Establishment and characterization of patient-derived xenografts as paraclinical models for head and neck cancer.


Journal

BMC cancer
ISSN: 1471-2407
Titre abrégé: BMC Cancer
Pays: England
ID NLM: 100967800

Informations de publication

Date de publication:
15 Apr 2020
Historique:
received: 17 12 2019
accepted: 25 03 2020
entrez: 16 4 2020
pubmed: 16 4 2020
medline: 19 12 2020
Statut: epublish

Résumé

We investigated whether head and neck squamous cell carcinoma (HNSCC) patient-derived xenografts (PDXs) reaffirm patient responses to anti-cancer therapeutics. Tumors from HNSCC patients were transplanted into immunodeficient mice and propagated via subsequent implantation. We evaluated established PDXs by histology, genomic profiling, and in vivo anti-cancer efficacy testing to confirm them as the authentic in vivo platform. From 62 HNSCCs, 15 (24%) PDXs were established. The primary cancer types were tongue (8), oropharynx (3), hypopharynx (1), ethmoid sinus cancer (1), supraglottic cancer (1), and parotid gland (1); six PDXs (40%) were established from biopsy specimens from advanced HNSCC. PDXs mostly retained donor characteristics and remained stable across passages. PIK3CA (H1047R), HRAS (G12D), and TP53 mutations (H193R, I195T, R248W, R273H, E298X) and EGFR, CCND1, MYC, and PIK3CA amplifications were identified. Using the acquisition method, biopsy showed a significantly higher engraftment rate when compared with that of surgical resection (100% [6/6] vs. 16.1% [9/56], P < 0.001). Specimens obtained from metastatic sites showed a significantly higher engraftment rate than did those from primary sites (100% [9/9] vs. 11.3% [6/53], P < 0.001). Three PDX models from HPV-positive tumors were established, as compared to 12 from HPV-negative (15.8% [3/19] and 27.9% [12/43] respectively, P = 0.311), suggesting that HPV positivity tends to show a low engraftment rate. Drug responses in PDX recapitulated the clinical responses of the matching patients with pan-HER inhibitors and pan-PI3K inhibitor. Genetically and clinically annotated HNSCC PDXs could be useful preclinical tools for evaluating biomarkers, therapeutic targets, and new drug discovery.

Sections du résumé

BACKGROUND BACKGROUND
We investigated whether head and neck squamous cell carcinoma (HNSCC) patient-derived xenografts (PDXs) reaffirm patient responses to anti-cancer therapeutics.
METHODS METHODS
Tumors from HNSCC patients were transplanted into immunodeficient mice and propagated via subsequent implantation. We evaluated established PDXs by histology, genomic profiling, and in vivo anti-cancer efficacy testing to confirm them as the authentic in vivo platform.
RESULTS RESULTS
From 62 HNSCCs, 15 (24%) PDXs were established. The primary cancer types were tongue (8), oropharynx (3), hypopharynx (1), ethmoid sinus cancer (1), supraglottic cancer (1), and parotid gland (1); six PDXs (40%) were established from biopsy specimens from advanced HNSCC. PDXs mostly retained donor characteristics and remained stable across passages. PIK3CA (H1047R), HRAS (G12D), and TP53 mutations (H193R, I195T, R248W, R273H, E298X) and EGFR, CCND1, MYC, and PIK3CA amplifications were identified. Using the acquisition method, biopsy showed a significantly higher engraftment rate when compared with that of surgical resection (100% [6/6] vs. 16.1% [9/56], P < 0.001). Specimens obtained from metastatic sites showed a significantly higher engraftment rate than did those from primary sites (100% [9/9] vs. 11.3% [6/53], P < 0.001). Three PDX models from HPV-positive tumors were established, as compared to 12 from HPV-negative (15.8% [3/19] and 27.9% [12/43] respectively, P = 0.311), suggesting that HPV positivity tends to show a low engraftment rate. Drug responses in PDX recapitulated the clinical responses of the matching patients with pan-HER inhibitors and pan-PI3K inhibitor.
CONCLUSIONS CONCLUSIONS
Genetically and clinically annotated HNSCC PDXs could be useful preclinical tools for evaluating biomarkers, therapeutic targets, and new drug discovery.

Identifiants

pubmed: 32293356
doi: 10.1186/s12885-020-06786-5
pii: 10.1186/s12885-020-06786-5
pmc: PMC7160896
doi:

Substances chimiques

Aminopyridines 0
Morpholines 0
NVP-BKM120 0
Afatinib 41UD74L59M
Methotrexate YL5FZ2Y5U1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

316

Subventions

Organisme : Health Promotion Administration, Ministry of Health and Welfare (TW)
ID : HI15C1592
Organisme : Korea Carbon Capture and Sequestration R and D Center (KR)
ID : HI13C2162

