694218.
X. Liu, J. Fang, S. Huang, X. Wu, X. Xie, J. Wang, F. Liu, M. Zhang, Z. Peng, N. Hu, Microsyst. Nanoeng. 2021, 7, 50.
A. Boussommier‐Calleja, R. Li, M. B. Chen, S. C. Wong, R. D. Kamm, Trends Cancer 2016, 2, 6.
G. S. Offeddu, Y. Shin, R. D. Kamm, Curr. Opin. Biomed. Eng. 2019, 13, 119.
A. R. Aref, M. Campisi, E. Ivanova, A. Portell, D. Larios, B. P. Piel, N. Mathur, C. Zhou, R. V. Coakley, A. Bartels, M. Bowden, Z. Herbert, S. Hill, S. Gilhooley, J. Carter, I. Cañadas, T. C. Thai, S. Kitajima, V. Chiono, C. P. Paweletz, D. A. Barbie, R. D. Kamm, R. W. Jenkins, Lab Chip 2018, 18, 3129.
J. C. Serrano, S. K. Gupta, R. D. Kamm, M. Guo, Annu. Rev. Fluid Mech. 2021, 53, 411.
M. F. Coughlin, R. D. Kamm, Adv. Healthcare Mater. 2020, 9, 1901410.
J. Pape, M. Emberton, U. Cheema, Front. Bioeng. Biotechnol. 2021, 9, 660502.
K. Haase, G. S. Offeddu, M. R. Gillrie, R. D. Kamm, Adv. Funct. Mater. 2020, 30, https://doi.org/10.1002/adfm.202002444.
X. Dai, H. Cheng, Z. Bai, J. Li, J. Cancer 2017, 8, 3131.
J. Insua‐Rodríguez, T. Oskarsson, Adv. Drug Delivery Rev. 2016, 97, 41.
Y. Sheng, M. Cao, Y. Liu, Y. He, G. Zhang, Y. Du, F. Gao, C. Yang, Mol. Cell. Biochem. 2021, 2,.
K. Shiga, M. Hara, T. Nagasaki, T. Sato, H. Takahashi, H. Takeyama, Cancers 2015, 7, 2443.
P. Bordignon, G. Bottoni, X. Xu, A. S. Popescu, Z. Truan, E. Guenova, L. Kofler, P. Jafari, P. Ostano, M. Röcken, V. Neel, G. P. Dotto, Cell Rep. 2019, 28, 2358.
L. Udabage, G. R. Brownlee, S. K. Nilsson, T. J. Brown, Exp. Cell Res. 2005, 310, 205.
R. K. Jain, Cancer Metastasis Rev. 1990, 9, 253.
E. Tagliabue, M. Campiglio, S. M. Pupa, S. Ménard, A. Balsari, Cancer Treat. Rev. 2012, 38, 212.
L. A. Applegate, D. P. Pioletti, Eur. Biopharm. Rev. 2010, 28, https://infoscience.epfl.ch/record/154224?ln=en&v=pdf.
G. S. Offeddu, L. Possenti, J. T. Loessberg‐Zahl, P. Zunino, J. Roberts, X. Han, D. Hickman, C. G. Knutson, R. D. Kamm, Small 2019, 15, 1902393.
X. Hu, S. Weinbaum, Microvasc. Res. 1999, 58, 281.
C. C. Dufort, K. E. Delgiorno, S. R. Hingorani, Gastroenterology 2016, 150, 1545.
P. A. Netti, D. A. Berk, M. A. Swartz, A. J. Grodzinsky, R. K. Jain, Cancer Res. 2000, 60, 2497.
M. Soltani, M. Sefidgar, H. Bazmara, C. Marcus, R. M. Subramaniam, A. Rahmim, in 2015 IEEE Nuclear Science Symp. and Medical Imaging Conf. NSS/MIC, IEEE, Piscataway, NJ, 2016, https://doi.org/10.1109/NSSMIC.2015.7582238.
