Concurrent Ascaris infection modulates host immunity resulting in impaired control of Salmonella infection in pigs

被引:0
作者
Midha, Ankur [1 ]
Oser, Larissa [1 ]
Schlosser-Brandenburg, Josephine [1 ]
Laubschat, Alexandra [1 ]
Mugo, Robert M. [1 ]
Musimbi, Zaneta D. [1 ]
Hoefler, Philipp [1 ]
Kundik, Arkadi [1 ]
Hayani, Rima [1 ]
Adjah, Joshua [1 ]
Groenhagen, Saskia [1 ]
Tieke, Malte [1 ]
Elizalde-Velazquez, Luis E. [1 ]
Kuehl, Anja A. [2 ,3 ,4 ]
Klopfleisch, Robert [5 ]
Tedin, Karsten [6 ]
Rausch, Sebastian [1 ]
Hartmann, Susanne [1 ]
机构
[1] Free Univ Berlin, Inst Immunol, Ctr Infect Med, Dept Vet Med, Berlin, Germany
[2] Charite Univ Med Berlin, Berlin, Germany
[3] Free Univ Berlin, Berlin, Germany
[4] Humboldt Univ, Core Unit Charite, iPATH Berlin, Campus Benjamin Franklin, Berlin, Germany
[5] Free Univ Berlin, Inst Vet Pathol, Dept Vet Med, Berlin, Germany
[6] Free Univ Berlin, Inst Microbiol & Epizoot, Ctr Infect Med, Dept Vet Med, Berlin, Germany
关键词
helminths; Ascaris; Salmonella; coinfection; immunomodulation; pig; ENTERICA SEROVAR TYPHIMURIUM; REGULATORY T-CELLS; LUMBRICOIDES; SUPPRESSION; RESPONSES; MONOCYTE; SWINE; RECRUITMENT; VACCINATION; MECHANISMS;
D O I
10.1128/msphere.00478-24
中图分类号
Q93 [微生物学];
学科分类号
071005 ; 100705 ;
摘要
Ascaris is one of the most widespread helminth infections, leading to chronic morbidity in humans and considerable economic losses in pig farming. In addition, pigs are an important reservoir for the zoonotic salmonellosis, where pigs can serve as asymptomatic carriers. Here, we investigated the impact of an ongoing Ascaris infection on the immune response to Salmonella in pigs. We observed higher bacterial burdens in experimentally coinfected pigs compared to pigs infected with Salmonella alone. The impaired control of Salmonella in the coinfected pigs was associated with repressed interferon gamma responses in the small intestine and with the alternative activation of gut macrophages evident in elevated CD206 expression. Ascaris single and coinfection were associated with a rise of CD4(-)CD8 alpha(+)FoxP3(+) Treg in the lymph nodes draining the small intestine and liver. In addition, macrophages from coinfected pigs showed enhanced susceptibility to Salmonella infection in vitro and the Salmonella-induced monocytosis and tumor necrosis factor alpha production by myeloid cells was repressed in pigs coinfected with Ascaris. Hence, our data indicate that acute Ascaris infection modulates different immune effector functions with important consequences for the control of tissue-invasive coinfecting pathogens.
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页数:19
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共 68 条
  • [1] Modulation of human macrophage activity by Ascaris antigens is dependent on macrophage polarization state
    Almeida, Sara
    Nejsum, Peter
    Williams, Andrew R.
    [J]. IMMUNOBIOLOGY, 2018, 223 (4-5) : 405 - 412
  • [2] Porcine Macrophage Markers and Populations: An Update
    Alvarez, Belen
    Revilla, Concepcion
    Poderoso, Teresa
    Ezquerra, Angel
    Dominguez, Javier
    [J]. CELLS, 2023, 12 (16)
  • [3] Influence of the Intestinal Microbiota on Colonization Resistance to Salmonella and the Shedding Pattern of Naturally Exposed Pigs
    Arguello, Hector
    Estelle, Jordi
    Leonard, Finola C.
    Crispie, Fiona
    Cotter, Paul D.
    O'Sullivan, Orla
    Lynch, Helen
    Walia, Kavita
    Duffy, Geraldine
    Lawlor, Peadar G.
    Gardiner, Gillian E.
