Celiac disease-associated Neisseria flavescens decreases mitochondrial respiration in CaCo-2 epithelial cells: Impact of Lactobacillus paracasei CBA L74 on bacterial-induced cellular imbalance.


Journal

Cellular microbiology
ISSN: 1462-5822
Titre abrégé: Cell Microbiol
Pays: India
ID NLM: 100883691

Informations de publication

Date de publication:
08 2019
Historique:
received: 17 11 2018
revised: 10 04 2019
accepted: 22 04 2019
pubmed: 2 5 2019
medline: 29 8 2020
entrez: 2 5 2019
Statut: ppublish

Résumé

We previously identified a Neisseria flavescens strain in the duodenum of celiac disease (CD) patients that induced immune inflammation in ex vivo duodenal mucosal explants and in CaCo-2 cells. We also found that vesicular trafficking was delayed after the CD-immunogenic P31-43 gliadin peptide-entered CaCo-2 cells and that Lactobacillus paracasei CBA L74 (L. paracasei-CBA) supernatant reduced peptide entry. In this study, we evaluated if metabolism and trafficking was altered in CD-N. flavescens-infected CaCo-2 cells and if any alteration could be mitigated by pretreating cells with L. paracasei-CBA supernatant, despite the presence of P31-43. We measured CaCo-2 bioenergetics by an extracellular flux analyser, N. flavescens and P31-43 intracellular trafficking by immunofluorescence, cellular stress by TBARS assay, and ATP by bioluminescence. We found that CD-N. flavescens colocalised more than control N. flavescens with early endocytic vesicles and more escaped autophagy thereby surviving longer in infected cells. P31-43 increased colocalisation of N. flavescens with early vesicles. Mitochondrial respiration was lower (P < .05) in CD-N. flavescens-infected cells versus not-treated CaCo-2 cells, whereas pretreatment with L. paracasei-CBA reduced CD-N. flavescens viability and improved cell bioenergetics and trafficking. In conclusion, CD-N. flavescens induces metabolic imbalance in CaCo-2 cells, and the L. paracasei-CBA probiotic could be used to correct CD-associated dysbiosis.

Identifiants

pubmed: 31042331
doi: 10.1111/cmi.13035
pmc: PMC6618323
doi:

Substances chimiques

Culture Media, Conditioned 0
LAMP2 protein, human 0
Lysosomal-Associated Membrane Protein 2 0
MAP1LC3A protein, human 0
Microtubule-Associated Proteins 0
Peptide Fragments 0
Thiobarbituric Acid Reactive Substances 0
Vesicular Transport Proteins 0
early endosome antigen 1 0
gliadin peptide (31-43) 0
Adenosine Triphosphate 8L70Q75FXE
Gliadin 9007-90-3

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13035

Informations de copyright

© 2019 The Authors Cellular Microbiology Published by John Wiley & Sons Ltd.