K. Hashizume, K. L. Black, J. Neuropathol. Exp. Neurol. 2002, 61, 725.
S. Weinbaum, J. M. Tarbell, E. R. Damiano, Annu. Rev. Biomed. Eng. 2007, 9, 121.
G. Wang, G. L. Tiemeier, B. M. van den Berg, T. J. Rabelink, Am. J. Pathol. 2020, 190, 781.
P. Zhao, M. S. Damerow, P. Stern, A. H. Liu, A. Sweet‐Cordero, K. Siziopikou, J. R. Neilson, P. A. Sharp, C. Cheng, Oncogene 2013, 32, 5186.
R. C. Andresen Eguiluz, K. B. Kaylan, G. H. Underhill, D. E. Leckband, Biomaterials 2017, 140, 45.
S. V. Lopez‐Quintero, R. Amaya, M. Pahakis, J. M. Tarbell, Am. J. Physiol.: Heart Circ. Physiol. 2009, 296, H1451.
G. S. Offeddu, K. Haase, M. R. Gillrie, R. Li, O. Morozova, D. Hickman, C. G. Knutson, R. D. Kamm, Biomaterials 2019, 212, 115.
G. S. Offeddu, C. Hajal, C. R. Foley, Z. Wan, L. Ibrahim, M. F. Coughlin, R. D. Kamm, Commun. Biol. 2021, 4, 255.
D. Chappell, K. Hofmann‐kiefer, U. Welsch, B. F. Becker, Basic Res Cardiol 2009, 104, 78.
M. Esquivel‐Velázquez, P. Ostoa‐Saloma, M. I. Palacios‐Arreola, K. E. Nava‐Castro, J. I. Castro, J. Morales‐Montor, J. Interferon Cytokine Res. 2015, 35, https://doi.org/10.1089/jir.2014.0026.
A. Li, S. Dubey, M. L. Varney, B. J. Dave, R. K. Singh, J. Immunol. 2003, 170, 3369.
S. Meran, D. Thomas, P. Stephens, J. Martin, T. Bowen, A. Phillips, R. Steadman, J. Biol. Chem. 2007, 282, 25687.
T. Stylianopoulos, J. D. Martin, M. Snuderl, F. Mpekris, S. R. Jain, R. K. Jain, Cancer Res. 2013, 73, 3833.
F. Mpekris, M. Panagi, C. Voutouri, J. D. Martin, R. Samuel, S. Takahashi, N. Gotohda, T. Suzuki, P. Papageorgis, P. Demetriou, C. Pierides, L. Koumas, P. Costeas, M. Kojima, G. Ishii, A. Constantinidou, K. Kataoka, H. Cabral, T. Stylianopoulos, Adv. Sci. 2021, 8, 2001917.
C. Chen, S. Zhao, A. Karnad, J. W. Freeman, J. Hematol. Oncol. 2018, 11, 64.
B. Bernert, H. Porsch, P. Heldin, J. Biol. Chem. 2011, 286, 42349.
P. Auvinen, R. Tammi, J. Parkkinen, M. Tammi, U. Ågren, R. Johansson, P. Hirvikoski, M. Eskelinen, V. M. Kosma, Am. J. Pathol. 2000, 156, 529.
A. B. Ariffin, P. F. Forde, S. Jahangeer, D. M. Soden, J. Hinchion, Cancer Res. 2014, 74, 2655.
K. Keramida, J. Thymis, M. Anastasiou, K. Katogiannis, I. Kotsantis, P. Economopoulou, V. Pappa, P. Tsirigotis, V. Bistola, M. Thodi, A. Psyrri, G. Filippatos, I. Ikonomidis, Int. J. Cardiol. 2022, 360, 62.
S. Weinbaum, L. M. Cancel, B. M. Fu, J. M. Tarbell, Cardiovasc. Eng. Technol. 2021, 12, 37.
I. H. Benoy, R. Salgado, P. Van Dam, K. Geboers, E. Van Marck, S. Scharpé, P. B. Vermeulen, L. Y. Dirix, Clin. Cancer Res. 2004, 10, 7157.