    [J]. MSYSTEMS, 2019, 4 (02)
  • [4] Early Salmonella Typhimurium infection in pigs disrupts Microbiome composition and functionality principally at the ileum mucosa
    Arguello, Hector
    Estelle, Jordi
    Zaldivar-Lopez, Sara
    Jimenez-Marin, Angeles
    Carvajal, Ana
    Asuncion Lopez-Basco, Ma
    Crispie, Fiona
    O'Sullivan, Orla
    Cotter, Paul D.
    Priego-Capote, Feliciano
    Morera, Luis
    Garrido, Juan J.
    [J]. SCIENTIFIC REPORTS, 2018, 8
  • [5] Salmonella in Swine: Prevalence, Multidrug Resistance, and Vaccination Strategies
    Bearson, Shawn M. D.
    [J]. ANNUAL REVIEW OF ANIMAL BIOSCIENCES, 2022, 10 : 373 - 393
  • [6] Salmonella Infection in Nursery Piglets and Its Role in the Spread of Salmonellosis to Further Production Periods
    Bernad-Roche, Maria
    Casanova-Higes, Alejandro
    Marin-Alcala, Clara M.
    Cebollada-Solanas, Alberto
    Mainar-Jaime, Raul C.
    [J]. PATHOGENS, 2021, 10 (02): : 1 - 14
  • [7] The European Union One Health 2021 Zoonoses Report
    Boelaert, Frank
    Amore, Giusi
    Rizzi, Valentina
    Stoicescu, Anca
    Felicio, Maria Teresa Da Silva
    Correia, Sandra Luisa De Almeida Florentino
    Hempen, Michaela
    Messens, Winy
    Antoniou, Sotiria-Eleni
    Baldinelli, Francesca
    Broglia, Alessandro
    Dhollander, Sofie
    Kohnle, Lisa
    Mur, Lina
    Niskanen, Taina
    Haussig, Joana
    Cristea, Veronica
    Scavia, Gaia
    Altieri, Ilaria
    Anniballi, Fabrizio
    Bella, Antonino
    Caccio, Simone
    Casulli, Adriano
    Ciervo, Alessandra
    Delibato, Elisabetta
    D'Errico, Michele Luca
    Fernandez, Aurora Garcia
    Morales, Maria Angeles Gomez
    Iacoponi, Francesca
    Knijn, Arnold
    Lalle, Marco
    Lucarelli, Claudia
    Morabito, Stefano
    Ortoffi, Marco
    Pasquali, Paolo
    Barbariol, Pierfrancesco
    Riccardo, Flavia
    Suffredini, Elisabetta
    Tozzoli, Rosangela
    Ventola, Eleonora
    Villa, Laura
    Angeloni, Giorgia
    Barco, Lisa
    Manca, Grazia
    Capello, Katia
    Cento, Giulia
    Ciot, Laura
    De Benedictis, Paola
    Gagliazzo, Laura
    Ishebabi, Annie
    [J]. EFSA JOURNAL, 2022, 20 (12)
  • [8] Changes in the Porcine Intestinal Microbiome in Response to Infection with Salmonella enterica and Lawsonia intracellularis
    Borewicz, Klaudyna A.
    Kim, Hyeun Bum
    Singer, Randall S.
    Gebhart, Connie J.
    Sreevatsan, Srinand
    Johnson, Timothy
    Isaacson, Richard E.
    [J]. PLOS ONE, 2015, 10 (10):
  • [9] Cytokine-Mediated Regulation of ARG1 in Macrophages and Its Impact on the Control of Salmonella enterica Serovar Typhimurium Infection
    Brigo, Natascha
    Pfeifhofer-Obermair, Christa
    Tymoszuk, Piotr
    Demetz, Egon
    Engl, Sabine
    Barros-Pinkelnig, Marina
    Dichtl, Stefanie
    Fischer, Christine
    Valente De Souza, Lara
    Petzer, Verena
    von Raffay, Laura
    Hilbe, Richard
    Berger, Sylvia
    Seifert, Markus
    Schleicher, Ulrike
    Bogdan, Christian
    Weiss, Gunter
    [J]. CELLS, 2021, 10 (07)
  • [10] Burdick Sanchez Nicole C, 2017, Transl Anim Sci, V1, P69, DOI 10.2527/tas2016.0008