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Synergistic Effect of Maternal Micronutrient Supplementation on ORFV DNA Vaccine Immune Response in a Pregnant Model

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Abstract

Contagious ecthyma is a contagious zoonotic disease caused by the Orf virus that can infect farm animals and humans, but no vaccine is available for pregnant mothers. Excessive oxidative stress during pregnancy can suppress the vaccine immune response in pregnant mothers; hence, maternal micronutrient supplementation could effectively improve the immune response, health, and oxidative status during pregnancy. In this study, we employed an 8-week-old pregnant rat model to receive a single intramuscular dose of 200 µg of ORF DNA vaccine with or without vitamin E and selenium supplementation to evaluate their effect on immune responses (specific IgG and IgG isotypes), oxidative stress, liver enzymes, and blood glucose levels in maternal-neonatal serum and milk secretions. Additionally, antioxidant-related gene expressions were analyzed in the maternal placenta and pups’ liver. The results showed that supplementation of vitamin E and selenium with ORF DNA vaccination increased the production of specific antibody and IgG isotypes (IgG1 and IgG2a) and reduced the oxidative stress in neonatal-maternal serum and milk compared to both the control group and those vaccinated without supplementation (p < 0.05). Notably, the ORF DNA vaccine did not cause oxidative stress and hepatic damage. However, combined supplementation of vitamin E and selenium with DNA vaccination significantly decreased serum malondialdehyde (MDA) levels and improved the antioxidant-related enzyme activities of glutathione peroxidase (GPX), superoxide dismutase 1 (SOD1), and selenoprotein P (SELP) in the maternal placenta and liver of pups (p < 0.05). In conclusion, maternal supplementation of vitamin E and selenium enhanced the immune responses of the ORF DNA vaccine by mitigating oxidative stress in pregnant rats and could thus be a promising strategy for better health outcomes for both mothers and neonates.

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References

  1. Spyrou V, Valiakos G (2015) Orf virus infection in sheep or goats. Vet Microbiol 181(1–2):178–182. https://doi.org/10.1016/j.vetmic.2015.08.010

    Article  CAS  PubMed  Google Scholar 

  2. Tryland M, Beckmen KB, Burek-Huntington KA, Breines EM, Klein J (2018) Orf virus infection in Alaskan mountain goats, Dall’s sheep, muskoxen, caribou and Sitka black-tailed deer. Acta Vet Scand 60(1):12. https://doi.org/10.1186/s13028-018-0366-8

    Article  PubMed  PubMed Central  Google Scholar 

  3. Andreani J, Fongue J, Bou Khalil JY, David L, Mougari S, Le Bideau M et al (2019) Human infection with Orf virus and description of its whole genome, France, 2017. Emerg Infect Dis 25(12):2197–2204. https://doi.org/10.3201/eid2512.181513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Rajkomar V, Hannah M, Coulson IH, Owen CM (2016) A case of human to human transmission of orf between mother and child. Clin Exp Dermatol 41(1):60–63. https://doi.org/10.1111/ced.12697

    Article  CAS  PubMed  Google Scholar 

  5. Nandi S, De UK, Chowdhury S (2011) Current status of contagious ecthyma or orf disease in goat and sheep-A global perspective. Small Rumin Res 96:73–82. https://doi.org/10.1016/j.smallrumres.2010.11.018

    Article  Google Scholar 

  6. Kumar R, Moudgil P, Grakh K, **dal N, Sharma M, Gupta R (2022) Epidemiology, clinical features, and molecular detection of orf virus in Haryana (India) and its adjoining areas. Trop Anim Health Prod 54:268. https://doi.org/10.1007/s11250-022-03269-6

    Article  PubMed  PubMed Central  Google Scholar 

  7. Arora M, Lakshmi R (2021) Vaccines - safety in pregnancy. Best Pract Res Clin Obstet Gynaecol 76:23–40. https://doi.org/10.1016/j.bpobgyn.2021.02.002

    Article  PubMed  PubMed Central  Google Scholar 

  8. Başkan E, Yilmaz E, Doǧruk S, Adim Ş, Tokgöz N, Tunali Ş (2005) Orf virus infection in pregnancy: a case report. Turkiye Klinikleri J Med Sci 25:137–139

