Organoid models derived from patients with malignant phyllodes tumor of the breast.
Breast
Drug screening
Histological characterization
Individual therapy
Malignant phyllodes tumor
Organoid
Journal
Breast cancer research and treatment
ISSN: 1573-7217
Titre abrégé: Breast Cancer Res Treat
Pays: Netherlands
ID NLM: 8111104
Informations de publication
Date de publication:
Jul 2023
Jul 2023
Historique:
received:
13
03
2023
accepted:
03
05
2023
medline:
7
6
2023
pubmed:
19
5
2023
entrez:
19
5
2023
Statut:
ppublish
Résumé
Phyllodes tumor of the breast is a kind of rare neoplasm, which accounts for less than 1% of all breast tumors. Malignant phyllodes tumor (MPT) is the highest risk subtype of phyllodes tumor, and is characterized by the tendency of local recurrence and distant metastasis. The prediction of prognosis and the individual therapy for MPT is still challenging. It's urgent to develop a new reliable in vitro preclinical model in order to understand this disease better and to explore appropriate anticancer drugs for individual patients. Two surgically resected MPT specimens were processed for organoid establishment. MPT organoids were subsequently subjected to H&E staining, immunohistochemical analysis and drug screening, respectively. We successfully established two organoid lines from different patients with MPT. The MPT organoids can well retain the histological features and capture the marker expression in original tumor tissues, including p63, vimentin, Bcl-2, CD34, c-Kit, and Ki-67, even after a long-term culture. The dose titration tests of eight typical chemotherapeutic drugs (paclitaxel, docetaxel, vincristine, doxorubicin, cisplatin, gemcitabine, cyclophosphamide, ifosfamide) on the two MPT organoid lines showed patient-specific drug responses and varying IC Organoids derived from MPT may be a novel preclinical model for testing personalized therapies for patients with MPT.
Identifiants
pubmed: 37204665
doi: 10.1007/s10549-023-06973-5
pii: 10.1007/s10549-023-06973-5
doi:
Substances chimiques
Antineoplastic Agents
0
Doxorubicin
80168379AG
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
193-201Subventions
Organisme : Guangdong Basic and Applied Basic Research Foundation
ID : 2021A1515110618
Organisme : Guangdong Basic and Applied Basic Research Foundation
ID : 2022A1515011428
Organisme : Shenzhen Science and Technology Program
ID : KCXFZ20211020163407011
Organisme : Shenzhen Science and Technology Program
ID : JCYJ20210324105612034
Organisme : Shenzhen Science and Technology Program
ID : JCYJ20220531094206014
Organisme : Shenzhen Science and Technology Program
ID : GJHZ20180928115030292
Organisme : Shenzhen San-Ming Project
ID : SZSM201612010
Organisme : Shenzhen Key Medical Discipline Construction Fund
ID : SZXK017
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A et al (2021) Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71(3):209–249. https://doi.org/10.3322/caac.21660
doi: 10.3322/caac.21660
pubmed: 33538338
Rosen PP, Oberman HA (1993) Tumors of the mammary gland. Armed Forces Institute of Pathology, Washington, DC, p 7
Lakhani SR, Ellis IO, Schnitt SJ, Tan PH, van de Vijver MJ (2012) World Health Organization classification of tumours. Lyon, IARC, p 4
Jorge Blanco A, Vargas Serrano B, Rodríguez Romero R, Martínez CE (1999) Phyllodes tumors of the breast. Eur Radiol 9(2):356–360. https://doi.org/10.1007/s003300050680
doi: 10.1007/s003300050680
pubmed: 10101663
Tan PH, Thike AA, Tan WJ, Thu MM, Busmanis I, Li H et al (2012) Predicting clinical behaviour of breast phyllodes tumours: a nomogram based on histological criteria and surgical margins. J Clin Pathol 65(1):69–76. https://doi.org/10.1136/jclinpath-2011-200368
doi: 10.1136/jclinpath-2011-200368
pubmed: 22049216
