Autophagy occurs in lymphocytes infiltrating Sjögren's syndrome minor salivary glands and correlates with histological severity of salivary gland lesions.

Atg5 Autophagy LC3B Lymphocytes Minor salivary gland Sjögren’s syndrome

Journal

Arthritis research & therapy
ISSN: 1478-6362
Titre abrégé: Arthritis Res Ther
Pays: England
ID NLM: 101154438

Informations de publication

Date de publication:
13 10 2020
Historique:
received: 28 04 2020
accepted: 11 09 2020
entrez: 14 10 2020
pubmed: 15 10 2020
medline: 22 6 2021
Statut: epublish

Résumé

The organization of minor salivary glands (MSG) infiltrates, in patients with Sjögren's syndrome (SS), associates with disease severity and progression. Aberrant regulation of lymphocyte autophagy is involved in autoimmunity, and in previous work, we provided the first evidence of upregulated autophagy in CD4+ T cells infiltrating SS MSG. The aim of this study was to further explore autophagy in SS infiltrating and circulating lymphocytes and to investigate its role in disease histopathological progression. After collection of 20 SS MSG, the presence of lymphocyte aggregates (foci) and the formation of germinal center (GC)-like structures were observed by H&E and confirmed by immunohistochemistry. The expression of autophagy-related genes, Atg5 and MAP1LC3A, was detected by RT-PCR on microdissected salivary gland tissue and control tonsils. In MSG and tonsils, autophagic lymphocytes were identified by the detection of the autophagosome protein LC3B visualized as LC3 puncta staining by immunofluorescence. Peripheral blood autophagy was assessed by flow cytometry in SS and healthy controls (HC). Real-time PCR demonstrated higher expression in the autophagy genes Atg5 and MAP1LC3A in MSG GCs as compared to both small foci (p = 0.0075, p = 0.0002) and GCs from tonsils (p = 0.0001, p = 0.0037). In MSG, LC3 puncta staining was detectable on both CD3+ and CD20+ lymphocytes; in tonsils, LC3 puncta was almost undetectable on all lymphocytes. Compared to HC (n = 20), flow cytometry did not reveal any increase of autophagy in SS circulating lymphocytes (n = 30). In SS MSG, lymphocytes' autophagy is a feature of infiltrating T and B cells and is associated with histological severity. Interestingly, in MSG aberrant regulation of autophagy is detectable in GC-like structures possibly indicating its involvement in the development and persistence of the autoimmune process within the lesions.

Sections du résumé

BACKGROUNDS
The organization of minor salivary glands (MSG) infiltrates, in patients with Sjögren's syndrome (SS), associates with disease severity and progression. Aberrant regulation of lymphocyte autophagy is involved in autoimmunity, and in previous work, we provided the first evidence of upregulated autophagy in CD4+ T cells infiltrating SS MSG. The aim of this study was to further explore autophagy in SS infiltrating and circulating lymphocytes and to investigate its role in disease histopathological progression.
METHODS
After collection of 20 SS MSG, the presence of lymphocyte aggregates (foci) and the formation of germinal center (GC)-like structures were observed by H&E and confirmed by immunohistochemistry. The expression of autophagy-related genes, Atg5 and MAP1LC3A, was detected by RT-PCR on microdissected salivary gland tissue and control tonsils. In MSG and tonsils, autophagic lymphocytes were identified by the detection of the autophagosome protein LC3B visualized as LC3 puncta staining by immunofluorescence. Peripheral blood autophagy was assessed by flow cytometry in SS and healthy controls (HC).
RESULTS
Real-time PCR demonstrated higher expression in the autophagy genes Atg5 and MAP1LC3A in MSG GCs as compared to both small foci (p = 0.0075, p = 0.0002) and GCs from tonsils (p = 0.0001, p = 0.0037). In MSG, LC3 puncta staining was detectable on both CD3+ and CD20+ lymphocytes; in tonsils, LC3 puncta was almost undetectable on all lymphocytes. Compared to HC (n = 20), flow cytometry did not reveal any increase of autophagy in SS circulating lymphocytes (n = 30).
CONCLUSIONS
In SS MSG, lymphocytes' autophagy is a feature of infiltrating T and B cells and is associated with histological severity. Interestingly, in MSG aberrant regulation of autophagy is detectable in GC-like structures possibly indicating its involvement in the development and persistence of the autoimmune process within the lesions.