    Google Scholar 

  9. Watson WJ, Meyer MW, Madison DL (1993) Orf virus infection in pregnancy. S D J Med 46(12):423–424

    CAS  PubMed  Google Scholar 

  10. Rodrigues CMC, Plotkin SA (2020) Impact of vaccines; health, economic and social perspectives. Front Microbiol 11:1526. https://doi.org/10.3389/fmicb.2020.01526

    Article  PubMed  PubMed Central  Google Scholar 

  11. Pravieux JJ, Poulet H, Charreyre C, Juillard V (2007) Protection of newborn animals through maternal immunization. J Comp Pathol 137(Suppl 1):S32–S34. https://doi.org/10.1016/j.jcpa.2007.04.009

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chu HY, Englund JA (2014) Maternal immunization. Clin Infect Dis 59(4):560–568. https://doi.org/10.1093/cid/ciu327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Bhanuprakash V, Hosamani M, Venkatesan G, Balamurugan V, Yogisharadhya R, Singh RK (2012) Animal poxvirus vaccines: a comprehensive review. Expert Rev Vaccines 11(11):1355–1374. https://doi.org/10.1586/erv.12.116

    Article  CAS  PubMed  Google Scholar 

  14. Ahmed S, Bo D, Zhao J (2022) Immunocastration with gene vaccine (KISS1) induces a cell-mediated immune response in ram testis: a transcriptome evaluation. Reprod Domest Anim 57(6):653–664

    Article  CAS  PubMed  Google Scholar 

  15. Zhang H, Qian P, Peng B, Shi L, Chen H, Li X (2015) A novel subunit vaccine co-expressing GM-CSF and PCV2b Cap protein enhances protective immunity against porcine circovirus type 2 in piglets. Vaccine 33(21):2449–2456. https://doi.org/10.1016/j.vaccine.2015.03.090

    Article  CAS  PubMed  Google Scholar 

  16. Wang R, Liao X, Fan D, Wang L, Song J, Feng K (2018) Maternal immunization with a DNA vaccine candidate elicits specific passive protection against post-natal Zika virus infection in immunocompetent BALB/c mice. Vaccine 36(24):3522–3532. https://doi.org/10.1016/j.vaccine.2018.04.05

    Article  CAS  PubMed  Google Scholar 

  17. Contreras M, Peres Rubio C, de la Fuente J, Villar M, Merino O, Mosqueda J, Cerón JJ (2020) Changes in serum biomarkers of oxidative stress in cattle vaccinated with tick recombinant antigens: a pilot study. Vaccines (Basel) 9(1):5. https://doi.org/10.3390/vaccines9010005

    Article  CAS  PubMed  Google Scholar 

  18. Pofi R, Tomlinson JW (2020) Glucocorticoids in pregnancy. Obstet Med 13(2):62–69. https://doi.org/10.1177/1753495X19847832

    Article  PubMed  Google Scholar 

  19. Panda BSK, Mohapatra SK, Verma AK, Kamboj A, Alhussien MN, Dang AK (2020) A comparative study on various immunological parameters influencing embryo survivability in crossbred dairy cows. Theriogenology 157:140–148. https://doi.org/10.1016/j.theriogenology.2020.05.041

    Article  CAS  PubMed  Google Scholar 

  20. Uetake K, Akiyama K, Tanaka T (2014) Relationship between stress levels of the antepartum cow and her newborn calf. Anim Sci J 85(1):81–84. https://doi.org/10.1111/asj.12078

    Article  CAS  PubMed  Google Scholar 

  21. Cederberg J, Basu S, Eriksson UJ (2001) Increased rate of lipid peroxidation and protein carbonylation in experimental diabetic pregnancy. Diabetologia 44(6):766–774. https://doi.org/10.1007/s001250051686

    Article  CAS  PubMed  Google Scholar 

  22. Zhao Z, Reece EA (2005) Experimental mechanisms of diabetic embryopathy and strategies for develo** therapeutic interventions. J Soc Gynecol Investig 12(8):549–557. https://doi.org/10.1016/j.jsgi.2005.07.005

    Article  PubMed  Google Scholar 

  23. Spears JW, Weiss WP (2008) Role of antioxidants and trace elements in health and immunity of transition dairy cows. Vet J 176(1):70–76. https://doi.org/10.1016/j.tvjl.2007.12.015

    Article  CAS  PubMed  Google Scholar 

  24. Sordillo LM (2016) Nutritional strategies to optimize dairy cattle. Immunity J Dairy Sci. 99(6):4967–4982. https://doi.org/10.3168/jds.2015-10354

