CDK4 phosphorylation status and rational use for combining CDK4/6 and BRAF/MEK inhibition in advanced thyroid carcinomas.

ATC CDK4 Thr172-phosphorylation PDTC biomarkers dabrafenib palbociclib trametinib

Journal

Frontiers in endocrinology
ISSN: 1664-2392
Titre abrégé: Front Endocrinol (Lausanne)
Pays: Switzerland
ID NLM: 101555782

Informations de publication

Date de publication:
2023
Historique:
received: 26 06 2023
accepted: 26 09 2023
medline: 15 11 2023
pubmed: 15 11 2023
entrez: 15 11 2023
Statut: epublish

Résumé

CDK4/6 inhibitors (CDK4/6i) have been established as standard treatment against advanced Estrogen Receptor-positive breast cancers. These drugs are being tested against several cancers, including in combinations with other therapies. We identified the T172-phosphorylation of CDK4 as the step determining its activity, retinoblastoma protein (RB) inactivation, cell cycle commitment and sensitivity to CDK4/6i. Poorly differentiated (PDTC) and anaplastic (ATC) thyroid carcinomas, the latter considered one of the most lethal human malignancies, represent major clinical challenges. Several molecular evidence suggest that CDK4/6i could be considered for treating these advanced thyroid cancers. We analyzed by two-dimensional gel electrophoresis the CDK4 modification profile and the presence of T172-phosphorylated CDK4 in a collection of 98 fresh-frozen tissues and in 21 cell lines. A sub-cohort of samples was characterized by RNA sequencing and immunohistochemistry. Sensitivity to CDK4/6i (palbociclib and abemaciclib) was assessed by BrdU incorporation/viability assays. Treatment of cell lines with CDK4/6i and combination with BRAF/MEK inhibitors (dabrafenib/trametinib) was comprehensively evaluated by western blot, characterization of immunoprecipitated CDK4 and CDK2 complexes and clonogenic assays. CDK4 phosphorylation was detected in all well-differentiated thyroid carcinomas (n=29), 19/20 PDTC, 16/23 ATC and 18/21 thyroid cancer cell lines, including 11 ATC-derived ones. Tumors and cell lines without phosphorylated CDK4 presented very high p16 Our study supports further clinical evaluation of CDK4/6i and their combination with anti-BRAF/MEK therapies as a novel effective treatment against advanced thyroid tumors. Moreover, the complementary use of our 11 genes predictor with p16/KI67 evaluation could represent a prompt tool for recognizing the intrinsically CDK4/6i insensitive patients, who are potentially better candidates to immediate chemotherapy.

Sections du résumé

Background UNASSIGNED
CDK4/6 inhibitors (CDK4/6i) have been established as standard treatment against advanced Estrogen Receptor-positive breast cancers. These drugs are being tested against several cancers, including in combinations with other therapies. We identified the T172-phosphorylation of CDK4 as the step determining its activity, retinoblastoma protein (RB) inactivation, cell cycle commitment and sensitivity to CDK4/6i. Poorly differentiated (PDTC) and anaplastic (ATC) thyroid carcinomas, the latter considered one of the most lethal human malignancies, represent major clinical challenges. Several molecular evidence suggest that CDK4/6i could be considered for treating these advanced thyroid cancers.
Methods UNASSIGNED
We analyzed by two-dimensional gel electrophoresis the CDK4 modification profile and the presence of T172-phosphorylated CDK4 in a collection of 98 fresh-frozen tissues and in 21 cell lines. A sub-cohort of samples was characterized by RNA sequencing and immunohistochemistry. Sensitivity to CDK4/6i (palbociclib and abemaciclib) was assessed by BrdU incorporation/viability assays. Treatment of cell lines with CDK4/6i and combination with BRAF/MEK inhibitors (dabrafenib/trametinib) was comprehensively evaluated by western blot, characterization of immunoprecipitated CDK4 and CDK2 complexes and clonogenic assays.
Results UNASSIGNED
CDK4 phosphorylation was detected in all well-differentiated thyroid carcinomas (n=29), 19/20 PDTC, 16/23 ATC and 18/21 thyroid cancer cell lines, including 11 ATC-derived ones. Tumors and cell lines without phosphorylated CDK4 presented very high p16
Conclusion UNASSIGNED
Our study supports further clinical evaluation of CDK4/6i and their combination with anti-BRAF/MEK therapies as a novel effective treatment against advanced thyroid tumors. Moreover, the complementary use of our 11 genes predictor with p16/KI67 evaluation could represent a prompt tool for recognizing the intrinsically CDK4/6i insensitive patients, who are potentially better candidates to immediate chemotherapy.

