Linking murine resistance to secondary cystic echinococcosis with antibody responses targeting Echinococcus granulosus tegumental antigens

Miles, Sebastián; Magnone, Javier; Cyrklaff, Marek; Arbildi, Paula; Frischknecht, Friedrich; Dematteis, Sylvia; Mourglia‐Ettlin, Gustavo

doi:10.1016/j.imbio.2020.151916

Cited by 10 publications

(6 citation statements)

References 90 publications

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“…20,21 In this regard, local (peritoneal cavity) and systemic (serum) antibody responses in infected Balb/c and C57Bl/6 mice were associated with their differences in permissiveness to secondary CE. 8,10 Accordingly, our results on serum (Figure 1) and peritoneal ( Figure 2) pAb from both strains were in line with such reports. Protective roles of natural antibodies have been described in numerous infections; 14,22 however, their functions not only depend on the ability to recognize pathogens but also on F I G U R E 1 Serum pAb profiles in early murine secondary CE.…”

Section: Discussionsupporting

confidence: 92%

Polyreactive antibodies as potential humoral biomarkers of host resistance to cystic echinococcosis

Garcia-Luna

Magnone

Miles

et al. 2020

Parasite Immunology

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Cystic echinococcosis (CE) is a cosmopolitan zoonosis caused by the larval stage of the cestode parasite Echinococcus granulosus sensu lato (s.l.). Primary CE occurs in intermediate hosts (ungulates, accidentally humans) after ingestion of oncosphere-containing eggs, which develop into metacestodes (hydatid cysts) mainly in the host liver and lungs. Secondary CE occurs after spillage of protoscoleces from a fertile cyst within an infected intermediate host, since protoscoleces' developmental plasticity allows them to become new cysts within intermediate hosts or adult worms if ingested by definitive hosts (usually dogs). 1 Human studies on CE susceptibility/resistance are scarce, 2-4 although immune responses and host immunogenetics were suggested to determine the infection outcome. 5,6 Accordingly, studies performed in individuals seropositive for CE, but ultrasound normal, reported a unique antibody profile potentially associated with host resistance. 7 Additionally, mouse strains showing differences in susceptibility to secondary CE exhibited distinct parasite-specific immune responses. 8-10

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Section: Discussionsupporting

confidence: 92%

Polyreactive antibodies as potential humoral biomarkers of host resistance to cystic echinococcosis

Garcia-Luna

Magnone

Miles

et al. 2020

Parasite Immunology

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“…in the metacestode stage, a wide range of mammal species are known to be natural intermediate hosts, consequently, a long list of species has been used for experimental infections (Breijo et al ., 1998 ). The experimental model for secondary echinococcosis established in rodents and lagomorphs by intraperitoneal injection of PSCs into the peritoneum has been proven to be useful in studying basic aspects of Echinococcus spp., such as immunobiology, investigating in vivo differentiation process of their secondary cysts in a host and the early local interactions between host and parasite during this process, and testing new chemotherapeutic agents or therapeutical protocols, vaccine candidates and diagnostics or follow-up tools (Dempster et al ., 1991 ; Breijo et al ., 1998 ; Cucher et al ., 2013 ; Wang et al ., 2018 ; Miles et al ., 2020 ). Similarly, infection of laboratory model of E. shiquicus metacestode has been successfully established by means of secondary infection through intraperitoneal injection.…”

Section: Discussionmentioning

confidence: 99%

“…The development of E. shiquicus in an attempt to investigate secondary cysts infection through intraperitoneal metacestode material injection in different laboratory animal models shows that mice and jirds are able to support the development of E. shiquicus larva despite some differences in cyst characteristics, for example, cysts from mice do not produce PSCs, while cysts produced by jirds can produce large numbers of PSCs (Sato et al ., 1998 ; Miles et al ., 2020 ). In the present study in Mongolian jirds, as the duration of post infection increases, the size of the cyst as well as the production of PSC increased.…”

Section: Discussionmentioning

confidence: 99%

“…And the 2 animal models of E. shiquicus metacestode in the present study will provide sufficient experimental materials for future investigations on the biological characteristics and growth and development of E. shiquicus . Infection of different intermediate hosts with the same Echinococcus species produces 2 forms of cysts, the fertile and sterile cysts, which may be related to host specificity and immune response to the parasites (Romig and Bilger, 1999 ; Miles et al ., 2020 ). Previous studies have shown that once metacestodes have been established, both fertile and sterile cysts can grow normally as long as the laminated layer remains intact and whether PSCs are produced or not (Hidalgo et al ., 2019 ).…”