N. Todorović‐Raković, J. Milovanović, J. Interferon Cytokine Res. 2013, 33, 563.
J. D. Martin, M. Panagi, C. Wang, T. T. Khan, M. R. Martin, C. Voutouri, K. Toh, P. Papageorgis, F. Mpekris, C. Polydorou, G. Ishii, S. Takahashi, N. Gotohda, T. Suzuki, M. E. Wilhelm, V. A. Melo, S. Quader, J. Norimatsu, R. M. Lanning, M. Kojima, M. D. Stuber, T. Stylianopoulos, K. Kataoka, H. Cabral, ACS Nano 2019, 13, 6396.
P. Papageorgis, T. Stylianopoulos, Int. J. Oncol. 2015, 46, 933.
J. Liu, S. Liao, B. Diop‐Frimpong, W. Chen, S. Goel, K. Naxerova, M. Ancukiewicz, Y. Boucher, R. K. Jain, L. Xu, Proc. Natl. Acad. Sci. USA 2012, 109, 16618.
J. B. McCarthy, D. El‐Ashry, E. A. Turley, Front. Cell Dev. Biol. 2018, 6, 48.
R. A. A. Mohammed, I. O. Ellis, A. M. Mahmmod, E. C. Hawkes, A. R. Green, E. A. Rakha, S. G. Martin, Mod. Pathol. 2011, 24, 774.
E. M. Huuse, S. A. Moestue, E. M. Lindholm, T. F. Bathen, H. Nalwoga, K. Krüger, A. Bofin, G. M. Mælandsmo, L. A. Akslen, O. Engebraaten, I. S. Gribbestad, J. Magn. Reson. Imaging 2012, 35, 1098.
K. Krüger, I. M. Stefansson, K. Collett, J. B. Arnes, T. Aas, L. A. Akslen, Breast 2013, 22, 282.
I. S. Bujor, A. Cioca, R. A. Ceaușu, F. Veaceslav, C. Nica, A. M. Cîmpean, M. Raica, In Vivo (Brooklyn). 2018, 32, 79.
S. E. Tarullo, Y. He, C. Daughters, T. P. Knutson, C. M. Henzler, M. A. Price, R. Shanley, P. Witschen, C. Tolg, R. E. Kaspar, C. Hallstrom, L. Gittsovich, M. L. Sulciner, X. Zhang, C. L. Forster, C. A. Lange, O. Shats, M. Desler, K. H. Cowan, D. Yee, K. L. Schwertfeger, E. A. Turley, J. B. McCarthy, A. C. Nelson, J. Pathol. 2023, 260, 289.
Z. Wan, S. Zhang, A. X. Zhong, S. E. Shelton, M. Campisi, S. K. Sundararaman, G. S. Offeddu, E. Ko, L. Ibrahim, M. F. Coughlin, T. Liu, J. Bai, D. A. Barbie, R. D. Kamm, Biomaterials 2021, 276, 121032.
G. S. Offeddu, J. C. Serrano, S. W. Chen, S. E. Shelton, Y. Shin, M. Floryan, R. D. Kamm, J. Biomech. 2021, 119, 110330.
K. Haase, M. R. Gillrie, C. Hajal, R. D. Kamm, Adv. Sci. 2019, 6, 1900878.
K. Haase, F. Piatti, M. Marcano, Y. Shin, R. Visone, A. Redaelli, M. Rasponi, R. D. Kamm, bioRxiv, 2021, https://doi.org/10.1016/j.biomaterials.2021.121248.
J. Scallan, V. H. Huxley, R. J. Korthuis, Capillary Fluid Exchange, Morgan & Claypool Life Sciences, San Rafael, CA 2010, PMID: 21452435.
C. Hajal, G. S. Offeddu, Y. Shin, S. Zhang, O. Morozova, D. Hickman, C. G. Knutson, R. D. Kamm, Nat. Protoc. 2022, 17, 95.