Identifiants

pubmed: 37964967
doi: 10.3389/fendo.2023.1247542
pmc: PMC10641312
doi:

Banques de données

figshare
['10.6084/m9.figshare.24278626']

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1247542

Informations de copyright

Copyright © 2023 Pita, Raspé, Coulonval, Decaussin-Petrucci, Tarabichi, Dom, Libert, Craciun, Andry, Wicquart, Leteurtre, Trésallet, Marlow, Copland, Durante, Maenhaut, Cavaco, Dumont, Costante and Roger.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

Oncogene. 2008 Mar 6;27(11):1554-61
pubmed: 17873908
J Clin Oncol. 2017 Sep 1;35(25):2875-2884
pubmed: 28580882
Cancer Cell. 2018 Jul 9;34(1):9-20
pubmed: 29731395
PLoS Genet. 2016 Aug 05;12(8):e1006239
pubmed: 27494611
Pathol Res Pract. 2003;199(6):399-404
pubmed: 12924440
Cell. 2014 Oct 23;159(3):676-90
pubmed: 25417114
Cancer Cell. 2010 Jul 13;18(1):63-73
pubmed: 20609353
Mol Cell Biol. 2006 Jul;26(13):5070-85
pubmed: 16782892
Tumour Biol. 2016 Mar;37(3):3359-64
pubmed: 26446458
Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4171-6
pubmed: 19237555
Clin Cancer Res. 2018 Jul 1;24(13):3059-3068
pubmed: 29615459
Endocr Pathol. 2022 Mar;33(1):27-63
pubmed: 35288841
Mod Pathol. 2021 Jan;34(1):32-41
pubmed: 32719445
Cell Rep. 2021 Apr 6;35(1):108944
pubmed: 33826903
Endocr Relat Cancer. 2011 Dec 01;18(6):743-57
pubmed: 21937739
J Clin Invest. 2016 Mar 1;126(3):1052-66
pubmed: 26878173
Science. 2022 Jan 14;375(6577):eabc1495
pubmed: 35025636
Science. 2018 Dec 21;362(6421):1416-1422
pubmed: 30573629
Thyroid. 2019 Aug;29(8):1036-1043
pubmed: 31319771
Thyroid. 2000 Sep;10(9):741-6
pubmed: 11041450
Oncogene. 2020 Jul;39(29):5165-5176
pubmed: 32541838
Eur J Endocrinol. 2023 Jan 10;188(1):
pubmed: 36651156
Hum Mol Genet. 2015 Apr 15;24(8):2318-29
pubmed: 25576899
Thyroid. 2018 Jul;28(7):945-951
pubmed: 29742974
N Engl J Med. 2016 Nov 3;375(18):1738-1748
pubmed: 27717303
Br J Cancer. 2006 Dec 18;95(12):1670-7
pubmed: 17117177
Oncotarget. 2015 Dec 15;6(40):42445-67
pubmed: 26636651
Oncotarget. 2015 Oct 27;6(33):34629-48
pubmed: 26431489
Cancer Med. 2021 Sep;10(17):5748-5756
pubmed: 34405547
Expert Rev Anticancer Ther. 2019 Jul;19(7):569-587
pubmed: 31219365
Oncotarget. 2018 Jul 24;9(57):30940-30941
pubmed: 30123416
Nat Commun. 2022 Sep 7;13(1):5258
pubmed: 36071033
Mol Cell Biol. 2009 Nov;29(21):5657-70
pubmed: 19720745
Lancet Oncol. 2012 Aug;13(8):773-81
pubmed: 22805291
J Biol Chem. 2003 Jul 18;278(29):26533-40
pubmed: 12730225
J Clin Endocrinol Metab. 2010 Dec;95(12):5338-47
pubmed: 20810568
Eur Thyroid J. 2022 Dec 22;12(1):
pubmed: 36377723
Mol Endocrinol. 2006 Dec;20(12):3279-92
pubmed: 16916940
Mol Cell Biol. 2000 Aug;20(15):5690-9
pubmed: 10891505
Curr Opin Oncol. 2023 Jan 1;35(1):1-9
pubmed: 36398690
Endocr Relat Cancer. 2009 Mar;16(1):17-44
pubmed: 18987168
Cell Div. 2006 Nov 08;1:25
pubmed: 17092340
Cancer Biol Ther. 2012 Jul;13(9):776-81
pubmed: 22688732
Mol Biol Cell. 2008 Nov;19(11):4814-25
pubmed: 18799615
Cancer Res. 2007 Nov 1;67(21):10148-58
pubmed: 17981789
Genes Dev. 1999 Jun 15;13(12):1501-12
pubmed: 10385618
Endocr Pathol. 2008 Fall;19(3):184-9
pubmed: 18766473
Ann Surg Oncol. 2007 May;14(5):1772-9
pubmed: 17195959
Exp Cell Res. 2003 Nov 15;291(1):135-49
pubmed: 14597415
J Clin Invest. 2007 Jan;117(1):218-28
pubmed: 17160137
Clin Cancer Res. 2019 May 15;25(10):3141-3151
pubmed: 30737244
Cancer. 2023 Apr 1;129(7):1051-1063
pubmed: 36760031
Mol Cell Biol. 2009 Aug;29(15):4188-200
pubmed: 19487459
Ann Surg Oncol. 2008 Oct;15(10):2811-26
pubmed: 18612701
Sci Rep. 2018 Feb 13;8(1):2918
pubmed: 29440769
Oncotarget. 2017 Dec 23;9(13):10905-10919
