Contribution of Vasoactive Intestinal Peptide to Immune Homeostasis in Trophoblast-Maternal Leukocyte Interaction under LPS Stimulation

Fraccaroli, Laura Virginia; Grasso, Esteban; Hauk, Vanesa; Cortelezzi, Marta; Leirós, Claudia Pérez; Ramhorst, Rosanna

doi:10.1159/000355039

Cited by 5 publications

(3 citation statements)

References 47 publications

(61 reference statements)

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“…It should be pointed out that the knowledge concerning the influence of LPS on the expression of neuropeptides investigated during the present study is very scanty and not limited to experiments on low single doses of bacterial endotoxin. Most of the information concerns the roles of VIP in the immune maintenance during LPS intoxication [ 46 ]. It is known that VIP may affect the monocytes stimulated by LPS, and this activity manifests itself in an increase of IL-10, IL-6 and TNFα synthesis [ 47 ], which can suggest the possibility of using VIP in adjunctive therapy to antibiotic treatments [ 48 , 49 ].…”

Section: Discussionmentioning

confidence: 99%

Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis

2017

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BackgroundThe present research was conducted to investigate the influence of a low, single dose of LPS, which does not result in any clinical symptoms of intoxication on the expression of selected neuropeptides within the intestines of the domestic pig.MethodsThis experiment was conducted on immature female pigs of the Pitrain × Duroc breed (n = five per group). Seven days after the intravenous injection of 10 mL saline solution for control animals and 5 μg/kg b.w. (in 10 mL saline solution) LPS Salmonella Enteritidis for the experimental group, the excised segments of duodenum, jejunum, ileum, ileocecal valve, caecum, descending colon, transverse colon, ascending colon and rectum were prepared to extract the main enteric neuropeptides, including GAL, NPY, SOM, SP, VIP.ResultsThe results of this research indicate that single low-dose LPS S. Enteritidis produced changes in the content of the selected neuropeptides of the porcine intestine. The most visible changes were observed in the transverse colon, where LPS induced the increase of GAL expression from 19.41 ± 7.121 to 92.92 ± 11.447 ng/g tissue.ConclusionThe exact functions of the substances studied and mechanisms of responses to LPS action depend on the sections of the intestines. The mechanisms of observed changes are not fully understood, but fluctuations in neuronal active substance levels may be connected with neurodegenerative and/or pro-inflammatory activity of LPS.

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Section: Discussionmentioning

confidence: 99%

Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis

2017

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“…Moreover, VIP increases progesterone and human chorionic gonadotrophin secretion in human trophoblast cells (31), activates trophoblast migration and invasion through VIP receptor type 1 and 2, and regulates the interaction of trophoblast cells with maternal leukocytes through autocrine and paracrine loops (32,34). Consistent with an immunomodulatory role during pregnancy, VIP promoted antiinflammatory and tolerogenic responses in cocultures of human leukocytes and trophoblast cell lines (32)(33)(34)(35)(36)(37). In mouse pregnancy, VIP was shown to stimulate mouse embryo weight gain in vitro (38), and the injection of a VIP receptor antagonist at d E9 to E11 impaired neurodevelopment, inducing microcephaly through microcephalin signaling (23,39).…”

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confidence: 91%

Trophoblast VIP deficiency entails immune homeostasis loss and adverse pregnancy outcome in mice