    Article  CAS  PubMed  Google Scholar 

  25. Singh HP, Jain RK, Tiwari D, Mehta MK, Mudgal V (2021) Strategic supplementation of antioxidant micronutrients in peri-parturient murrah buffaloes helps augment the udder health and milk production. Biol Trace Elem Res 199(6):2182–2190. https://doi.org/10.1007/s12011-020-02319-0

    Article  PubMed  Google Scholar 

  26. Mattioli GA, Rosa DE, Turic E, Relling AE, Galarza E, Fazzio LE (2018) Effects of copper and zinc supplementation on weight gain and hematological parameters in pre-weaning calves. Biol Trace Elem Res 185(2):327–331. https://doi.org/10.1007/s12011-017-1239-0

    Article  CAS  PubMed  Google Scholar 

  27. Li D, Cai Z, Pan Z, Yang Y, Zhang J (2021) The effects of vitamin and mineral supplementation on women with gestational diabetes mellitus. BMC Endocr Disord 21(1):106. https://doi.org/10.1186/s12902-021-00712-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Salimi-Jeda A, Abbassi S, Mousavizadeh A (2021) SARS-CoV-2: current trends in emerging variants, pathogenesis, immune responses, potential therapeutic, and vaccine development strategies. Int Immunopharmacol 101(Pt A):108232. https://doi.org/10.1016/j.intimp.2021.108232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Cesur F, Atasever Z, Özoran Y (2023) Impact of vitamin D3 supplementation on COVID-19 vaccine response and immunoglobulin G antibodies in deficient women: a randomized controlled trial. Vaccine 41(17):2860–2867. https://doi.org/10.1016/j.vaccine.2023.03.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Bae M, Kim HJM (2020) The role of vitamin C, vitamin D, and selenium in immune system against COVID-19. Molecules 25(22):5346. https://doi.org/10.3390/molecules25225346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Lotfi F, Akbarzadeh-Khiavi M, Lotfi Z, Rahbarnia L, Safary A, Zarredar H (2021) Micronutrient therapy and effective immune response: a promising approach for management of COVID-19. Infection 49(6):1133–1147. https://doi.org/10.1007/s15010-021-01644-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ahmed S, Jiang X, Liu G, Yang H, Sadiq A, Yi D (2023) The protective role of maternal genetic immunization on maternal-fetal health and welfare. Int J Gynaecol Obstet 163(3):763–777. https://doi.org/10.1002/ijgo.14853

    Article  CAS  PubMed  Google Scholar 

  33. Gázquez A, Sánchez-Campillo M, Arnao MB, Barranco A, Rueda R, Jensen SK (2023) Natural vitamin E supplementation during pregnancy in rats increases RRR-α-tocopherol stereoisomer proportion and enhances fetal antioxidant capacity, compared to synthetic vitamin E administration. Ann Nutr Metab 79:60–69

    Article  Google Scholar 

  34. Anan Y, Ogra Y, Somekawa L, Suzuki KT (2009) Effects of chemical species of selenium on maternal transfer during pregnancy and lactation. Life Sci 84:888–893

    Article  CAS  PubMed  Google Scholar 

  35. Mohd Aftab S, Usama A, Asad A, Farogh A, Md (2021) Faheem H. role of vitamin E in pregnancy. In: Pınar E, Júlia Scherer S (eds.) Vitamin E in Health and Disease. Rijeka: IntechOpen, p Ch 6

  36. Lei XG, Combs GF Jr, Sunde RA, Caton JS, Arthington JD, Vatamaniuk MZ (2022) Dietary selenium across species. Ann Rev Nutr 42:337–75

    Article  CAS  Google Scholar 

  37. Wassie T, Fanmei Z, Jiang X, Liu G, Girmay S, Min Z (2019) Recombinant B2L and Kisspeptin-54 DNA vaccine induces immunity against Orf virus and inhibits spermatogenesis in rats. Sci Rep 9(1):16262. https://doi.org/10.1038/s41598-019-52744-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shan C, **e X, Luo H, Muruato AE, Liu Y, Wakamiya M (2019) Maternal vaccination and protective immunity against Zika virus vertical transmission. Nat Commun 10(1):5677. https://doi.org/10.1038/s41467-019-13589-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Saouli A, Adjroud O, Ncir M, Bachir A, El Feki A (2023) Attenuating effects of selenium and zinc against hexavalent chromium-induced oxidative stress, hormonal instability, and placenta damage in preimplanted rats. Environ Sci Pollut Res Int 30(21):60050–60079. https://doi.org/10.1007/s11356-023-26700-3