pubmed: 29541385
J Oncol. 2011;2011:542358
pubmed: 21772843
J Endocrinol Invest. 2019 May;42(5):527-540
pubmed: 30191474
Eur Thyroid J. 2019 Oct;8(5):227-245
pubmed: 31768334
Clin Cancer Res. 2014 Sep 1;20(17):4449-58
pubmed: 24958809
Sci Rep. 2017 Dec 4;7(1):16878
pubmed: 29203879
Adv Enzyme Regul. 1984;22:27-55
pubmed: 6382953
Cell. 2020 Apr 16;181(2):424-441.e21
pubmed: 32234521
Cancer Discov. 2021 Oct;11(10):2582-2601
pubmed: 33990344
J Cell Biol. 1992 Apr;117(2):383-93
pubmed: 1313816
Nat Commun. 2019 Jun 24;10(1):2764
pubmed: 31235699
Trends Cancer. 2017 Jan;3(1):39-55
pubmed: 28303264
Cancer Discov. 2016 Jul;6(7):740-53
pubmed: 27217383
Mol Cell Biol. 1994 Apr;14(4):2713-21
pubmed: 8139570
Mol Biol Cell. 2011 Nov;22(21):3971-85
pubmed: 21900495
Thyroid. 2018 Jan;28(1):79-87
pubmed: 29161986
J Cell Sci. 2012 Sep 15;125(Pt 18):4253-63
pubmed: 22718346
Int J Cancer. 1998 Jun 10;76(6):806-11
pubmed: 9626345
Curr Opin Oncol. 2021 Jan;33(1):3-8
pubmed: 33060402
Endocr Relat Cancer. 2019 Jan 1;26(4):425-436
pubmed: 30699064
J Clin Endocrinol Metab. 2006 Aug;91(8):2892-9
pubmed: 16684830
Oncogene. 2010 Jul 15;29(28):4018-32
pubmed: 20473330
Eur J Cancer. 2007 Jan;43(1):194-201
pubmed: 17046239
J Clin Endocrinol Metab. 2008 Nov;93(11):4331-41
pubmed: 18713817
Cancer Discov. 2018 Feb;8(2):216-233
pubmed: 29101163
Cell Cycle. 2014;13(18):2879-88
pubmed: 25486476
Biostatistics. 2004 Oct;5(4):557-72
pubmed: 15475419
Endocr Relat Cancer. 2003 Jun;10(2):179-86
pubmed: 12790780
PLoS Genet. 2013 May;9(5):e1003546
pubmed: 23737759
J Biol Chem. 2003 Dec 26;278(52):52052-60
pubmed: 14551212
Cell Cycle. 2006 Jan;5(1):61-70
pubmed: 16294008
Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4166-70
pubmed: 19237565
Am J Surg Pathol. 2007 Aug;31(8):1256-64
pubmed: 17667551
J Clin Oncol. 2018 Jan 1;36(1):7-13
pubmed: 29072975
N Engl J Med. 2016 Nov 17;375(20):1925-1936
pubmed: 27959613
Br J Clin Pharmacol. 2014 Sep;78(3):524-32
pubmed: 24606567
Nat Biotechnol. 2011 Jan;29(1):24-6
pubmed: 21221095
Cell Rep. 2018 Mar 13;22(11):2978-2994
pubmed: 29539425
J Clin Endocrinol Metab. 2014 Mar;99(3):E497-507
pubmed: 24423316
Nat Med. 2012 Oct;18(10):1503-10
pubmed: 22983396
Cell Cycle. 2011 Aug 1;10(15):2497-503
pubmed: 21775818
Pharmacol Rev. 2006 Sep;58(3):621-81
pubmed: 16968952
J Immunother Cancer. 2018 Jul 11;6(1):68
pubmed: 29996921
Cell Cycle. 2007 Nov 15;6(22):2817-25
pubmed: 18032931
Cell Cycle. 2010 Feb 15;9(4):689-99
pubmed: 20107323
Nat Rev Endocrinol. 2017 Nov;13(11):644-660
pubmed: 28707679
Cancer Res. 2009 Jun 1;69(11):4577-81
pubmed: 19458076
Oncogene. 2017 Jul 27;36(30):4349-4361
pubmed: 28368408
Br J Cancer. 2009 Nov 17;101(10):1782-91
pubmed: 19809427
Thyroid. 2016 Jan;26(1):1-133
pubmed: 26462967
Cancer Lett. 2018 Mar 28;417:131-140
pubmed: 29306020
EMBO Mol Med. 2017 Aug;9(8):1052-1066
pubmed: 28566333
Mol Cell Endocrinol. 2018 Jan 15;460:24-35
pubmed: 28652169
Thyroid. 2021 Mar;31(3):337-386
pubmed: 33728999
World J Surg. 2007 May;31(5):934-45
pubmed: 17431717
Nat Rev Cancer. 2022 Jun;22(6):356-372
pubmed: 35304604
Endocr Relat Cancer. 2008 Sep;15(3):801-15
pubmed: 18753363
Ann Oncol. 2022 Jul;33(7):674-684
pubmed: 35491008
Oncogene. 2019 May;38(18):3355-3370
pubmed: 30696953
Nat Rev Mol Cell Biol. 2006 Sep;7(9):667-77
pubmed: 16921403
Nat Rev Cancer. 2011 Jul 07;11(8):558-72
pubmed: 21734724
PLoS One. 2012;7(10):e37807
pubmed: 23115614
Am J Transl Res. 2019 Sep 15;11(9):5888-5896
pubmed: 31632557
Mol Oncol. 2022 Nov 30;:
pubmed: 36453028
Sci Transl Med. 2017 Apr 26;9(387):
pubmed: 28446688
Cell Cycle. 2022 Jan;21(1):12-32
pubmed: 34913830

