Interaction between Wolbachia pipientis and Leishmania infantum in heartworm infected dogs.
Canine
Dirofilariosis
IFNγ
IL-10
IL-4
IL-6
Immune response
Leishmaniosis
TNFα
Wolbachia
Journal
Parasites & vectors
ISSN: 1756-3305
Titre abrégé: Parasit Vectors
Pays: England
ID NLM: 101462774
Informations de publication
Date de publication:
27 Feb 2023
27 Feb 2023
Historique:
received:
28
11
2022
accepted:
10
01
2023
entrez:
28
2
2023
pubmed:
1
3
2023
medline:
3
3
2023
Statut:
epublish
Résumé
Wolbachia is a Gram-negative endosymbiont associated with several species of arthropods and filarioid nematodes, including Dirofilaria immitis. This endosymbiont may elicit a Th1 response, which is a component of the immunity against Leishmania infantum. To investigate the interactions between Wolbachia of D. immitis and L. infantum in naturally infected dogs and cytokine circulation, dogs without clinical signs (n = 187) were selected. Dogs were tested for microfilariae (mfs) by Knott, for female antigens of D. immitis by SNAP, and for anti-L. infantum antibodies by IFAT and assigned to four groups. Dogs of group 1 (G1) and 2 (G2) were positive for D. immitis and positive or negative to L. infantum, respectively. Dogs of group 3 (G3) and 4 (G4) were negative to D. immitis and positive or negative to L. infantum, respectively. Wolbachia and L. infantum DNA was quantified by real-time PCR (qPCR) in dog blood samples. A subset of dogs (n = 65) was examined to assess pro- and anti-inflammatory cytokine production using an ELISA test. Of 93 dogs positive to D. immitis with circulating mfs, 85% were positive to Wolbachia, with the highest amount of DNA detected in G1 and the lowest in dogs with low mfs load in G1 and G2. Among dogs positive to L. infantum, 66% from G1 showed low antibody titer, while 48.9% from G3 had the highest antibody titer. Of 37 dogs positive to Wolbachia from G1, 26 (70.3%) had low antibody titers to L. infantum (1:160). Among cytokines, TNFα showed the highest mean concentration in G1 (246.5 pg/ml), IFNγ being the one most represented (64.3%). IL-10 (1809.5 pg/ml) and IL-6 (123.5 pg/ml) showed the highest mean concentration in dogs from G1. A lower percentage of dogs producing IL-4 was observed in all groups examined, with the highest mean concentration (2794 pg/ml) recorded in G2. Results show the association of D. immitis and Wolbachia with the lower antibody titers of L. infantum in co-infected dogs, suggesting the hypothesis that the endosymbiont may affect the development of the patent leishmaniosis. However, due to the limitations associated with the heterogeneity of naturally infected dogs in field conditions, results should be validated by investigation on experimental models.
Sections du résumé
BACKGROUND
BACKGROUND
Wolbachia is a Gram-negative endosymbiont associated with several species of arthropods and filarioid nematodes, including Dirofilaria immitis. This endosymbiont may elicit a Th1 response, which is a component of the immunity against Leishmania infantum.
METHODS
METHODS
To investigate the interactions between Wolbachia of D. immitis and L. infantum in naturally infected dogs and cytokine circulation, dogs without clinical signs (n = 187) were selected. Dogs were tested for microfilariae (mfs) by Knott, for female antigens of D. immitis by SNAP, and for anti-L. infantum antibodies by IFAT and assigned to four groups. Dogs of group 1 (G1) and 2 (G2) were positive for D. immitis and positive or negative to L. infantum, respectively. Dogs of group 3 (G3) and 4 (G4) were negative to D. immitis and positive or negative to L. infantum, respectively. Wolbachia and L. infantum DNA was quantified by real-time PCR (qPCR) in dog blood samples. A subset of dogs (n = 65) was examined to assess pro- and anti-inflammatory cytokine production using an ELISA test.
RESULTS
RESULTS
Of 93 dogs positive to D. immitis with circulating mfs, 85% were positive to Wolbachia, with the highest amount of DNA detected in G1 and the lowest in dogs with low mfs load in G1 and G2. Among dogs positive to L. infantum, 66% from G1 showed low antibody titer, while 48.9% from G3 had the highest antibody titer. Of 37 dogs positive to Wolbachia from G1, 26 (70.3%) had low antibody titers to L. infantum (1:160). Among cytokines, TNFα showed the highest mean concentration in G1 (246.5 pg/ml), IFNγ being the one most represented (64.3%). IL-10 (1809.5 pg/ml) and IL-6 (123.5 pg/ml) showed the highest mean concentration in dogs from G1. A lower percentage of dogs producing IL-4 was observed in all groups examined, with the highest mean concentration (2794 pg/ml) recorded in G2.
CONCLUSION
CONCLUSIONS
Results show the association of D. immitis and Wolbachia with the lower antibody titers of L. infantum in co-infected dogs, suggesting the hypothesis that the endosymbiont may affect the development of the patent leishmaniosis. However, due to the limitations associated with the heterogeneity of naturally infected dogs in field conditions, results should be validated by investigation on experimental models.
Identifiants
pubmed: 36850014
doi: 10.1186/s13071-023-05662-y
pii: 10.1186/s13071-023-05662-y
pmc: PMC9972713
doi:
Substances chimiques
Cytokines
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
77Informations de copyright
© 2023. The Author(s).