    Article  CAS  PubMed  Google Scholar 

  40. Pang W, Zhang Q, Guo K, He Y, Fu M, Xu X (2017) Prokaryotic expression of B2L protein of orf virus and establishment of indirect ELISA for detection of antibodies against orf virus. Chinese Veterinary Science/Zhongguo Shouyi Kexue 47:150–156

    Google Scholar 

  41. Coradduzza E, Sanna D, Scarpa F, Azzena I, Fiori MS, Scivoli R (2022) A deeper insight into evolutionary patterns and phylogenetic history of ORF virus through the whole genome sequencing of the first Italian strains. Viruses 14(7):1473. https://doi.org/10.3390/v14071473

    Article  PubMed  PubMed Central  Google Scholar 

  42. Shaukat A, Shaukat I, Rajput SA, Shukat R, Hanif S, Huang S (2022) Icariin alleviates Escherichia coli lipopolysaccharide-mediated endometritis in mice by inhibiting inflammation and oxidative stress. Int J Mol Sci 23(18):10219. https://doi.org/10.3390/ijms231810219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Schumann G, Bonora R, Ceriotti F, Férard G, Ferrero CA, Franck PF (2002) IFCC primary reference procedures for the measurement of catalytic activity concentrations of enzymes at 37 degrees C. International Federation of Clinical Chemistry and Laboratory Medicine. Part 5. Reference procedure for the measurement of catalytic concentration of aspartate aminotransferase. Clin Chem Lab Med 40(7):734–738. https://doi.org/10.1515/CCLM.2002.126

    Article  CAS  PubMed  Google Scholar 

  44. Shaukat A, Shaukat I, Rajput SA, Shukat R, Hanif S, Jiang K (2021) Ginsenoside Rb1 protects from Staphylococcus aureus-induced oxidative damage and apoptosis through endoplasmic reticulum-stress and death receptor-mediated pathways. Ecotoxicol Environ Saf 219:112353. https://doi.org/10.1016/j.ecoenv.2021.112353

    Article  CAS  PubMed  Google Scholar 

  45. Yu W, Hu X, Cao B (2022) Viral infections during pregnancy: the big challenge threatening maternal and fetal health. Matern Fetal Med 4:72–86. https://doi.org/10.1097/FM9.0000000000000133

    Article  CAS  PubMed  Google Scholar 

  46. Kumar M, Saadaoui M, Al Khodor S (2022) Infections and pregnancy: effects on maternal and child health. Front Cell Infect Microbiol 12:873253. https://doi.org/10.3389/fcimb.2022.873253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hosamani M, Scagliarini A, Bhanuprakash V, McInnes CJ, Singh RK (2009) Orf: an update on current research and future perspectives. Expert Rev of Anti-infective Therapy 7:879–893

    Article  PubMed  Google Scholar 

  48. Bala JA, Balakrishnan KN, Abdullah AA, Kimmy T, Abba Y, Bin Mohamed R (2018) Dermatopathology of Orf virus (Malaysian Isolates) in mice experimentally inoculated at different sites with and without dexamethasone administration. J Pathog 2018:9207576. https://doi.org/10.1155/2018/9207576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bukar AM, Jesse FFA, Abdullah CAC, Noordin MM, Lawan Z, Mangga HK (2021) Immunomodulatory strategies for parapoxvirus: current status and future approaches for the development of vaccines against Orf virus infection. Vaccines 9(11):134. https://doi.org/10.3390/vaccines9111341

    Article  CAS  Google Scholar 

  50. Van Rompay KKA, Keesler RI, Ardeshir A, Watanabe J, Usachenko J, Singapuri A et al (2019) DNA vaccination before conception protects Zika virus–exposed pregnant macaques against prolonged viremia and improves fetal outcomes. Sci Transl Med 11(523):eaay2736. https://doi.org/10.1126/scitranslmed.aay2736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Kharbanda EO, Vazquez-Benitez G (2022) COVID-19 mRNA vaccines during pregnancy: new evidence to help address vaccine hesitancy. JAMA 327(15):1451–1453. https://doi.org/10.1001/jama.2022.2459