Lenhard MS, Kahlert S, Himsl I, Ditsch N, Untch M, Bauerfeind I (2008) Phyllodes tumour of the breast: clinical follow-up of 33 cases of this rare disease. Eur J Obstet Gynecol Reprod Biol 138(2):217–221. https://doi.org/10.1016/j.ejogrb.2007.08.002
doi: 10.1016/j.ejogrb.2007.08.002
pubmed: 17868973
Kapiris I, Nasiri N, A’Hern R, Healy V, Gui GP (2001) Outcome and predictive factors of local recurrence and distant metastases following primary surgical treatment of high-grade malignant phyllodes tumours of the breast. Eur J Surg Oncol 27(8):723–730. https://doi.org/10.1053/ejso.2001.1207
doi: 10.1053/ejso.2001.1207
pubmed: 11735168
Zhang Y, Kleer CG (2016) Phyllodes tumor of the breast: histopathologic features, differential diagnosis, and molecular/genetic updates. Arch Pathol Lab Med 140(7):665–671. https://doi.org/10.5858/arpa.2016-0042-RA
doi: 10.5858/arpa.2016-0042-RA
pubmed: 27362571
Tse GM, Niu Y, Shi HJ (2010) Phyllodes tumor of the breast: an update. Breast Cancer 17(1):29–34. https://doi.org/10.1007/s12282-009-0114-z
doi: 10.1007/s12282-009-0114-z
pubmed: 19434472
Chaney AW, Pollack A, McNeese MD, Zagars GK, Pisters PW, Pollock RE et al (2000) Primary treatment of cystosarcoma phyllodes of the breast. Cancer 89(7):1502–1511. https://doi.org/10.1002/1097-0142(20001001)89:7%3c1502::aid-cncr13%3e3.0.co;2-p
doi: 10.1002/1097-0142(20001001)89:7<1502::aid-cncr13>3.0.co;2-p
pubmed: 11013364
Strode M, Khoury T, Mangieri C, Takabe K (2017) Update on the diagnosis and management of malignant phyllodes tumors of the breast. Breast 33:91–96. https://doi.org/10.1016/j.breast.2017.03.001
doi: 10.1016/j.breast.2017.03.001
pubmed: 28327352
Domcke S, Sinha R, Levine DA, Sander C, Schultz N (2013) Evaluating cell lines as tumour models by comparison of genomic profiles. Nat Commun 4:2126. https://doi.org/10.1038/ncomms3126
doi: 10.1038/ncomms3126
pubmed: 23839242
Kamb A (2005) What’s wrong with our cancer models? Nat Rev Drug Discov 4(2):161–165. https://doi.org/10.1038/nrd1635
doi: 10.1038/nrd1635
pubmed: 15688078
Siolas D, Hannon GJ (2013) Patient-derived tumor xenografts: transforming clinical samples into mouse models. Cancer Res 73(17):5315–5319. https://doi.org/10.1158/0008-5472.CAN-13-1069
doi: 10.1158/0008-5472.CAN-13-1069
pubmed: 23733750
pmcid: 3766500
Tuveson D, Clevers H (2019) Cancer modeling meets human organoid technology. Science 364(6444):952–955. https://doi.org/10.1126/science.aaw6985
doi: 10.1126/science.aaw6985
pubmed: 31171691
Sachs N, de Ligt J, Kopper O, Gogola E, Bounova G, Weeber F et al (2018) A living biobank of breast cancer organoids captures disease heterogeneity. Cell 172(1–2):373–386. https://doi.org/10.1016/j.cell.2017.11.010
doi: 10.1016/j.cell.2017.11.010
pubmed: 29224780
Vlachogiannis G, Hedayat S, Vatsiou A, Jamin Y, Fernández-Mateos J, Khan K et al (2018) Patient-derived organoids model treatment response of metastatic gastrointestinal cancers. Science 359(6378):920–926. https://doi.org/10.1126/science.aao2774
doi: 10.1126/science.aao2774
pubmed: 29472484
pmcid: 6112415
Tiriac H, Belleau P, Engle DD, Plenker D, Deschênes A, Somerville TDD et al (2018) Organoid profiling identifies common responders to chemotherapy in pancreatic cancer. Cancer Discov 8(9):1112–1129. https://doi.org/10.1158/2159-8290.CD-18-0349
doi: 10.1158/2159-8290.CD-18-0349
pubmed: 29853643
pmcid: 6125219
Yan HHN, Siu HC, Law S, Ho SL, Yue SSK, Tsui WY et al (2018) A comprehensive human gastric cancer organoid biobank captures tumor subtype heterogeneity and enables therapeutic screening. Cell Stem Cell 23(6):882–897. https://doi.org/10.1016/j.stem.2018.09.016
doi: 10.1016/j.stem.2018.09.016
pubmed: 30344100
Ooft SN, Weeber F, Dijkstra KK, McLean CM, Kaing S, van Werkhoven E et al (2019) Patient-derived organoids can predict response to chemotherapy in metastatic colorectal cancer patients. Sci Transl Med 11(513):2574. https://doi.org/10.1126/scitranslmed.aay2574
