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Abstract

Staphylococcal enterotoxin B (SEB) is an extensively studied super-antigen. A previous study by us suggested that SEB exposure during pregnancy could alter the percentage of CD4 and CD8 T cells in the peripheral blood of neonatal offspring rats.

It is unknown whether SEB exposure during pregnancy can influence the development of regulatory T cells (Tregs) in the peripheral blood of neonatal offspring rats.

Pregnant rats at gestational day 16 were intravenously injected with 15 µg SEB. Peripheral blood was acquired from neonatal offspring rats on days 1, 3 and 5 after delivery and from adult offspring rats for determination of Treg number by cytometry, cytokines by ELISA, and FoxP3 expression by real-time PCR and western blot.

SEB given to pregnant rats significantly increased the absolute number of Tregs and the expression levels of FoxP3, IL-10 and TGF-β (<0.05, <0.01) in the peripheral blood of not only neonatal but also adult offspring rats. Furthermore, repeated SEB exposure in adult offspring rats significantly decreased the absolute number of Tregs (<0.01), and the expression levels of FoxP3, IL-10 and TGF-β (<0.05, <0.01) in their peripheral blood.

Prenatal SEB exposure attenuates the development and function of Tregs to repeated SEB exposure in the peripheral blood of adult offspring rats.

Funding
This study was supported by the:
  • National Natural Science Foundation of China (Award 81571454)
    • Principle Award Recipient: Jun-chang Guan
  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
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2020-02-11
2024-12-14
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References

