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Journal of Immunology Research
Volume 2017 (2017), Article ID 8081642, 10 pages
https://doi.org/10.1155/2017/8081642
Research Article

Administration of Rhodiola kirilowii Extracts during Mouse Pregnancy and Lactation Stimulates Innate but Not Adaptive Immunity of the Offspring

1Department of Regenerative Medicine and Cell Biology, Military Institute of Hygiene and Epidemiology, Kozielska 4, 01-163 Warsaw, Poland
2Pathomorphology Department, Center for Biostructure Research, Warsaw Medical University, Chałubińskiego 5, 02-004 Warsaw, Poland

Correspondence should be addressed to Robert Zdanowski; moc.oohay@xotzr

Received 2 March 2017; Accepted 14 September 2017; Published 30 October 2017

Academic Editor: Daniel Ortuño-Sahagún

Copyright © 2017 Sławomir Lewicki et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. Jędrychowski, A. Gałaś, R. Whyatt, and F. Perera, “The prenatal use of antibiotics and the development of allergic disease in one year old infants. A preliminary study,” International Journal of Occupational Medicine and Environmental Health, vol. 19, no. 1, pp. 70–76, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Hecht, “Drug safety labeling for doctors,” FDA Consumer, vol. 13, no. 8, pp. 12-13, 1979. View at Google Scholar
  3. E. Skopińska-Różewska, M. Mościcka-Wesołowska, A. Wasiutyński, J. Małdyk, M. Malejczyk, and J. Pazdur, “Lymphatic system of mice born from mothers treated with ampicillin or cloxacillin during gestation,” Archivum Immunologiae et Therapiae Experimentalis, vol. 34, no. 2, pp. 203–209, 1985. View at Google Scholar
  4. B. Włodarska, J. Bany, M. Marczak et al., “Altered immune reactivity of mice born from mothers treated with ampicillin during gestation,” Folia Biologica, vol. 33, no. 3, pp. 211–215, 1987. View at Google Scholar
  5. N. T. Mueller, E. Bakacs, J. Combellick, Z. Grigoryan, and M. G. Dominguez-Bello, “The infant microbiome development: mom matters,” Trends in Molecular Medicine, vol. 21, no. 2, pp. 109–117, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. T. F. Landers, B. Cohen, T. E. Wittum, and E. L. Larson, “A review of antibiotic use in food animals: perspective, policy, and potential,” Public Health Reports, vol. 127, no. 1, pp. 4–22, 2012. View at Publisher · View at Google Scholar
  7. C. L. Ventola, “The antibiotic resistance crisis: part 1: causes and threats,” Pharmacy and Therapeutics, vol. 40, no. 4, pp. 277–283, 2015. View at Google Scholar
  8. A. G. Mathew, R. Cissell, and S. Liamthong, “Antibiotic resistance in bacteria associated with food animals: a United States perspective of livestock production,” Foodborne Pathogens and Disease, vol. 4, no. 2, pp. 115–133, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Grech-Baran, K. Sykłowska-Baranek, and A. Pietrosiuk, “Approaches of Rhodiola kirilowii and Rhodiola rosea field cultivation in Poland and their potential health benefits,” Annals of Agricultural and Environmental Medicine, vol. 22, no. 2, pp. 281–285, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. M. L. Chuang, T. C. Wu, Y. T. Wang et al., “Adjunctive treatment with Rhodiola crenulata in patients with chronic obstructive pulmonary disease - a randomized placebo controlled double blind clinical trial,” PLoS One, vol. 10, no. 6, article e0128142, 2015. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Yu, Y. Qin, Q. Wang et al., “The efficacy and safety of Chinese herbal medicine, Rhodiola formulation in treating ischemic heart disease: a systematic review and meta-analysis of randomized controlled trials,” Complementary Therapies in Medicine, vol. 22, no. 4, pp. 814–825, 2014. View at Publisher · View at Google Scholar · View at Scopus