doi: 10.1126/scitranslmed.aay2574
Chen P, Zhang X, Ding R, Yang L, Lyu X, Zeng J et al (2021) Patient-derived organoids can guide personalized-therapies for patients with advanced breast cancer. Adv Sci 8(22):2101176. https://doi.org/10.1002/advs.202101176
doi: 10.1002/advs.202101176
Xu Y, Zhu X, Hahm HS, Wei W, Hao E, Hayek A et al (2010) Revealing a core signaling regulatory mechanism for pluripotent stem cell survival and self-renewal by small molecules. Proc Natl Acad Sci USA 107(18):8129–8134. https://doi.org/10.1073/pnas.1002024107
doi: 10.1073/pnas.1002024107
pubmed: 20406903
pmcid: 2889586
Chen D, Tan Y, Li Z, Li W, Yu L, Chen W et al (2021) Organoid cultures derived from patients with papillary thyroid cancer. J Clin Endocrinol Metab 106(5):1410–1426. https://doi.org/10.1210/clinem/dgab020
doi: 10.1210/clinem/dgab020
pubmed: 33524147
Cimino-Mathews A, Sharma R, Illei PB, Vang R, Argani P (2014) A subset of malignant phyllodes tumors express p63 and p40 a diagnostic pitfall in breast core needle biopsies. Am J Surg Pathol 38(12):1689–1696. https://doi.org/10.1097/PAS.0000000000000301
doi: 10.1097/PAS.0000000000000301
pubmed: 25046342
pmcid: 4373607
Thway K, Nicholson AG, Lawson K, Gonzalez D, Rice A, Balzer B et al (2011) Primary pulmonary myxoid sarcoma with EWSR1-CREB1 fusion: a new tumor entity. Am J Surg Pathol 35(11):1722–1732. https://doi.org/10.1097/PAS.0b013e318227e4d2
doi: 10.1097/PAS.0b013e318227e4d2
pubmed: 21997693
Virk RK, Khan A (2010) Pseudoangiomatous stromal hyperplasia: an overview. Arch Pathol Lab Med 134(7):1070–1074. https://doi.org/10.5858/2008-0686-RS.1
doi: 10.5858/2008-0686-RS.1
pubmed: 20586640
Moore T, Lee AH (2001) Expression of CD34 and bcl-2 in phyllodes tumours, fibroadenomas and spindle cell lesions of the breast. Histopathology 38(1):62–67. https://doi.org/10.1046/j.1365-2559.2001.01053.x
doi: 10.1046/j.1365-2559.2001.01053.x
pubmed: 11135048
Miettinen M, Lasota J (2005) KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol 13(3):205–220. https://doi.org/10.1097/01.pai.0000173054.83414.22
doi: 10.1097/01.pai.0000173054.83414.22
pubmed: 16082245
Wang F, Jia Y, Tong Z (2015) Comparison of the clinical and prognostic features of primary breast sarcomas and malignant phyllodes tumor. Jpn J Clin Oncol 45(2):146–152. https://doi.org/10.1093/jjco/hyu177
doi: 10.1093/jjco/hyu177
pubmed: 25387733
Pervaiz N, Colterjohn N, Farrokhyar F, Tozer R, Figueredo A, Ghert M (2008) A systematic meta-analysis of randomized controlled trials of adjuvant chemotherapy for localized resectable soft-tissue sarcoma. Cancer 113(3):573–581. https://doi.org/10.1002/cncr.23592
doi: 10.1002/cncr.23592
pubmed: 18521899
Eilber FC, Brennan MF, Eilber FR, Eckardt JJ, Grobmyer SR, Riedel E et al (2007) Chemotherapy is associated with improved survival in adult patients with primary extremity synovial sarcoma. Ann Surg 246(1):105–113. https://doi.org/10.1097/01.sla.0000262787.88639.2b
doi: 10.1097/01.sla.0000262787.88639.2b
pubmed: 17592298
pmcid: 1899195
Petrioli R, Coratti A, Correale P, D’Aniello C, Grimaldi L, Tanzini G et al (2002) Adjuvant epirubicin with or without ifosfamide for adult soft-tissue sarcoma. Am J Clin Oncol 25(5):468–473. https://doi.org/10.1097/00000421-200210000-00009
doi: 10.1097/00000421-200210000-00009
pubmed: 12393986
Kleer CG, Giordano TJ, Braun T, Oberman HA (2001) Pathologic, immunohistochemical, and molecular features of benign and malignant phyllodes tumors of the breast. Mod Pathol 14(3):185–190. https://doi.org/10.1038/modpathol.3880282
doi: 10.1038/modpathol.3880282
pubmed: 11266524
