Humans with inherited T cell CD28 deficiency are susceptible to skin papillomaviruses but are otherwise healthy

Béziat, Vivien; Rapaport, Franck; Hu, Jiafen; Titeux, Matthias; Claustres, Mathilde Bonnet des; Bourgey, Mathieu; Griffin, Heather; Bandet, Élise; Cindy, S.; Sherkat, Roya; Rokni‐Zadeh, Hassan; Louis, David M.; Changi‐Ashtiani, Majid; Delmonte, Ottavia M.; Fukushima, Toshiaki; Habib, Tanwir; Guennoun, Andrea; Khan, Taushif; Bender, Noemi; Rahman, Mahbuba; About, Frédégonde; Yang, Rui; Rao, Geetha; Rouzaud, Claire; Li, Jingwei; Shearer, Debra; Balogh, Karla K.; Ali, Fatima; Ata, Manar; Dabiri, Soroosh; Momenilandi, Mana; Nammour, Justine; Alyanakian, Marie Alexandra; Leruez‐Ville, Marianne; Guenat, David; Materna, Marie; Marcot, Léa; Vladikine, Natasha; Soret, Christine; Vahidnezhad, Hassan; Youssefian, Leila; Saeidian, Amir Hossein; Uitto, Jouni; Catherinot, Émilie; Navabi, Shadi Sadat; Zarhrate, Mohammed; Woodley, David T.; Jeljeli, Mohamed; Abraham, Thomas; Belkaya, Serkan; Lorenzo, Lazaro; Rosain, Jérémie; Bayat, Mousa; Lanternier, Fanny; Lortholary, Olivier; Zakavi, Faramarz; Gros, Philippe; Orth, Gérard; Abel, Laurent; Prétet, Jean‐Luc; Fraïtag, Sylvie; Jouanguy, Emmanuelle; Davis, Mark M.; Tangye, Stuart G.; Notarangelo, Luigi D.; Marr, Nico; Waterboer, Tim; Langlais, David; Doorbar, John; Hovnanian, Alain; Christensen, Neil D.; Bossuyt, Xavier; Shahrooei, Mohammad; Casanova, Jean Laurent

doi:10.1016/j.cell.2021.06.004

Cited by 60 publications

(56 citation statements)

References 123 publications

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“…How the preferential usage of different costimulatory signals may elicit functionally specific or compensatory CD8 + T cell activities also remains to be understood. The recent identification of a family with a genetic defect in CD28 demonstrated the surprising finding that affected individuals were generally healthy but for a greatly enhanced sensitivity to human papillomavirus infection, suggesting compensatory functions between costimulatory receptors (Be ´ziat et al, 2021). Further emphasizing the potential interaction among diverse costimulatory and inhibitory pathways are observations from preclinical studies demonstrating that efficacy of anti-CD137, anti-GITR, and anti-CTLA-4 required CD226 for anti-tumor activity (Wang et al, 2018;Weulersse et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Mechanistic convergence of the TIGIT and PD-1 inhibitory pathways necessitates co-blockade to optimize anti-tumor CD8+ T cell responses

Banta¹,

Chitre³

et al. 2022

Immunity

138

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Section: Discussionmentioning

confidence: 99%

Mechanistic convergence of the TIGIT and PD-1 inhibitory pathways necessitates co-blockade to optimize anti-tumor CD8+ T cell responses

Banta¹,

Chitre³

et al. 2022

Immunity

138

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“…RNA was quantified using a nanodrop Spectrophotometer (Nano Drop Technologies; ND-1000, Wilmington, DE, USA) and 0.2 µg RNA was used for the reverse-transcriptase reaction using the SuperScript III RT Kit (Thermo-Fisher Scientific, Waltham, MA, USA). Following reverse transcription, 2 µL cDNA was used in the total 20 µL quantitative PCR (qPCR) SYBR Green reaction (Agilent, Santa Clara, CA, USA) according to the manufacturer’s instructions and as described in our previous studies [ 20 , 35 ].…”

Section: Methodsmentioning

confidence: 99%

Depo Medroxyprogesterone (DMPA) Promotes Papillomavirus Infections but Does Not Accelerate Disease Progression in the Anogenital Tract of a Mouse Model

