Modelling Chlamydia and HPV co-infection in patient-derived ectocervix organoids reveals distinct cellular reprogramming.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
24 02 2022
Historique:
received: 20 05 2021
accepted: 20 01 2022
entrez: 25 2 2022
pubmed: 26 2 2022
medline: 13 4 2022
Statut: epublish

Résumé

Coinfections with pathogenic microbes continually confront cervical mucosa, yet their implications in pathogenesis remain unclear. Lack of in-vitro models recapitulating cervical epithelium has been a bottleneck to study coinfections. Using patient-derived ectocervical organoids, we systematically modeled individual and coinfection dynamics of Human papillomavirus (HPV)16 E6E7 and Chlamydia, associated with carcinogenesis. The ectocervical stem cells were genetically manipulated to introduce E6E7 oncogenes to mimic HPV16 integration. Organoids from these stem cells develop the characteristics of precancerous lesions while retaining the self-renewal capacity and organize into mature stratified epithelium similar to healthy organoids. HPV16 E6E7 interferes with Chlamydia development and induces persistence. Unique transcriptional and post-translational responses induced by Chlamydia and HPV lead to distinct reprogramming of host cell processes. Strikingly, Chlamydia impedes HPV-induced mechanisms that maintain cellular and genome integrity, including mismatch repair in the stem cells. Together, our study employing organoids demonstrates the hazard of multiple infections and the unique cellular microenvironment they create, potentially contributing to neoplastic progression.

Identifiants

pubmed: 35210413
doi: 10.1038/s41467-022-28569-1
pii: 10.1038/s41467-022-28569-1
pmc: PMC8873204
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1030

Subventions

Organisme : NIEHS NIH HHS
ID : P30 ES000002
Pays : United States
Organisme : NIEHS NIH HHS
ID : U01 ES029520
Pays : United States

Informations de copyright

© 2022. The Author(s).