Identifiants

pubmed: 33050949
doi: 10.1186/s13075-020-02317-6
pii: 10.1186/s13075-020-02317-6
pmc: PMC7557086
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

238

Références

Front Immunol. 2018 Sep 12;9:1952
pubmed: 30258435
J Autoimmun. 2020 Mar;108:102418
pubmed: 32029330
Methods Mol Biol. 2008;445:77-88
pubmed: 18425443
Arthritis Rheum. 2011 Jul;63(7):2021-30
pubmed: 21480190
Nat Cell Biol. 2018 May;20(5):521-527
pubmed: 29686264
Autophagy. 2016;12(1):1-222
pubmed: 26799652
Arthritis Res Ther. 2017 Jul 25;19(1):178
pubmed: 28743286
Rheumatology (Oxford). 2019 Feb 15;:
pubmed: 30770920
Arthritis Rheumatol. 2019 Jan;71(1):170-171
pubmed: 30178631
J Clin Invest. 2018 Aug 31;128(9):3752-3753
pubmed: 30124470
J Autoimmun. 2019 Nov;104:102335
pubmed: 31540861
J Mol Biol. 2020 Apr 3;432(8):2525-2545
pubmed: 31972172
Sci Rep. 2019 Jul 12;9(1):10147
pubmed: 31300716
J Immunol. 2007 Oct 1;179(7):4929-38
pubmed: 17878393
Front Immunol. 2012 Feb 21;3:22
pubmed: 22566906
Rheumatology (Oxford). 2020 Jan 1;59(1):165-170
pubmed: 31274159
J Biol Chem. 2007 Mar 2;282(9):6763-72
pubmed: 17192262
Nat Rev Rheumatol. 2018 Mar;14(3):133-145
pubmed: 29416129
Ann Rheum Dis. 2019 Feb;78(2):249-260
pubmed: 30472652
J Autoimmun. 2018 Nov;94:16-32
pubmed: 30219390
Cells. 2017 Jun 28;6(3):
pubmed: 28657591
Ann Rheum Dis. 2011 Aug;70(8):1363-8
pubmed: 21715359
Methods. 2017 Jan 1;112:147-156
pubmed: 27263026
J Autoimmun. 2010 Jun;34(4):400-7
pubmed: 19889514
J Autoimmun. 2018 Jun;90:132-145
pubmed: 29486915
Nature. 2011 Jan 20;469(7330):323-35
pubmed: 21248839
Ann Rheum Dis. 2002 Jun;61(6):554-8
pubmed: 12006334
PLoS One. 2015 Sep 17;10(9):e0137675
pubmed: 26378792
Arthritis Res Ther. 2019 Jan 29;21(1):39
pubmed: 30696478
Autophagy. 2008 Apr;4(3):309-14
pubmed: 18188005
FASEB J. 2012 Nov;26(11):4722-32
pubmed: 22835828

Auteurs

Serena Colafrancesco (S)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Marta Vomero (M)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Valentina Iannizzotto (V)

Rheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.

Antonina Minniti (A)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Cristiana Barbati (C)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Francesca Arienzo (F)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Linda Mastromanno (L)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Tania Colasanti (T)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Raffaella Izzo (R)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Saba Nayar (S)

Rheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.

Elena Pipi (E)

Rheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.

Bruna Cerbelli (B)

Dipartimento di Radiologia, Oncologia e Scienze Patologiche, Sapienza University of Rome, Rome, Italy.

Carla Giordano (C)

Dipartimento di Radiologia, Oncologia e Scienze Patologiche, Sapienza University of Rome, Rome, Italy.

Francesco Ciccia (F)

Dipartimento di Medicina di Precisione, Rheumatology Unit, University of Campania "L. Vanvitelli", Naples, Italy.

Fabrizio Conti (F)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Guido Valesini (G)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Francesca Barone (F)

Rheumatology Research Group, Institute of Inflammation and Ageing, University of Birmingham, Birmingham, UK.
National Institute for Health Research (NIHR) Birmingham Biomedical Research Centre, University Hospitals Birmingham NHS Foundation Trust, UK and Sandwell and West Birmingham Trust, Birmingham, UK.

Roberta Priori (R)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy.

Cristiano Alessandri (C)

Dipartimento di Scienze Cliniche Internistiche, Anestesiologiche e Cardiovascolari, Sapienza University of Rome, Rome, Italy. cristiano.alessandri@uniroma1.it.

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