  12. K. P. Mishra, L. Ganju, and S. B. Singh, “Anti-cellular and immunomodulatory potential of aqueous extract of Rhodiola imbricata rhizome,” Immunopharmacology and Immunotoxicology, vol. 34, no. 3, pp. 513–518, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. J. L. Cui, T. T. Guo, Z. X. Ren, N. S. Zhang, and M. L. Wang, “Diversity and antioxidant activity of culturable endophytic fungi from alpine plants of Rhodiola crenulata, R. angusta, and R. sachalinensis,” PLoS One, vol. 10, no. 3, article e0118204, 2015. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Zuo, Z. Li, L. Chen, and X. Xu, “Activity of compounds from Chinese herbal medicine Rhodiola kirilowii (Regel) Maxim against HCV NS3 serine protease,” Antiviral Research, vol. 76, no. 1, pp. 86–92, 2007. View at Publisher · View at Google Scholar · View at Scopus
  15. Y. C. Wong, M. Zhao, Y. Y. Zong, C. Y. Chan, and C. T. Che, “Chemical constituents and anti-tuberculous activity of root of Rhodiola kirilowii,” Zhongguo Zhong Yao Za Zhi, vol. 33, no. 13, pp. 1561–1565, 2008. View at Google Scholar
  16. K. Khanna, K. P. Mishra, L. Ganju, and S. B. Singh, “Golden root: a wholesome treat of immunity,” Biomedicine & Pharmacotherapy, vol. 87, pp. 496–502, 2017. View at Publisher · View at Google Scholar
  17. E. Skopinska-Różewska, M. Bychawska, B. Białas-Chromiec, and E. Sommer, “The in vivo effect of Rhodiola rosea and Rhodiola quadrifida hydro-alcoholic extracts on chemokinetic activity of spleen lymphocytes in mice,” Central European Journal of Immunology, vol. 34, no. 1, pp. 42–45, 2009. View at Google Scholar
  18. R. Wójcik, A. K. Siwicki, E. Skopińska-Rózewska, A. Wasiutyński, E. Sommer, and M. Furmanowa, “The effect of Chinese medicinal herb Rhodiola kirilowii extracts on cellular immunity in mice and rats,” Polish Journal of Veterinary Sciences, vol. 12, no. 3, pp. 399–405, 2009. View at Google Scholar
  19. R. Zdanowski, S. Lewicki, E. Skopińska-Różewska, W. Buchwald, P. M. Mrozikiewicz, and W. Stankiewicz, “Alcohol- and water-based extracts obtained from Rhodiola rosea affect differently the number and metabolic activity of circulating granulocytes in Balb/c mice,” Annals of Agricultural and Environmental Medicine, vol. 21, no. 1, pp. 120–123, 2014. View at Google Scholar
  20. E. Skopińska-Rózewska, R. Wójcik, A. K. Siwicki et al., “The effect of Rhodiola quadrifida extracts on cellular immunity in mice and rats,” Polish Journal of Veterinary Sciences, vol. 11, no. 2, pp. 105–111, 2008. View at Google Scholar
  21. A. K. Siwicki, E. Skopińska-Rożewska, M. Hartwich et al., “The influence of Rhodiola rosea extracts on nonspecific and specific cellular immunity in pigs, rats and mice,” Central European Journal of Immunology, vol. 32, no. 2, pp. 84–91, 2007. View at Google Scholar
  22. E. Skopińska-Różewska, W. Stankiewicz, R. Zdanowski et al., “The in vivo effect of Rhodiola quadrifida extracts on the antibody production, on the blood leukocytes subpopulations and on the bacterial infection in mice,” Central European Journal of Immunology, vol. 37, no. 2, pp. 140–144, 2012. View at Google Scholar
  23. R. Zdanowski, S. Lewicki, K. Sikorska et al., “The influence of aqueous and hydro-alcoholic extracts of roots and rhizomes of Rhodiola kirilowii on the course of pregnancy in mice,” Central European Journal of Immunology, vol. 39, no. 4, pp. 471–475, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Lewicki, B. J. Bałan, E. Skopińska-Różewska et al., “Modulatory effects of feeding pregnant and lactating mice Rhodiola kirilowii extracts on the immune system of offspring,” Experimental and Therapeutic Medicine, vol. 12, no. 5, pp. 3450–3458, 2016. View at Publisher · View at Google Scholar · View at Scopus