Références

Int J Cancer. 2000 Jan 1;85(1):35-9
pubmed: 10585579
J Infect. 2011 Sep;63(3):200-6
pubmed: 21704071
Proc Natl Acad Sci U S A. 2014 May 6;111(18):E1823-32
pubmed: 24757057
PLoS Pathog. 2009 Oct;5(10):e1000605
pubmed: 19798429
Viruses. 2017 Aug 18;9(8):
pubmed: 28820495
J Cancer Epidemiol. 2019 Jan 10;2019:9092565
pubmed: 30733803
Nat Commun. 2020 Jun 16;11(1):3132
pubmed: 32546784
Oncogene. 2002 Jan 17;21(3):437-46
pubmed: 11821956
STAR Protoc. 2021 Nov 17;2(4):100969
pubmed: 34841280
Int J Cancer. 2015 Dec 1;137(11):2757-61
pubmed: 26077226
Int J Cancer. 1989 Apr 15;43(4):672-6
pubmed: 2467886
Virology. 2004 May 1;322(2):213-9
pubmed: 15110519
J Mol Med (Berl). 2021 Apr;99(4):531-553
pubmed: 33580825
F1000Res. 2016 Jun 15;5:1384
pubmed: 30101006
Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2490-5
pubmed: 15699322
J Exp Med. 2001 Apr 16;193(8):935-42
pubmed: 11304554
J Virol. 1995 May;69(5):2989-97
pubmed: 7707525
Oncogene. 2002 Jan 10;21(2):165-75
pubmed: 11803460
Trends Biochem Sci. 2004 Aug;29(8):409-17
pubmed: 15362224
Cancer Res Treat. 2005 Dec;37(6):319-24
pubmed: 19956366
Cancers (Basel). 2014 Aug 05;6(3):1597-614
pubmed: 25099886
Nat Rev Cancer. 2013 Aug;13(8):585-95
pubmed: 23842645
Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10516-21
pubmed: 22689991
Viruses. 2017 Aug 18;9(8):
pubmed: 28820433
Obstet Gynecol. 1983 Jul;62(1):117-27
pubmed: 6856213
Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):10002-7
pubmed: 10944189
Mol Microbiol. 2014 Oct;94(1):186-201
pubmed: 25116793
JAMA. 2007 Feb 28;297(8):813-9
pubmed: 17327523
Science. 2004 Feb 6;303(5659):844-8
pubmed: 14704432
Annu Rev Biochem. 2005;74:681-710
pubmed: 15952900
JCO Precis Oncol. 2017;2017:
pubmed: 29850653
J Infect Dis. 2010 Jun 15;201 Suppl 2:S88-95
pubmed: 20470046
Vaccine. 2006 Aug 31;24 Suppl 3:S3/52-61
pubmed: 16950018
J Med Microbiol. 2016 May;65(5):406-413
pubmed: 26944507
Nucleic Acids Res. 2017 Apr 7;45(6):3242-3252
pubmed: 28115629
Bioinformatics. 2010 Oct 1;26(19):2363-7
pubmed: 20688976
Oncol Lett. 2018 Dec;16(6):7035-7047
pubmed: 30546437
Proc Natl Acad Sci U S A. 1983 Jun;80(12):3812-5
pubmed: 6304740
Virology. 2009 Feb 20;384(2):260-5
pubmed: 19135222
J Pathol. 1999 Sep;189(1):12-9
pubmed: 10451482
J Bacteriol. 1988 Mar;170(3):1389-92
pubmed: 3343223
J Pathol. 2007 Aug;212(4):356-67
pubmed: 17573670
J Biol Chem. 2002 Jun 14;277(24):21730-9
pubmed: 11934887
Science. 2017 Jul 28;357(6349):409-413
pubmed: 28596308
Nat Cell Biol. 2021 Feb;23(2):184-197
pubmed: 33462395
Nat Med. 2016 Nov;22(11):1342-1350
pubmed: 27694933
Proc Natl Acad Sci U S A. 2015 Jun 23;112(25):E3255-64
pubmed: 26056290
Nucleic Acids Res. 2019 Sep 26;47(17):9087-9103
pubmed: 31400114
Medicine (Baltimore). 2016 Mar;95(13):e3077
pubmed: 27043670

Auteurs

Stefanie Koster (S)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Rajendra Kumar Gurumurthy (RK)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Naveen Kumar (N)

Chair of Microbiology, University of Würzburg, Würzburg, Germany.

Pon Ganish Prakash (PG)

Chair of Microbiology, University of Würzburg, Würzburg, Germany.

Jayabhuvaneshwari Dhanraj (J)

Chair of Microbiology, University of Würzburg, Würzburg, Germany.

Sofia Bayer (S)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Hilmar Berger (H)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Shilpa Mary Kurian (SM)

Chair of Microbiology, University of Würzburg, Würzburg, Germany.

Marina Drabkina (M)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Hans-Joachim Mollenkopf (HJ)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Christian Goosmann (C)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Volker Brinkmann (V)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.

Zachary Nagel (Z)

Harvard T.H. Chan School of Public Health, Boston, MA, USA.

Mandy Mangler (M)

Klinik für Gynäkologie und Geburtsmedizin, Vivantes Auguste-Viktoria-Klinikum, Berlin, Germany.
Department of Gynecology, Charité University Medicine, Berlin, Germany.

Thomas F Meyer (TF)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany.
Laboratory of Infection Oncology, Institute of Clinical Molecular Biology (IKMB), Christian Albrechts University of Kiel, Kiel, Germany.

Cindrilla Chumduri (C)

Department of Molecular Biology, Max Planck Institute for Infection Biology, Berlin, Germany. cindrilla.chumduri@uni-wuerzburg.de.
Chair of Microbiology, University of Würzburg, Würzburg, Germany. cindrilla.chumduri@uni-wuerzburg.de.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH