Dormant Tumor Cell Vaccination: A Mathematical Model of Immunological Dormancy in Triple-Negative Breast Cancer.

T lymphocytes breast cancer cancer cell vaccine chemotherapy immune-induced cancer dormancy mathematical model tumor heterogeneity type I IFN

Journal

Cancers
ISSN: 2072-6694
Titre abrégé: Cancers (Basel)
Pays: Switzerland
ID NLM: 101526829

Informations de publication

Date de publication:
11 Jan 2021
Historique:
received: 22 12 2020
accepted: 07 01 2021
entrez: 14 1 2021
pubmed: 15 1 2021
medline: 15 1 2021
Statut: epublish

Résumé

Triple-negative breast cancer (TNBC) is a molecular subtype of breast malignancy with a poor clinical prognosis. There is growing evidence that some chemotherapeutic agents induce an adaptive anti-tumor immune response. This reaction has been proposed to maintain the equilibrium phase of the immunoediting process and to control tumor growth by immunological cancer dormancy. We recently reported a model of immunological breast cancer dormancy based on the murine 4T1 TNBC model. Treatment of 4T1 cells in vitro with high-dose chemotherapy activated the type I interferon (type I IFN) signaling pathway, causing a switch from immunosuppressive to cytotoxic T lymphocyte-dependent immune response in vivo, resulting in sustained dormancy. Here, we developed a deterministic mathematical model based on the assumption that two cell subpopulations exist within the treated tumor: one population with high type I IFN signaling and immunogenicity and lower growth rate; the other population with low type I IFN signaling and immunogenicity and higher growth rate. The model reproduced cancer dormancy, elimination, and immune-escape in agreement with our previously reported experimental data. It predicted that the injection of dormant tumor cells with active type I IFN signaling results in complete growth control of the aggressive parental cancer cells injected at a later time point, but also of an already established aggressive tumor. Taken together, our results indicate that a dormant cell population can suppress the growth of an aggressive counterpart by eliciting a cytotoxic T lymphocyte-dependent immune response.

Identifiants

pubmed: 33440806
pii: cancers13020245
doi: 10.3390/cancers13020245
pmc: PMC7827392
pii:
doi:

Types de publication

Journal Article

Langues

eng

Références

Br J Cancer. 2010 Oct 12;103(8):1139-43
pubmed: 20877357
Cancer Immunol Immunother. 2017 Feb;66(2):259-271
pubmed: 28040849
Nat Rev Dis Primers. 2019 Sep 23;5(1):66
pubmed: 31548545
Cell Rep. 2015 May 19;11(7):1018-30
pubmed: 25959818
Nat Med. 2014 Nov;20(11):1301-9
pubmed: 25344738
Science. 2011 Mar 25;331(6024):1565-70
pubmed: 21436444
Nat Rev Cancer. 2007 Nov;7(11):834-46
pubmed: 17957189
Breast Cancer Res. 2007;9(3):208
pubmed: 17561992
Nat Med. 2012 Aug;18(8):1224-31
pubmed: 22820642
Breast Cancer Res Treat. 2010 Jul;122(2):359-69
pubmed: 19826947
Cells. 2019 Aug 22;8(9):
pubmed: 31443516
J Immunol. 2004 Jan 15;172(2):864-70
pubmed: 14707057
PLoS One. 2016 Nov 7;11(11):e0165817
pubmed: 27820870
Surg Oncol Clin N Am. 2018 Jan;27(1):95-120
pubmed: 29132568
J Theor Biol. 2015 Sep 7;380:463-72
pubmed: 26116366
Nat Rev Cancer. 2017 Oct;17(10):605-619
pubmed: 28912577
Nat Immunol. 2002 Nov;3(11):991-8
pubmed: 12407406
Math Biosci. 2018 Oct;304:48-61
pubmed: 30055212
J Cell Mol Med. 2019 Aug;23(8):4854-4865
pubmed: 31210425
Front Oncol. 2018 Aug 21;8:322
pubmed: 30186768
Nat Immunol. 2005 Jul;6(7):722-9
pubmed: 15951814
Nature. 2001 Sep 13;413(6852):165-71
pubmed: 11557981
Br J Cancer. 2016 Jan 19;114(2):177-87
pubmed: 26695443
Curr Protoc Immunol. 2001 May;Chapter 20:Unit 20.2
pubmed: 18432775
BMC Med. 2017 Jul 18;15(1):133
pubmed: 28716075
Front Immunol. 2018 Aug 15;9:1894
pubmed: 30158936
Bull Math Biol. 1994 Mar;56(2):295-321
pubmed: 8186756
Eur J Immunol. 2015 Apr;45(4):999-1009
pubmed: 25545618
Nat Rev Immunol. 2006 Nov;6(11):836-48
pubmed: 17063185
Cancer Immunol Res. 2015 May;3(5):436-43
pubmed: 25941355
Ann Oncol. 2015 Aug;26(8):1698-704
pubmed: 25995301
PLoS Comput Biol. 2014 Aug 28;10(8):e1003800
pubmed: 25167199
Cold Spring Harb Perspect Med. 2018 Mar 1;8(3):
pubmed: 28710258
Cancer Res. 2013 Jun 15;73(12):3534-44
pubmed: 23536560
Mol Cell. 2015 Nov 19;60(4):537-46
pubmed: 26590713
Cancer Biol Med. 2015 Jun;12(2):106-16
pubmed: 26175926
Cancer Immunol Immunother. 2011 Mar;60(3):319-26
pubmed: 21267721
Clin Cancer Res. 2011 Aug 1;17(15):4987-95
pubmed: 21690573
Nat Rev Immunol. 2015 Jul;15(7):405-14
pubmed: 26027717
Cancer Treat Rev. 2018 Feb;63:40-47
pubmed: 29207310
Cancer Res. 2005 Sep 1;65(17):7950-8
pubmed: 16140967
Oncogene. 2019 Apr;38(15):2814-2829
pubmed: 30546090
Math Biosci. 2001 May;171(1):59-82
pubmed: 11325384
J Natl Cancer Inst. 1993 Apr 7;85(7):546-53
pubmed: 8455201
Adv Exp Med Biol. 2013;734:201-34
pubmed: 23143981
Ann Oncol. 2009 Dec;20(12):1913-27
pubmed: 19901010
Cell. 2018 May 3;173(4):879-893.e13
pubmed: 29681456
Cell. 2016 Mar 10;164(6):1233-1247
pubmed: 26967289
Expert Opin Pharmacother. 2015 May;16(7):983-98
pubmed: 25881743
Vaccines (Basel). 2015 Jul 30;3(3):597-619
pubmed: 26350597
BMC Cancer. 2008 Aug 09;8:228
pubmed: 18691423
Med Oncol. 2017 Dec 18;35(1):13
pubmed: 29255938
J Math Biol. 1998 Sep;37(3):235-52
pubmed: 9785481
Ann Oncol. 2010 Oct;21 Suppl 7:vii36-40
pubmed: 20943641
N Engl J Med. 2010 Nov 11;363(20):1938-48
pubmed: 21067385
Br Med J. 1957 Apr 13;1(5023):841-7
pubmed: 13413231
Front Immunol. 2017 Nov 13;8:1544
pubmed: 29181007
Lancet Oncol. 2018 Jan;19(1):40-50
pubmed: 29233559
Ann Oncol. 2012 Aug;23 Suppl 6:vi40-5
pubmed: 23012301
J Innate Immun. 2011;3(4):355-64
pubmed: 21502747
Oncoimmunology. 2012 Nov 1;1(8):1323-1343
pubmed: 23243596
Front Immunol. 2020 Jan 21;10:3038
pubmed: 32038612
Clin Cancer Res. 2011 May 1;17(9):2619-27
pubmed: 21372217
Ann Oncol. 2012 Aug;23 Suppl 6:vi46-51
pubmed: 23012302
Leuk Lymphoma. 2005 Mar;46(3):313-27
pubmed: 15621821
Cancer Discov. 2016 Jun;6(6):630-49
pubmed: 27072748
Bull Math Biol. 2011 Jan;73(1):2-32
pubmed: 20225137
Nat Rev Cancer. 2013 May;13(5):365-76
pubmed: 23535846
J Theor Biol. 2006 Feb 21;238(4):841-62
pubmed: 16153659
Trends Pharmacol Sci. 2015 Dec;36(12):822-846
pubmed: 26538316
Cancer Res. 2019 Nov 15;79(22):5826-5838
pubmed: 31575547
Cancer Gene Ther. 2000 Jul;7(7):1086-99
pubmed: 10917212
J Clin Oncol. 2010 Jun 20;28(18):2966-73
pubmed: 20458051
Ann Oncol. 2016 Feb;27(2):249-56
pubmed: 26598540
Nat Med. 2015 Oct;21(10):1128-38
pubmed: 26444637
Oncoimmunology. 2020 Jan 9;9(1):1703449
pubmed: 32002302
Mol Ther. 2002 Nov;6(5):627-36
pubmed: 12409261
BBA Clin. 2015 Mar 12;3:257-75
pubmed: 26676166
Cancers (Basel). 2020 Apr 08;12(4):
pubmed: 32276534
Cancer Treat Rev. 2013 Dec;39(8):925-34
pubmed: 23562214
J Theor Biol. 2018 Apr 7;442:1-10
pubmed: 29337259
J Clin Oncol. 2009 Dec 1;27(34):5838-47
pubmed: 19884552
Breast J. 2006 Sep-Oct;12(5):475-80
pubmed: 16958969
J Clin Oncol. 2008 Mar 10;26(8):1275-81
pubmed: 18250347
Breast Cancer Res. 2018 Oct 22;20(1):126
pubmed: 30348199
Cancer Res. 2004 Jun 1;64(11):4001-9
pubmed: 15173014
Interface Focus. 2013 Aug 6;3(4):20130010
pubmed: 24511375

Auteurs

Reza Mehdizadeh (R)

Institute of Biochemistry and Biophysics, University of Tehran, Tehran 1417614335, Iran.
Laboratory of Experimental and Translational Oncology, Pathology, Department of Oncology, Microbiology and Immunology, Faculty of Sciences and Medicine, University of Fribourg, 1700 Fribourg, Switzerland.

Seyed Peyman Shariatpanahi (SP)

Institute of Biochemistry and Biophysics, University of Tehran, Tehran 1417614335, Iran.

Bahram Goliaei (B)

Institute of Biochemistry and Biophysics, University of Tehran, Tehran 1417614335, Iran.

Sanam Peyvandi (S)

Laboratory of Experimental and Translational Oncology, Pathology, Department of Oncology, Microbiology and Immunology, Faculty of Sciences and Medicine, University of Fribourg, 1700 Fribourg, Switzerland.

Curzio Rüegg (C)

Laboratory of Experimental and Translational Oncology, Pathology, Department of Oncology, Microbiology and Immunology, Faculty of Sciences and Medicine, University of Fribourg, 1700 Fribourg, Switzerland.

Classifications MeSH