  1. Hassoun A, Linden PK, Friedman B. Incidence, prevalence, and management of MRSA bacteremia across patient populations-a review of recent developments in MRSA management and treatment. Crit Care 2017; 21:211 [View Article][PubMed]
    [Google Scholar]
  2. McCormick JK, Yarwood JM, Schlievert PM. Toxic shock syndrome and bacterial superantigens: an update. Annu Rev Microbiol 2001; 55:77–104 [View Article][PubMed]
    [Google Scholar]
  3. Kawabe Y, Ochi A. Selective anergy of V beta 8+,CD4+ T cells in Staphylococcus enterotoxin B-primed mice. J Exp Med 1990; 172:1065–1070 [View Article][PubMed]
    [Google Scholar]
  4. Kawabe Y, Ochi A. Programmed cell death and extrathymic reduction of Vbeta8+ CD4+ T cells in mice tolerant to Staphylococcus aureus enterotoxin B. Nature 1991; 349:245–248 [View Article][PubMed]
    [Google Scholar]
  5. Abdi Z, Eskandary H, Nematollahi-Mahani SN. Induction of human glioma tumor in Sprague-Dawley rats with intact immune system. Turk Neurosurg 2017; 27:716–724 [View Article][PubMed]
    [Google Scholar]
  6. Moon EK, Lee SH, Goo TW, Quan F-S. Immune responses induced by co-infection with Capillaria hepatica in Clonorchis sinensis-infected rats. J Helminthol 2018; 92:395–402 [View Article][PubMed]
    [Google Scholar]
  7. Osborne BF, Caulfield JI, Solomotis SA, Schwarz JM. Neonatal infection produces significant changes in immune function with no associated learning deficits in juvenile rats. Dev Neurobiol 2017; 77:1221–1236 [View Article][PubMed]
    [Google Scholar]
  8. Calzada D, Baos S, Cremades-Jimeno L, Cárdaba B. Immunological mechanisms in allergic diseases and allergen tolerance: the role of Treg cells. J Immunol Res 2018; 2018:1–10 [View Article][PubMed]
    [Google Scholar]
  9. Kim JM, Rudensky A. The role of the transcription factor FOXP3 in the development of regulatory T cells. Immunol Rev 2006; 212:86–98 [View Article]
    [Google Scholar]
  10. Kawai K, Uchiyama M, Hester J, Wood K, Issa F. Regulatory T cells for tolerance. Hum Immunol 2018; 79:294–303 [View Article][PubMed]
    [Google Scholar]
  11. Miles B, Connick E. Control of the germinal center by follicular regulatory T cells during infection. Front Immunol 2018; 9:2704 [View Article][PubMed]
    [Google Scholar]
  12. Umetsu DT, Akbari O, Dekruyff RH. Regulatory T cells control the development of allergic disease and asthma. J Allergy Clin Immunol 2003; 112:480–487 [View Article][PubMed]
    [Google Scholar]
  13. Feunou P, Poulin L, Habran C, Le Moine A, Goldman M et al. Cd4+Cd25+ and CD4+CD25- T cells act respectively as inducer and effector T suppressor cells in superantigen-induced tolerance. J Immunol 2003; 171:3475–3484 [View Article][PubMed]
    [Google Scholar]
  14. Maeda H, Fujimoto S, Greene MI. Suppressor T cells regulate the nonanergic cell population that remains after peripheral tolerance is induced to the Mls-1 antigen in T cell receptor Vbeta 8.1 transgenic mice. Proc Natl Acad Sci U S A 2000; 97:13257–13262 [View Article][PubMed]
    [Google Scholar]
  15. Charles MA, Delpierre C, Bréant B. Developmental origin of health and adult diseases (DOHaD): evolution of a concept over three decades. Med Sci 2016; 32:15–20 [View Article][PubMed]
    [Google Scholar]
  16. Luyten LJ, Saenen ND, Janssen BG, Vrijens K, Plusquin M et al. Air pollution and the fetal origin of disease: a systematic review of the molecular signatures of air pollution exposure in human placenta. Environ Res 2018; 166:310–323 [View Article][PubMed]
    [Google Scholar]
  17. Nguyen B, Venet D, Lambertini M, Desmedt C, Salgado R et al. Imprint of parity and age at first pregnancy onthe genomic landscape of subsequent breastcancer. Breast Cancer Res 2019; 21:25
    [Google Scholar]
  18. Lin J, Yao Z. Maternal-infant correlation of multidrug-resistant Staphylococcus aureus carriage: a prospective cohort study. Front Pediatr 2018; 6:384 [View Article][PubMed]
    [Google Scholar]
  19. Pinter DM, Mandel J, Hulten KG, Minkoff H, Tosi MF. Maternal-infant perinatal transmission of methicillin-resistant and methicillin-sensitive Staphylococcus aureus. Am J Perinatol 2009; 26:145–151 [View Article][PubMed]
    [Google Scholar]
  20. Zhou P, Zhang X-S, Xu Z-B, Gao S-X, Zheng Q-W et al. Staphylococcal enterotoxin B administration in pregnant rats alters the splenic lymphocyte response in adult offspring rats. BMC Microbiol 2017; 17:1 [View Article][PubMed]
    [Google Scholar]
  21. Shevach EM. Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 2009; 30:636–645 [View Article][PubMed]
    [Google Scholar]
  22. Laiosa MD, Eckles KG, Langdon M, Rosenspire AJ, McCabe MJ. Exposure to inorganic mercury in vivo attenuates extrinsic apoptotic signaling in Staphylococcal aureus enterotoxin B stimulated T-cells. Toxicol Appl Pharmacol 2007; 225:238–250 [View Article][PubMed]
    [Google Scholar]
  23. Zhang T, Yu F-l, Yang W-x, Ruan M-m, Yue Z-y et al. Staphylococcal enterotoxin B administration during pregnancy imprints the increased CD4:CD8 T-cell ratio in the peripheral blood from neonatal to adult offspring rats. J Med Microbiol 2015; 64:1–6 [View Article]
    [Google Scholar]
  24. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor FOXP3. Science 2003; 299:1057–1061 [View Article][PubMed]
    [Google Scholar]
  25. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999; 190:995–1004 [View Article][PubMed]
    [Google Scholar]
  26. Powrie F, Carlino J, Leach MW, Mauze S, Coffman RL. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med 1996; 183:2669–2674 [View Article][PubMed]
    [Google Scholar]
  27. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S. Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002; 3:135–142 [View Article][PubMed]
    [Google Scholar]
  28. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J et al. Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000; 192:303–310 [View Article][PubMed]
    [Google Scholar]
  29. Miller C, Ragheb JA, Schwartz RH. Anergy and cytokine-mediated suppression as distinct superantigen-induced tolerance mechanisms in vivo . J Exp Med 1999; 190:53–64 [View Article][PubMed]
    [Google Scholar]
  30. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003; 3:253–257 [View Article][PubMed]
    [Google Scholar]
  31. Shevach EM. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 2006; 25:195–201 [View Article][PubMed]
    [Google Scholar]
  32. Taylor AL, Llewelyn MJ. Superantigen-induced proliferation of human CD4+CD25- T cells is followed by a switch to a functional regulatory phenotype. J Immunol 2010; 185:6591–6598 [View Article][PubMed]
    [Google Scholar]
  33. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995; 155:1151–1164[PubMed]
    [Google Scholar]
  34. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4:330–336 [View Article][PubMed]
    [Google Scholar]
  35. Grundström S, Cederbom L, Sundstedt A, Scheipers P, Ivars F. Superantigen-induced regulatory T cells display different suppressive functions in the presence or absence of natural CD4+CD25+ regulatory T cells in vivo . J Immunol 2003; 170:5008–5017 [View Article][PubMed]
    [Google Scholar]
  36. Gomez de Agüero M, Ganal-Vonarburg SC, Fuhrer T, Rupp S, Uchimura Y et al. The maternal microbiota drives early postnatal innate immune development. Science 2016; 351:1296–1302 [View Article][PubMed]
    [Google Scholar]
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