Références

Cancer Res. 2013 Aug 1;73(15):4885-97
pubmed: 23737486
Nature. 2015 Jan 29;517(7536):576-82
pubmed: 25631445
Cell Rep. 2013 Sep 26;4(6):1116-30
pubmed: 24055055
Cancer Res Treat. 2019 Jan;51(1):300-312
pubmed: 29747488
Cancer Res. 2013 Jul 15;73(14):4372-82
pubmed: 23856246
Nat Genet. 2017 Jan 31;49(2):170-174
pubmed: 28138153
Cancer Res. 2013 Sep 1;73(17):5315-9
pubmed: 23733750
Nat Rev Cancer. 2006 Oct;6(10):813-23
pubmed: 16990858
PLoS One. 2015 Aug 13;10(8):e0134346
pubmed: 26270481
BMC Genomics. 2014 Dec 23;15:1172
pubmed: 25539684
J Transl Med. 2013 Aug 27;11:198
pubmed: 23981300
Oncogene. 2016 Jun 23;35(25):3217-26
pubmed: 26592450
Lab Invest. 2008 Apr;88(4):342-53
pubmed: 18283272
J Clin Med. 2018 Mar 02;7(3):
pubmed: 29498669
Nature. 2012 Mar 28;483(7391):603-7
pubmed: 22460905
Nat Rev Drug Discov. 2015 Aug;14(8):513-5
pubmed: 26228747
Cancer Immunol Res. 2015 Jan;3(1):12-7
pubmed: 25568068
Nat Biotechnol. 2013 Mar;31(3):213-9
pubmed: 23396013
Cell Rep. 2018 Aug 21;24(8):2167-2178
pubmed: 30134176
Bioinformatics. 2010 Mar 1;26(5):589-95
pubmed: 20080505
Br J Cancer. 1978 Feb;37(2):213-23
pubmed: 629859
N Engl J Med. 2007 May 10;356(19):1944-56
pubmed: 17494927
Int J Cancer. 2015 Jun 15;136(12):2940-8
pubmed: 25404014
Clin Cancer Res. 2013 Feb 15;19(4):855-64
pubmed: 23251001
Cancer Discov. 2014 Sep;4(9):998-1013
pubmed: 25185190
J Clin Oncol. 2008 Feb 1;26(4):612-9
pubmed: 18235120
Anticancer Res. 1986 Sep-Oct;6(5):1165-70
pubmed: 3800324
Clin Cancer Res. 2007 Jul 1;13(13):3989-98
pubmed: 17606733
Br J Cancer. 2001 May 18;84(10):1424-31
pubmed: 11355958
Lancet Oncol. 2017 Mar;18(3):323-335
pubmed: 28131786
Lung Cancer. 2018 Oct;124:168-178
pubmed: 30268457
Cancer. 2005 May 1;103(9):1843-9
pubmed: 15772957
Sci Rep. 2015 Oct 06;5:14495
pubmed: 26440065
N Engl J Med. 2010 Jul 1;363(1):24-35
pubmed: 20530316
Bioinformatics. 2016 Sep 15;32(18):2847-9
pubmed: 27207943
Nat Rev Clin Oncol. 2012 Apr 17;9(6):338-50
pubmed: 22508028
Cancers (Basel). 2019 Jul 06;11(7):
pubmed: 31284584
Cancer. 2008 Nov 15;113(10 Suppl):2901-9
pubmed: 18980273
Clin Cancer Res. 2015 Feb 1;21(3):544-52
pubmed: 25424851
Cancer Res. 2014 Dec 15;74(24):7546-59
pubmed: 25320014
Cancer Discov. 2017 Jun;7(6):586-595
pubmed: 28365644
Laryngoscope. 2017 Dec;127(12):2777-2783
pubmed: 28561270
Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19936-41
pubmed: 18077425
Nat Methods. 2016 Sep 29;13(10):806-7
pubmed: 27684579
Cell Rep. 2018 Oct 30;25(5):1318-1331.e4
pubmed: 30380421
Carcinogenesis. 2004 Jun;25(6):857-64
pubmed: 15033906
Biomedica. 2015 Oct-Dec;35(4):480-95
pubmed: 26844437
PLoS One. 2015 Nov 20;10(11):e0142429
pubmed: 26588841

Auteurs

Han Na Kang (HN)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

Jae-Hwan Kim (JH)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

A-Young Park (AY)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

Jae Woo Choi (JW)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.
Severance Biomedical Science Institute, Yonsei University College of Medicine, Seoul, South Korea.

Sun Min Lim (SM)

Division of Medical Oncology, Department of Internal Medicine, CHA Bundang Medical Center, Seongnam-si, South Korea.

Jinna Kim (J)

Department of Pathology, Yonsei University College of Medicine, Seoul, South Korea.

Eun Joo Shin (EJ)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

Min Hee Hong (MH)

Yonsei Cancer Center, Division of Medical Oncology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea.

Kyoung-Ho Pyo (KH)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.
Severance Biomedical Science Institute, Yonsei University College of Medicine, Seoul, South Korea.

Mi Ran Yun (MR)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

Dong Hwi Kim (DH)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea.

Hanna Lee (H)

Severance Biomedical Science Institute, Yonsei University College of Medicine, Seoul, South Korea.

Sun Och Yoon (SO)

Department of Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, South Korea.

Da Hee Kim (DH)

Department of Otorhinolaryngology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea.

Young Min Park (YM)

Department of Otorhinolaryngology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea.

Hyung Kwon Byeon (HK)

Department of Otolaryngology-Head and Neck Surgery Korea, University College of Medicine, Seoul, South Korea.

Inkyung Jung (I)

Department of Biostatistics and Medical Informatics, Yonsei University College of Medicine, Seoul, South Korea.

Soonmyung Paik (S)

Severance Biomedical Science Institute, Yonsei University College of Medicine, Seoul, South Korea.

Yoon Woo Koh (YW)

Department of Otorhinolaryngology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea. YWKOHENT@yuhs.ac.

Byoung Chul Cho (BC)

JE-UK Institute for Cancer Research, JEUK Co. Ltd., Gumi-City, Kyungbuk, South Korea. cbc1971@yuhs.ac.
Yonsei Cancer Center, Division of Medical Oncology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea. cbc1971@yuhs.ac.

Hye Ryun Kim (HR)

Yonsei Cancer Center, Division of Medical Oncology, Yonsei University College of Medicine, 50 Yonsei-ro, Seodaemun-gu, Seoul, 120-752, South Korea. nobelg@yuhs.ac.

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