Ganesh K, Wu C, O’Rourke KP, Szeglin BC, Zheng Y, Sauvé CG et al (2019) A rectal cancer organoid platform to study individual responses to chemoradiation. Nat Med 25(10):1607–1614. https://doi.org/10.1038/s41591-019-0584-2
doi: 10.1038/s41591-019-0584-2
pubmed: 31591597
pmcid: 7385919
Yao Y, Xu X, Yang L, Zhu J, Wan J, Shen L (2020) Patient-derived organoids predict chemoradiation responses of locally advanced rectal cancer. Cell Stem Cell 26(1):17–26. https://doi.org/10.1016/j.stem.2019.10.010
doi: 10.1016/j.stem.2019.10.010
pubmed: 31761724
Takebe T, Sekine K, Enomura M, Koike H, Kimura M, Ogaeri T et al (2013) Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499(7459):481–484. https://doi.org/10.1038/nature12271
doi: 10.1038/nature12271
pubmed: 23823721
Takebe T, Enomura M, Yoshizawa E, Kimura M, Koike H, Ueno Y et al (2015) Vascularized and complex organ buds from diverse tissues via mesenchymal cell-driven condensation. Cell Stem Cell 16(5):556–565. https://doi.org/10.1016/j.stem.2015.03.004
doi: 10.1016/j.stem.2015.03.004
pubmed: 25891906
Bar-Ephraim YE, Kretzschmar K, Clevers H (2020) Organoids in immunological research. Nat Rev Immunol 20(5):279–293. https://doi.org/10.1038/s41577-019-0248-y
doi: 10.1038/s41577-019-0248-y
pubmed: 31853049
Dijkstra KK, Cattaneo CM, Weeber F, Chalabi M, van de Haar J, Fanchi LF et al (2018) Generation of tumor-reactive T cells by co-culture of peripheral blood lymphocytes and tumor organoids. Cell 174(6):1586–1598. https://doi.org/10.1016/j.cell.2018.07.009
doi: 10.1016/j.cell.2018.07.009
pubmed: 30100188
pmcid: 6558289
Schnalzger TE, de Groot MH, Zhang C, Mosa MH, Michels BE, Röder J et al (2019) 3D model for CAR-mediated cytotoxicity using patient-derived colorectal cancer organoids. EMBO J 38(12):100928. https://doi.org/10.15252/embj.2018100928
doi: 10.15252/embj.2018100928
Neal JT, Li X, Zhu J, Giangarra V, Grzeskowiak CL, Ju J et al (2018) Organoid modeling of the tumor immune microenvironment. Cell 175(7):1972-1988.e16. https://doi.org/10.1016/j.cell.2018.11.021
doi: 10.1016/j.cell.2018.11.021
pubmed: 30550791
pmcid: 6656687
Roulis M, Kaklamanos A, Schernthanner M, Bielecki P, Zhao J, Kaffe E et al (2020) Paracrine orchestration of intestinal tumorigenesis by a mesenchymal niche. Nature 580(7804):524–529. https://doi.org/10.1038/s41586-020-2166-3
doi: 10.1038/s41586-020-2166-3
pubmed: 32322056
pmcid: 7490650
Corrò C, Novellasdemunt L, Li VSW (2020) A brief history of organoids. Am J Physiol Cell Physiol 319(1):151–165. https://doi.org/10.1152/ajpcell.00120.2020
doi: 10.1152/ajpcell.00120.2020
Kalbasi A, Ribas A (2020) Tumour-intrinsic resistance to immune checkpoint blockade. Nat Rev Immunol 20(1):25–39. https://doi.org/10.1038/s41577-019-0218-4
doi: 10.1038/s41577-019-0218-4
pubmed: 31570880
Wei SC, Duffy CR, Allison JP (2018) Fundamental mechanisms of immune checkpoint blockade therapy. Cancer Discov 8(9):1069–1086. https://doi.org/10.1158/2159-8290.CD-18-0367
doi: 10.1158/2159-8290.CD-18-0367
pubmed: 30115704
Junttila MR, de Sauvage FJ (2013) Influence of tumour micro-environment heterogeneity on therapeutic response. Nature 501(7467):346–354. https://doi.org/10.1038/nature12626
doi: 10.1038/nature12626
pubmed: 24048067
Klemm F, Joyce JA (2015) Microenvironmental regulation of therapeutic response in cancer. Trends Cell Biol 25(4):198–213. https://doi.org/10.1016/j.tcb.2014.11.006
doi: 10.1016/j.tcb.2014.11.006
pubmed: 25540894
Palucka AK, Coussens LM (2016) The basis of oncoimmunology. Cell 164(6):1233–1247. https://doi.org/10.1016/j.cell.2016.01.049
doi: 10.1016/j.cell.2016.01.049
pubmed: 26967289
pmcid: 4788788
Aboulkheyr Es H, Montazeri L, Aref AR, Vosough M, Baharvand H (2018) Personalized cancer medicine: an organoid approach. Trends Biotechnol 36(4):358–371. https://doi.org/10.1016/j.tibtech.2017.12.005
doi: 10.1016/j.tibtech.2017.12.005
pubmed: 29366522