  25. B. Kalicki, S. Lewicki, W. Stankiewicz et al., “Examination of correlation between vitamin D3 (25-OHD3) concentration and percentage of regulatory T lymphocytes (FoxP3) in children with allergy symptoms,” Central European Journal of Immunology, vol. 38, no. 1, pp. 70–75, 2013. View at Publisher · View at Google Scholar · View at Scopus
  26. G. Mor and I. Cardenas, “The immune system in pregnancy: a unique complexity,” American Journal of Reproductive Immunology, vol. 63, no. 6, pp. 425–433, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Lewicki, W. Stankiewicz, E. Skopińska-Różewska et al., “Spleen content of selected polyphenols, splenocytes morphology and function in mice fed Rhodiola kirilowii extracts during pregnancy and lactation,” Polish Journal of Veterinary Sciences, vol. 18, no. 4, pp. 847–855, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. V. Gupta, S. Saggu, R. K. Tulsawani, R. C. Sawhney, and R. Kumar, “A dose dependent adaptogenic and safety evaluation of Rhodiola imbricata Edgew, a high altitude rhizome,” Food and Chemical Toxicology, vol. 46, no. 5, pp. 1645–1652, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Senthilkumar, R. Chandran, and T. Parimelazhagan, “Hepatoprotective effect of Rhodiola imbricata rhizome against paracetamol-induced liver toxicity in rats,” Saudi Journal of Biological Sciences, vol. 21, no. 5, pp. 409–416, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. R. Zdanowski, E. Skopińska-Różewska, J. Wilczak, A. Borecka, A. Lewicka, and S. Lewicki, “Different effects of feeding pregnant and lactating mice Rhodiola kirilowii aqueous and hydro-alcoholic extracts on their serum angiogenic activity and selected polyphenols content,” Central European Journal of Immunology, vol. 42, pp. 17–23, 2017. View at Publisher · View at Google Scholar
  31. S. Guan, Y. Xiong, B. Song et al., “Protective effects of salidroside from Rhodiola rosea on LPS-induced acute lung injury in mice,” Immunopharmacology and Immunotoxicology, vol. 34, no. 4, pp. 667–672, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. X. Zhang, B. Zhu, S. Jin, S. Yan, and Z. Chen, “Effects of salidroside on bone marrow matrix metalloproteinases of bone marrow depressed anemic mice,” Sheng Wu Yi Xue Gong Cheng Xue Za Zhi, vol. 23, no. 6, pp. 1314–1319, 2006. View at Google Scholar
  33. R. V. Luckheeram, R. Zhou, A. D. Verma, and B. Xia, “CD4+ T cells: differentiation and functions,” Clinical and Developmental Immunology, vol. 2012, Article ID 925135, 12 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. A. A. Okoye and L. J. Picker, “CD4+ T-cell depletion in HIV infection: mechanisms of immunological failure,” Immunological Reviews, vol. 254, no. 1, pp. 54–64, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Bień, S. Lewicki, R. Zdanowski, E. Skopinska-Różewska, and M. Krzyżowska, “Feeding pregnant and lactating mice Rhodiola kirilowii extracts helps to preserve thymus function of their adult progeny,” Polish Journal of Veterinary Sciences, vol. 19, no. 3, pp. 581–587, 2016. View at Publisher · View at Google Scholar · View at Scopus
  36. M. W. Liu, M. X. Su, W. Zhang, L. M. Zhang, Y. H. Wang, and C. Y. Qian, “Rhodiola rosea suppresses thymus T-lymphocyte apoptosis by downregulating tumor necrosis factor-α-induced protein 8-like-2 in septic rats,” International Journal of Molecular Medicine, vol. 36, no. 2, pp. 386–398, 2015. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Lewicki, P. Orłowski, M. Krzyżowska, A. Kiepura, E. Skopińska-Różewska, and R. Zdanowski, “The effect of feeding mice during gestation and nursing with Rhodiola kirilowii extracts or epigallocatechin on CD4 and CD8 cells number and distribution in the spleen of their progeny,” Central European Journal of Immunology, vol. 42, no. 1, pp. 10–16, 2017. View at Publisher · View at Google Scholar
  38. X. Xu, P. Li, P. Zhang et al., “Differential effects of Rhodiola rosea on regulatory T cell differentiation and interferon-γ production in vitro and in vivo,” Molecular Medicine Reports, vol. 14, no. 1, pp. 529–536, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. D. Wolf, S. Sopper, A. Pircher, G. Gastl, and A. M. Wolf, “Treg(s) in Cancer: Friends or foe?” Journal of Cellular Physiology, vol. 230, no. 11, pp. 2598–2605, 2015. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Vivier, E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini, “Functions of natural killer cells,” Nature Immunology, vol. 9, no. 5, pp. 503–510, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. S. J. Lee, W. Y. Kang, Y. Yoon et al., “Natural killer (NK) cells inhibit systemic metastasis of glioblastoma cells and have therapeutic effects against glioblastomas in the brain,” BMC Cancer, vol. 15, p. 1011, 2015. View at Publisher · View at Google Scholar · View at Scopus
  42. D. Diwaker, K. P. Mishra, L. Ganju, and S. B. Singh, “Rhodiola inhibits dengue virus multiplication by inducing innate immune response genes RIG-I, MDA5 and ISG in human monocytes,” Archives of Virology, vol. 159, no. 8, pp. 1975–1986, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. D. C. Dale, L. Boxer, and W. C. Liles, “The phagocytes: neutrophils and monocytes,” Blood, vol. 112, no. 4, pp. 935–945, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. R. T. Steigbigel, L. H. Lambert, and J. S. Remington, “Phagocytic and bactericidal properties of normal human monocytes,” Journal of Clinical Investigation, vol. 53, no. 1, pp. 131–142, 1974. View at Publisher · View at Google Scholar
  45. W. Hirt, T. Nebe, and C. Birr, “Phagotest and Bursttest (Phagoburst), test kits for study of phagocyte functions,” Wiener Klinische Wochenschrift, vol. 106, no. 8, pp. 250–252, 1994. View at Google Scholar
  46. A. Filias, G. L. Theodorou, S. Mouzopoulou, A. A. Varvarigou, S. Mantagos, and M. Karakantza, “Phagocytic ability of neutrophils and monocytes in neonates,” BMC Pediatrics, vol. 11, no. 29, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Zhou, R. Somasundaram, R. F. Nederhof et al., “Impact of human granulocyte and monocyte isolation procedures on functional studies,” Clinical and Vaccine Immunology, vol. 19, no. 7, pp. 1065–1074, 2012. View at Publisher · View at Google Scholar · View at Scopus
  48. J. L. Banyer, N. H. Hamilton, I. A. Ramshaw, and A. J. Ramsay, “Cytokines in innate and adaptive immunity,” Reviews in Immunogenetics, vol. 2, no. 3, pp. 359–373, 2000. View at Google Scholar
  49. K. Newton and V. M. Dixit, “Signaling in innate immunity and inflammation,” Cold Spring Harbor Perspectives in Biology, vol. 4, no. 3, article a006049, 2012. View at Publisher · View at Google Scholar · View at Scopus
  50. S. S. Lin, L. W. Chin, P. C. Chao et al., “In vivo Th1 and Th2 cytokine modulation effects of Rhodiola rosea standardised solution and its major constituent, salidroside,” Phytotherapy Research, vol. 25, no. 11, pp. 1604–1611, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Ouyang, J. K. Kolls, and Y. Zheng, “The biological functions of T helper 17 cell effector cytokines in inflammation,” Immunity, vol. 28, no. 4, pp. 454–467, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. R. M. Onishi and S. L. Gaffen, “Interleukin-17 and its target genes: mechanisms of interleukin-17 function in disease,” Immunology, vol. 129, no. 3, pp. 311–321, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Lewicki, E. Skopińska-Różewska, B. J. Bałan et al., “Morpho-functional renal alterations in progeny of mice fed Rhodiola kirilowii extracts or epigallocatechin during pregnancy and lactation,” Journal of Medicinal Food, vol. 20, no. 1, pp. 86–92, 2017. View at Publisher · View at Google Scholar