Elsevier

Veterinary Parasitology

Volume 289, January 2021, 109325
Veterinary Parasitology

The immune gene expression induced by Cooperia punctata in naturally infected calves with resistance and susceptible phenotype traits

https://doi.org/10.1016/j.vetpar.2020.109325Get rights and content

Highlights

  • Immune gene expression was analysed from calves infected with Cooperia punctate.

  • Strong immune regulation was observed in early C. punctata infection in resistant calves.

  • The acute C. punctata infection in susceptible calves caused immunosuppression.

  • The IL-5 gene was the dominant genes in calves resistant to C. punctate.

  • INF-γ gene was the main cytokine identified in calves susceptible to C. punctate.

Abstract

The analysis of the immune gene expression was performed in Zebu × Holstein calves with resistant and susceptible phenotypes naturally infected with Cooperia punctata. Fourteen calves of 4 months old were grazed for 11 weeks under a tropical climate. The parasitic infection showed an average epg value of 1055 ± 1155 and an IgG optical density of 0.814 ± 0.0.037 with statistic differences among the different weeks (p < 0.05), and a pcv value of 24 ± 2.0 % (p > 0.05). High variation in epg value was observed, between 7 ± 7.14 and 4657 ± 1886, and, based on these differences; the infected hosts were classified as five resistant calves with epg ≤ 200 and nine susceptible calves with epg ≥ 300. Moreover, IgG levels displayed statistical differences between resistance and susceptible calves to C. punctata infection. The immune gene expression was analysed in three resistant and susceptible calves, respectively. Nine cytokine genes and the FCεR1A receptor were analysed at the 3rd and 11th weeks post-infection. In the first period upregulation was found, from 2.19- to 9.45-fold, (p < 0.05) for IL-2, -5, - 6, -10, TGF-β and FCεR1A in the resistant group; the expression was decreased at the 11th week with low level of IgG. In contrast, downregulation for susceptible calves was found for nine immune genes and upregulation for INF-γ in both periods together with increased IgG levels. In conclusion, immune gene expression was regulated at the begging infection of C. punctata in resistant grazing calves. In contrast, suppression of important genes was involved in calves susceptible to C. punctata.

Introduction

The nematode Cooperia spp. has become a problem in grazing cattle due to its high prevalence (80 %) and anthelmintic resistance in tropical and temperate regions (Felippelli et al., 2014; Suárez et al., 2017; García-Ruíz et al., 2019). Studies have reported the importance of the pathology caused by Cooperia spp. infection on the small intestinal mucosa that affects animal health and production and has impacts on farm economics (Stromberg et al., 2012; Höglund et al., 2018, das Neves et al., 2020). Despite the pathology caused by Cooperia spp., infection in calves induces an immune response to regulate the infection, although it requires time to achieve acquired immunity (Gasbarre et al., 2001). The development of immune response and the identification of cattle resistant to gastrointestinal nematodes (GINs) are closely related to the exposure of infected calves to nematode species such as Ostertagia ostertagi, Haemonchus placei and Cooperia spp. given the advantage of improving the genetic husbandry in endemic regions (Bricarello et al., 2007; Höglund et al., 2018; García-Ruíz et al., 2019). In México, the Zebu × Holstein cattle is a crossbreed selected by farmers due to its tolerance to warm climates. This crossbreed is used for its double zootechnic ability to produce milk and meat. However, cattle in tropical climates face problems with diverse pathogens, including the prevalence of parasites and anthelmintic resistance (Barajas-Rojas et al., 1993; Acosta-Rodríguez et al., 2005; Villa-Mancera and Reynoso-Palomar, 2019, das Neves et al., 2020). The characterisation of the immune response in young cattle from a selected group might contribute to the selection of calves with genetic tolerance to parasitic nematodes in this region.

Section snippets

Locality

The study was performed at CENID-SAI, INIFAP, Mor., México, in Jiutepec, Mor., México and at the ‘El Clarín’ Experimental Station of the Veterinary Faculty of Medicine and Zootechnic, UNAM. This station is located in Martínez de la Torre in Tlapacoyan, Veracruz, México, at 24°4′N; 97°03′W and experiences a sub-humid tropical climate with temperature around 23 °C, annual rainfall of 1840 mm and humidity 85 ± 6%.

Farm history

The experimental station maintains Zebu × Holstein cattle to produce milk and meat.

Phenotype parameters

The genus Cooperia was confirmed as the main species in infected calves by PCR-end point showing a fragment at 176 bp.

Discussion

The inflammation process is the main pathology associated with GINs following larval invasion and the growth of larval stages into the gastrointestinal tissue. At same time, a series of immune inflammatory cells and regulatory mechanisms are involved in modulating the infection (Gasbarre et al., 2001; Shea-Donohue et al., 2010). The C. punctata infectivity caused acute immunosuppressive gene expression in almost all genes except for INF-γ, IL-6 and IL-10 genes in susceptible calves that

Conclusions

The infection of the Zebu × Holstein calves with Cooperia punctata as the prevalent GIN showed the importance of the immune response during the beginning infection period in enhancing the immune protection that was observed the end of this experimental study. The present study worked with only a few cattle, but there are other studies that have involved numerous breeds and crossbreed cattle and reported similar observations. Also, inflammatory and immune regulatory genes and those genes related

Disclosure

The authors of this manuscript have no financial or personal relationship with other people or organization that could be inappropriately influence of the content of this paper.

CRediT authorship contribution statement

Ivette Matamoros-Mercado: Methodology, Software. Elke von-Son-de-Fernex: Methodology, Validation, Investigation, Writing - review & editing. Miguel Ángel Alonso-Díaz: Resources, Funding acquisition, Writing - review & editing. David Emanuel Reyes-Guerrero: Methodology, Formal analysis, Validation, Investigation, Writing - original draft. Sara Olazaran-Jenkins: Methodology, Validation. Betzaid Sánchez-Sánchez: Methodology, Formal analysis. Ma. Eugenia López-Arellano: Conceptualization, Funding

Declaration of Competing Interest

Authors have no potential conflict of interest pertaining to this submission.

Acknowledgements

This study received financial support from CENID-SAI, INIFAP number 20442833091. The present study was performance by Ivette Matamoros-Mercado and Betzaid Sánchez-Sánchez to obtain the Biotechnology Engineer Bachelor′s degree.

References (24)

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    The ability of H. placei E/S products was also recognised by IgG in infected calves, indicating a certain degree of immunity that requires more studies (Schallig et al., 1996; Contreras-Ochoa et al., 2019). However, it is important to mention that GI nematodes of cattle require a longer period of exposure before the level of immunity is observed (Klesius, 1988; Gasbarre et al., 2001; Matamoros-Mercado et al., 2021). A detailed analysis of H. placei E/S products and the activity of immune response against this parasite is little known concerning antigens; for instance, the 15 and 70 kDa E/S appeared to play an important role in a previous study (Contreras-Ochoa et al., 2019).

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