Auteurs

Jaime M Pita (JM)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Eric Raspé (E)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Katia Coulonval (K)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Myriam Decaussin-Petrucci (M)

Department of Pathology, Lyon Sud Hospital, Claude Bernard Lyon 1 University, Lyon, France.

Maxime Tarabichi (M)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Geneviève Dom (G)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Frederick Libert (F)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.
BRIGHTCore, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Ligia Craciun (L)

Tumor Bank of the Institut Jules Bordet Comprehensive Cancer Center - Hôpital Universitaire de Bruxelles, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Guy Andry (G)

Department of Head & Neck and Thoracic Surgery, Institut Jules Bordet Comprehensive Cancer Center - Hôpital Universitaire de Bruxelles, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Laurence Wicquart (L)

Tumorothèque du Groupement de Coopération Sanitaire-Centre Régional de Référence en Cancérologie (C2RC) de Lille, Lille, France.

Emmanuelle Leteurtre (E)

Department of Pathology, Univ. Lille, Centre National de la Recherche Scientifique (CNRS), Inserm, Centre Hospitalo-Universitaire (CHU) Lille, UMR9020-U1277-CANTHER-Cancer Heterogeneity, Plasticity and Resistance to Therapies, Lille, France.

Christophe Trésallet (C)

Department of General and Endocrine Surgery - Pitié-Salpêtrière Hospital, Sorbonne University, Assistance Publique des Hôpitaux de Paris, Paris, France.
Department of Digestive, Bariatric and Endocrine Surgery - Avicenne University Hospital, Paris Nord - Sorbonne University, Assistance Publique des Hôpitaux de Paris, Paris, France.

Laura A Marlow (LA)

Department of Cancer Biology, Mayo Clinic, Jacksonville, FL, United States.

John A Copland (JA)

Department of Cancer Biology, Mayo Clinic, Jacksonville, FL, United States.

Cosimo Durante (C)

Department of Translational and Precision Medicine, Sapienza University of Rome, Rome, Italy.

Carine Maenhaut (C)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Branca M Cavaco (BM)

Molecular Endocrinology Group, Unidade de Investigação em Patobiologia Molecular (UIPM), Instituto Português de Oncologia de Lisboa Francisco Gentil (IPOLFG), Lisbon, Portugal.

Jacques E Dumont (JE)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Giuseppe Costante (G)

Departments of Endocrinology and Medical Oncology, Institut Jules Bordet Comprehensive Cancer Center - Hôpital Universitaire de Bruxelles, Université Libre de Bruxelles (ULB), Brussels, Belgium.

Pierre P Roger (PP)

Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire (IRIBHM) and Université Libre de Bruxelles (ULB)-Cancer Research Center (U-CRC), Université Libre de Bruxelles (ULB), Brussels, Belgium.

Classifications MeSH