Références

Sci Rep. 2015 Dec 10;5:18176
pubmed: 26658723
Biochim Biophys Acta Mol Basis Dis. 2018 Feb;1864(2):554-562
pubmed: 29174139
J Immunol. 2016 Aug 15;197(4):1287-97
pubmed: 27430718
Cell Microbiol. 2019 Aug;21(8):e13035
pubmed: 31042331
Nature. 2013 Jan 17;493(7432):346-55
pubmed: 23325217
Science. 2002 Sep 27;297(5590):2275-9
pubmed: 12351792
Nat Commun. 2018 Feb 28;9(1):863
pubmed: 29491406
Prog Mol Subcell Biol. 2018;57:235-272
pubmed: 30097778
Redox Biol. 2014 Jan 10;2:206-10
pubmed: 24494194
Nature. 2010 Jan 28;463(7280):464-73
pubmed: 20110990
J Pathol. 2018 Apr;244(4):432-444
pubmed: 29327342
BMC Microbiol. 2011 Oct 04;11:219
pubmed: 21970810
Inflamm Bowel Dis. 2012 Apr;18(4):649-56
pubmed: 21826768
Gut. 2007 Apr;56(4):480-8
pubmed: 16891357
Exp Cell Res. 2008 Feb 15;314(4):801-13
pubmed: 18031739
J Med Microbiol. 2007 Dec;56(Pt 12):1669-1674
pubmed: 18033837
Med Microbiol Immunol. 2017 Apr;206(2):83-91
pubmed: 28204873
J Infect Dis. 2019 Jan 1;219(1):133-144
pubmed: 29688440
N Engl J Med. 2011 Sep 8;365(10):927-38
pubmed: 21899453
Int J Food Sci Nutr. 2014 Dec;65(8):953-9
pubmed: 25030417
Cell. 2017 Feb 9;168(4):657-669
pubmed: 28187287
PLoS One. 2014 Feb 10;9(2):e87615
pubmed: 24520333
Gastroenterology. 1992 Jan;102(1):330-54
pubmed: 1727768
Cell Host Microbe. 2014 Apr 9;15(4):403-11
pubmed: 24721569
Cell Microbiol. 2015 Sep;17(9):1365-75
pubmed: 25801707
Mol Nutr Food Res. 2012 Nov;56(11):1697-707
pubmed: 22968973
PLoS One. 2014 Nov 21;9(11):e113932
pubmed: 25415429
Expert Rev Hematol. 2017 Jan;10(1):65-79
pubmed: 27911100
Infect Immun. 2012 Mar;80(3):996-1006
pubmed: 22215736
Br J Nutr. 2015 Oct 28;114(8):1157-67
pubmed: 26428276
PLoS One. 2010 Aug 18;5(8):e12246
pubmed: 20805894
EMBO J. 2011 Oct 04;30(24):4970-85
pubmed: 21971085
Front Microbiol. 2018 Aug 14;9:1835
pubmed: 30154767
Int J Mol Sci. 2014 Nov 07;15(11):20518-37
pubmed: 25387079
Am J Physiol Gastrointest Liver Physiol. 2016 Jul 1;311(1):G40-9
pubmed: 27151946
Front Cell Infect Microbiol. 2013 Nov 19;3:80
pubmed: 24312900
Mol Cell Pediatr. 2016 Dec;3(1):8
pubmed: 26883352
Annu Rev Immunol. 2000;18:53-81
pubmed: 10837052
Sci Rep. 2018 Jul 23;8(1):11047
pubmed: 30038321
Am J Gastroenterol. 2016 Jun;111(6):879-90
pubmed: 27045926
Am J Clin Nutr. 2013 Oct;98(4):1123-35
pubmed: 23966426
Sci Rep. 2018 Jul 17;8(1):10821
pubmed: 30018339

Auteurs

Giuseppe Labruna (G)

IRCCS (Istituto di Ricovero e Cura a Carattere Scientifico) SDN, Naples, Italy.

Merlin Nanayakkara (M)

Dipartimento di Scienze Mediche Traslazionali and European Laboratory for the Investigation of Food Induced Disease (ELFID), Università degli Studi di Napoli Federico II, Naples, Italy.

Chiara Pagliuca (C)

Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Naples, Italy.

Marcella Nunziato (M)

Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Naples, Italy.
CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.

Laura Iaffaldano (L)

CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.

Valeria D'Argenio (V)

Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Naples, Italy.
CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.
Task Force on Microbiome Studies, Università degli Studi di Napoli Federico II and CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.

Roberta Colicchio (R)

Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Naples, Italy.

Andrea L Budelli (AL)

Kraft Heinz Innovation Center, Nijmegen, Netherlands.

Roberto Nigro (R)

Dipartimento di Ingegneria Chimica, dei Materiali e della Produzione Industriale, Università di Napoli Federico II, Naples, Italy.

Paola Salvatore (P)

Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Naples, Italy.

Maria Vittoria Barone (MV)

Dipartimento di Scienze Mediche Traslazionali and European Laboratory for the Investigation of Food Induced Disease (ELFID), Università degli Studi di Napoli Federico II, Naples, Italy.

Lucia Sacchetti (L)

CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.
Task Force on Microbiome Studies, Università degli Studi di Napoli Federico II and CEINGE-Biotecnologie Avanzate SCarl, Naples, Italy.

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