et al. 2018

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Immune homeostasis maintenance throughout pregnancy is critical for normal fetal development. Trophoblast cells differentiate into an invasive phenotype and contribute to the transformation of maternal arteries and the functional shaping of decidual leukocyte populations. Insufficient trophoblast invasion, inadequate vascular remodeling, and a loss of immunologic homeostasis are associated with pregnancy complications, such as preeclampsia and intrauterine growth restriction. Vasoactive intestinal peptide (VIP) is a pleiotropic neuropeptide synthetized in trophoblasts at the maternal-placental interface. It regulates the function of trophoblast cells and their interaction with decidual leukocytes. By means of a murine model of pregnancy in normal maternal background with VIP-deficient trophoblast cells, here we demonstrate that trophoblast VIP is critical for trophoblast function: VIP gene haploinsufficiency results in lower matrix metalloproteinase 9 expression, and reduced migration and invasion capacities. A reduced number of regulatory T cells at the implantation sites along with a lower expression of proangiogenic and antiinflammatory markers were also observed. Findings detected in the implantation sites at early stages were followed by an abnormal placental structure and lower fetal weight. This effect was overcome by VIP treatment of the early pregnant mice. Our results support the relevance of trophoblast-synthesized VIP as a critical factor in vivo for trophoblast-cell function and immune homeostasis maintenance in mouse pregnancy.-Hauk, V., Vota, D., Gallino, L., Calo, G., Paparini, D., Merech, F., Ochoa, F., Zotta, E., Ramhorst, R., Waschek, J., Leirós, C. P. Trophoblast VIP deficiency entails immune homeostasis loss and adverse pregnancy outcome in mice.

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“…In this sense, vasoactive intestinal peptide (VIP) is among several factors locally released that regulate trophoblast and immune cell function at the early maternal-fetal interface by the selective recruitment of specific leukocyte subpopulations and favoring a tolerogenic microenvironment (Fraccaroli et al, 2014(Fraccaroli et al, , 2015Merech et al, 2019;Paparini et al, 2019;Vota et al, 2016). On the other hand, VIP displayed embryo and neurotrophic effects in murine pregnancy (Gressens et al, 1993;Hauk et al, 2018;Hauk et al, 2019;Lim et al, 2008;Passemard et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Zika virus infection of first trimester trophoblast cells affects cell migration, metabolism and immune homeostasis control

Vota

Torti

Paparini

et al. 2020

Journal Cellular Physiology

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Zika virus (ZIKV) re‐emerged after circulating almost undetected for many years and the last spread in 2015 was the major outbreak reported. ZIKV infection was associated with congenital fetal growth anomalies such as microcephaly, brain calcifications, and low birth weight related to fetal growth restriction. In this study, we investigated the effect of ZIKV infection on first trimester trophoblast cell function and metabolism. We also studied the interaction of trophoblast cells with decidual immune populations. Results presented here demonstrate that ZIKV infection triggered a strong antiviral response in first trimester cytotrophoblast‐derived cells, impaired cell migration, increased glucose uptake and GLUT3 expression, and reduced brain derived neurotrophic factor (BDNF) expression. ZIKV infection also conditioned trophoblast cells to favor a tolerogenic response since an increased recruitment of CD14+ monocytes bearing an anti‐inflammatory profile, increased CD4+ T cells and NK CD56Dim and NK CD56Bright populations and an increment in the population CD4+ FOXP3+ IL‐10+ cells was observed. Interestingly, when ZIKV infection of trophoblast cells occurred in the presence of the vasoactive intestinal peptide (VIP) there was lower detection of viral RNA and reduced toll‐like receptor‐3 and viperin messenger RNA expression, along with reduced CD56Dim cells trafficking to trophoblast conditioned media. The effects of ZIKV infection on trophoblast cell function and immune‐trophoblast interaction shown here could contribute to defective placentation and ZIKV persistence at the fetal‐maternal interface. The inhibitory effect of VIP on ZIKV infection of trophoblast cells highlights its potential as a candidate molecule to interfere ZIKV infection during early pregnancy.

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Contribution of Vasoactive Intestinal Peptide to Immune Homeostasis in Trophoblast-Maternal Leukocyte Interaction under LPS Stimulation

Cited by 5 publications

References 47 publications

Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis

Modulation of the main porcine enteric neuropeptides by a single low-dose of lipopolysaccharide (LPS) Salmonella Enteritidis

Trophoblast VIP deficiency entails immune homeostasis loss and adverse pregnancy outcome in mice

Zika virus infection of first trimester trophoblast cells affects cell migration, metabolism and immune homeostasis control

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