Brendle

et al. 2022

Viruses

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Contraceptives such as Depo-medroxyprogesterone (DMPA) are used by an estimated 34 million women worldwide. DMPA has been associated with increased risk of several viral infections including Herpes simplex virus-2 (HSV-2) and Human immunodeficiency virus (HIV). In the current study, we used the mouse papillomavirus (MmuPV1) anogenital infection model to test two hypotheses: (1) contraceptives such as DMPA increase the susceptibility of the anogenital tract to viral infection and (2) long-term contraceptive administration induces more advanced disease at the anogenital tract. DMPA treatments of both athymic nude mice and heterozygous NU/J (Foxn1nu/+) but ovariectomized mice led to a significantly increased viral load at the anogenital tract, suggesting that endogenous sex hormones were involved in increased viral susceptibility by DMPA treatment. Consistent with previous reports, DMPA treatment suppressed host anti-viral activities at the lower genital tract. To test the impact of long-term contraceptive treatment on the MmuPV1-infected lower genital tract, we included two other treatments in addition to DMPA: 17β-estradiol and a non-hormone based contraceptive Cilostazol (CLZ, Pletal). Viral infections were monitored monthly up to nine months post infection by qPCR. The infected vaginal and anal tissues were harvested and further examined by histological, virological, and immunological analyses. Surprisingly, we did not detect a significantly higher grade of histology in animals in the long-term DMPA and 17β-estradiol treated groups when compared to the control groups in the athymic mice we tested. Therefore, although DMPA promotes initial papillomavirus infections in the lower genital tract, the chronic administration of DMPA does not promote cancer development in the infected tissues in our mouse model.

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“…Biopsies and tissues were fixed in 10% buffered formalin and embedded in paraffin. Sequential sections were cut for immunohistochemistry (IHC), in situ hybridization (ISH), RNA-ISH, and hematoxylin and eosin (H&E) analyses [ 17 , 25 , 28 ]. A 3913 bp EcoRV/BamH1sub genomic fragment of MmuPV1 was used as an in situ hybridization probe for the detection of MmuPV1 DNA in infected tissues [ 29 ].…”

Section: Methodsmentioning

confidence: 99%

Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues

Brendle

Cladel

et al. 2021

Viruses

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Papillomavirus L1 and L2, the major and minor capsid proteins, play significant roles in viral assembly, entry, and propagation. In the current study, we investigate the impact of L1 and L2 on viral life cycle and tumor growth with a newly established mouse papillomavirus (MmuPV1) infection model. MmuPV1 L1 knockout, L2 knockout, and L1 plus L2 knockout mutant genomes (designated as L1ATGko-4m, L2ATGko, and L1-L2ATGko respectively) were generated. The mutants were examined for their ability to generate lesions in athymic nude mice. Viral activities were examined by qPCR, immunohistochemistry (IHC), in situ hybridization (ISH), and transmission electron microscopy (TEM) analyses. We demonstrated that viral DNA replication and tumor growth occurred at both cutaneous and mucosal sites infected with each of the mutants. Infections involving L1ATGko-4m, L2ATGko, and L1-L2ATGko mutant genomes generally resulted in smaller tumor sizes compared to infection with the wild type. The L1 protein was absent in L1ATGko-4m and L1-L2ATGko mutant-treated tissues, even though viral transcripts and E4 protein expression were robust. Therefore, L1 is not essential for MmuPV1-induced tumor growth, and this finding parallels our previous observations in the rabbit papillomavirus model. Very few viral particles were detected in L2ATGko mutant-infected tissues. Interestingly, the localization of L1 in lesions induced by L2ATGko was primarily cytoplasmic rather than nuclear. The findings support the hypothesis that the L2 gene influences the expression, location, transport, and assembly of the L1 protein in vivo.

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Humans with inherited T cell CD28 deficiency are susceptible to skin papillomaviruses but are otherwise healthy

Cited by 60 publications

References 123 publications

Mechanistic convergence of the TIGIT and PD-1 inhibitory pathways necessitates co-blockade to optimize anti-tumor CD8+ T cell responses

Mechanistic convergence of the TIGIT and PD-1 inhibitory pathways necessitates co-blockade to optimize anti-tumor CD8+ T cell responses

Depo Medroxyprogesterone (DMPA) Promotes Papillomavirus Infections but Does Not Accelerate Disease Progression in the Anogenital Tract of a Mouse Model

Mouse Papillomavirus L1 and L2 Are Dispensable for Viral Infection and Persistence at Both Cutaneous and Mucosal Tissues

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