Références
Parasit Vectors. 2021 May 7;14(1):245
pubmed: 33962669
J Small Anim Pract. 2013 Apr;54(4):174-8
pubmed: 23425244
Vet Parasitol. 2006 Apr 30;137(3-4):214-21
pubmed: 16473467
Parasitology. 2009 Jul;136(8):823-31
pubmed: 19490725
Vet Parasitol. 2001 Jul 12;98(1-3):215-38
pubmed: 11516587
Infect Immun. 2003 Sep;71(9):5104-14
pubmed: 12933853
Endocr Metab Immune Disord Drug Targets. 2012 Mar;12(1):53-6
pubmed: 22214329
Res Vet Sci. 2020 Jun;130:19-25
pubmed: 32109759
Clin Vaccine Immunol. 2010 Feb;17(2):267-73
pubmed: 20032217
Transbound Emerg Dis. 2022 May;69(3):1274-1280
pubmed: 33787005
Parasit Vectors. 2020 Apr 21;13(1):195
pubmed: 32312297
Parasit Vectors. 2020 Jun 22;13(1):319
pubmed: 32571427
PLoS Negl Trop Dis. 2021 Sep 23;15(9):e0009817
pubmed: 34555036
Infect Immun. 1994 Jan;62(1):229-35
pubmed: 8262632
Vet Sci. 2022 Sep 07;9(9):
pubmed: 36136697
Parasit Vectors. 2020 Apr 15;13(1):193
pubmed: 32293524
Vet Parasitol. 2011 Apr 19;177(1-2):39-49
pubmed: 21163578
Mol Biochem Parasitol. 1995 Nov;74(2):223-7
pubmed: 8719164
Vet Res Commun. 2007 Feb;31(2):161-71
pubmed: 17216316
J Immunol. 2004 Jul 1;173(1):437-45
pubmed: 15210803
Acta Trop. 2022 Aug;232:106513
pubmed: 35598650
Mol Biochem Parasitol. 2009 Aug;166(2):134-41
pubmed: 19450730
Vet Parasitol. 2005 Oct 24;133(2-3):133-6
pubmed: 15885912
Parasit Vectors. 2016 May 10;9(1):170
pubmed: 27160085
Aust Vet J. 1973 Jan;49(1):23-7
pubmed: 4571749
Vet Parasitol. 2008 Dec 10;158(3):191-5
pubmed: 18947926
Vet Parasitol. 2005 Oct 24;133(2-3):137-48
pubmed: 15885913
Vet Parasitol. 2006 Dec 20;142(3-4):271-80
pubmed: 16920264
J Trop Med. 2012;2012:541571
pubmed: 21845197
Vet Immunol Immunopathol. 2005 Jan 10;103(1-2):67-75
pubmed: 15626462
Eur J Immunol. 2006 Jul;36(7):1764-71
pubmed: 16791879
Clin Microbiol Infect. 2013 Feb;19(2):131-40
pubmed: 23398406
Int J Parasitol. 2020 Jul;50(8):555-559
pubmed: 32479831
Parasitol Res. 2020 Apr;119(4):1381-1386
pubmed: 32107620
Proc Biol Sci. 2000 Dec 22;267(1461):2511-6
pubmed: 11197127
Clin Microbiol Infect. 2019 Mar;25(3):290-309
pubmed: 29730224
Front Cell Infect Microbiol. 2021 Feb 18;11:624009
pubmed: 33680991
Vet Immunol Immunopathol. 2007 Jan 15;115(1-2):184-8
pubmed: 17112598
Clin Microbiol Rev. 2012 Jul;25(3):507-44
pubmed: 22763636
Parasit Vectors. 2009 Mar 26;2 Suppl 1:S2
pubmed: 19426441
Front Immunol. 2019 Apr 05;10:670
pubmed: 31024534
J Microbiol Immunol Infect. 2017 Oct;50(5):727-729
pubmed: 27268067
Vet Parasitol. 2003 Nov 3;117(1-2):73-83
pubmed: 14597281
Adv Parasitol. 2005;60:245-84
pubmed: 16230105
Adv Immunol. 2000;74:275-317
pubmed: 10605608
BMC Microbiol. 2012 Jan 18;12 Suppl 1:S11
pubmed: 22375833
J Parasitol. 2000 Apr;86(2):228-32
pubmed: 10780537
Trends Parasitol. 2012 Dec;28(12):531-8
pubmed: 22995719
PLoS One. 2012;7(4):e35349
pubmed: 22558142
Pharmacol Res. 2020 Nov;161:105288
pubmed: 33160070
Mol Immunol. 2002 Dec;39(9):531-6
pubmed: 12431386
Clin Vaccine Immunol. 2009 Mar;16(3):337-43
pubmed: 19129471
J Infect Dis. 2001 May 1;183(9):1421-4
pubmed: 11294678
Parasite. 2010 Jun;17(2):79-89
pubmed: 20597434
Vet Immunol Immunopathol. 2005 Jul 15;106(3-4):303-8
pubmed: 15876457
Trends Immunol. 2007 Sep;28(9):378-84
pubmed: 17689290
Vet Immunol Immunopathol. 2007 Jan 15;115(1-2):189-93
pubmed: 17097150
J Comp Pathol. 2011 Nov;145(4):336-44
pubmed: 21511273
Parasit Vectors. 2008 May 09;1(1):10
pubmed: 18471289