Section: Discussionmentioning

confidence: 99%

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Establishment of a secondary infection laboratory model of Echinococcus shiquicus metacestode using BALB/c mice and Mongolian jirds (Meriones unguiculatus)

Fang

et al. 2023

Parasitology

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Echinococcus shiquicus is peculiar to the Qinghai–Tibet plateau of China. Research on this parasite has mainly focused on epidemiological surveys and life cycle studies. So far, limited laboratory studies have been reported. Here, experimental infection of E. shiquicus metacestode in BALB/c mice and Mongolian jirds (Meriones unguiculatus) was carried out to establish alternative laboratory animal models. Intraperitoneal inoculation of metacestode material containing protoscoleces (PSCs) obtained from infected plateau pikas were conducted on BALB/c mice. Furthermore, metacestode material without PSCs deriving from infected BALB/c mice was intraperitoneally inoculated to Mongolian jirds. Experimental animals were dissected for macroscopic and histopathological examination. The growth of cysts in BALB/c mice was infiltrative, and they invaded the murine entire body. Most of the metacestode cysts were multicystic, but a few were unilocular. The cysts contained sterile vesicles, which had no PSCs. The metacestode materials were able to successfully infect new mice. In the jirds model, E. shiquicus cysts were typically formed freely in the peritoneal cavity; the majority of these cysts were free while a small portion adhered loosely to nearby organs. The proportion of fertile cysts was high, and contained many PSCs. The PSCs produced in Mongolian jirds also successfully infected new ones, which confirms that jirds can serve as an alternative experimental intermediate host. In conclusion, a laboratory animal infection was successfully established for E. shiquicus using BALB/c mice and Mongolian jirds. These results provide new models for the in-depth study of Echinococcus metacestode survival strategy, host interactions and immune escape mechanism.

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“…In this regard, PSC of E. granulosus s.l. were shown susceptible to the killing by either activated macrophages [26,27,49] or the complement system [23,25,[50][51][52][53]. Therefore, an early peritoneal induction of IgG2a and IgG2b might correlate with a lower parasite survival during pre-encystment, partially contributing to the prophylactic activity observed after exogenous administration of rshCD5 or rshCD6 [8].…”

Section: Brief Definitive Reportmentioning

confidence: 99%

Recombinant CD5 and CD6 Ectodomains Induce Antiparasitic and Immunomodulatory Effects in Secondary Cystic Echinococcosis

García‐Luna,

Rivero‐Osorio,

González‐Porcile

et al. 2024

Parasite Immunology

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Scavenger receptors participate in a wide range of biological functions after binding to multiple non‐self or altered self‐ligands. Among them, CD5 and CD6 are lymphocyte scavenger receptors known to interact with different microbial‐associated molecular patterns, and the administration of the recombinant soluble ectodomains of human CD5 (rshCD5) and/or CD6 (rshCD6) has shown therapeutic/prophylactic potential in experimental models of fungal, bacterial and echinococcal infections. The latter is a zoonosis caused by the larval stage of the cestode parasite Echinococcus granulosus sensu lato, which in humans can induce secondary cystic echinococcosis (CE) after the spillage of protoscoleces contained within fertile cysts, either spontaneously or during surgical removal of primary hydatid cysts. Herein, we have analysed the mechanisms behind the significant protection observed in the mouse model of secondary CE following prophylactic administration of rshCD5 or rshCD6. Our results show that both molecules exhibit intrinsic antiparasitic activities in vitro, as well as immunomodulatory functions during early secondary CE, mainly through Th1/Th17 cytokine bias and promotion of peritoneal polyreactive antibodies. These data support the relevance of the parasite components bound by rshCD5 and rshCD6, as well as the potential of their prophylactic administration as a useful strategy to reduce secondary CE in patients.

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Linking murine resistance to secondary cystic echinococcosis with antibody responses targeting Echinococcus granulosus tegumental antigens

Cited by 10 publications

References 90 publications

Polyreactive antibodies as potential humoral biomarkers of host resistance to cystic echinococcosis

Polyreactive antibodies as potential humoral biomarkers of host resistance to cystic echinococcosis

Establishment of a secondary infection laboratory model of Echinococcus shiquicus metacestode using BALB/c mice and Mongolian jirds (Meriones unguiculatus)

Recombinant CD5 and CD6 Ectodomains Induce Antiparasitic and Immunomodulatory Effects in Secondary Cystic Echinococcosis

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