    Article  CAS  PubMed  Google Scholar 

  52. Hussain T, Murtaza G, Metwally E, Kalhoro DH, Kalhoro MS, Rahu BA et al (2021) The role of oxidative stress and antioxidant balance in pregnancy. Mediators Inflamm 2021:9962860. https://doi.org/10.1155/2021/9962860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Arogbokun O, Rosen E, Keil AP, Milne GL, Barrett E, Nguyen R (2021) Maternal oxidative stress biomarkers in pregnancy and child growth from birth to age 6. Clin Endocrinol Metab 106(5):1427–1436. https://doi.org/10.1210/clinem/dgab018

    Article  Google Scholar 

  54. Wang Y, Zhao K, Song D, Du L, Wang X, Gao F (2022) Evaluation of the immune response afforded by combined immunization with Orf virus DNA and subunit vaccine in mice. Vaccines 10(9):1499. https://doi.org/10.3390/vaccines10091499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Shao H-Y, Chen Y-C, Chung N-H, Lu Y-J, Chang C-K, Yu S-L (2018) Maternal immunization with a recombinant adenovirus-expressing fusion protein protects neonatal cotton rats from respiratory syncytia virus infection by transferring antibodies via breast milk and placenta. Virology 521:181–189. https://doi.org/10.1016/j.virol.2018.06.009

    Article  CAS  PubMed  Google Scholar 

  56. Narayanaswamy V, Pentecost BT, Schoen CN, Alfandari D, Schneider SS, Baker R, Arcaro KF (2022) Neutralizing antibodies and cytokines in breast milk after coronavirus disease 2019 (COVID-19) mRNA vaccination. Obstet Gynecol 2:181–191. https://doi.org/10.1097/AOG.0000000000004661

    Article  CAS  Google Scholar 

  57. Caudill C, Perry JL, Iliadis K, Tessema AT, Lee BJ, Mecham BS (2021) Transdermal vaccination via 3D-printed microneedles induces potent humoral and cellular immunity. Proc Natl Acad Sci USA 118(39):e2102595118. https://doi.org/10.1073/pnas.2102595118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hurley WL, Theil PK (2011) Perspectives on immunoglobulins in colostrum and milk. Nutrients 3(4):442–474. https://doi.org/10.3390/nu3040442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Abu-Raya B, Michalski C, Sadarangani M, Lavoie PM (2020) Maternal immunological adaptation during normal pregnancy. Front Immunol 11:575197. https://doi.org/10.3389/fimmu.2020.575197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Wang W, Sung N, Gilman-Sachs A, Kwak-Kim J (2020) T helper (Th) cell profiles in pregnancy and recurrent pregnancy losses: Th1/Th2/Th9/Th17/Th22/Tfh Cells. Front Immunol 11:2025. https://doi.org/10.3389/fimmu.2020.02025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Challis JR, Lockwood CJ, Myatt L, Norman JE, Strauss JF, Petraglia F (2009) Inflammation and pregnancy. Reprod Sci 16:206–215. https://doi.org/10.1177/1933719108329095

    Article  CAS  PubMed  Google Scholar 

  62. Shinde S, Wang D, Yussuf MH, Mwanyika-Sando M, Aboud S, Fawzi WW (2022) Micronutrient supplementation for pregnant and lactating women to improve maternal and infant nutritional status in low- and middle-income countries: protocol for a systematic review and meta-analysis. JMIR Res Protoc 11(8):e40134. https://doi.org/10.2196/40134

    Article  PubMed  PubMed Central  Google Scholar 

  63. Mousa A, Naqash A, Lim S (2019) Macronutrient and micronutrient intake during pregnancy: an overview of recent evidence. Nutrients 11(2):443. https://doi.org/10.3390/nu11020443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Fernandez GJ, Ramírez-Mejía JM, Castillo JA, Urcuqui-Inchima S (2023) Vitamin D modulates expression of antimicrobial peptides and proinflammatory cytokines to restrict Zika virus infection in macrophages. Int Immunopharmacol 119:110232. https://doi.org/10.1016/j.intimp.2023.110232

    Article  CAS  PubMed  Google Scholar 

  65. Zhang W, Zhang R, Wang T, Jiang H, Guo M, Zhou E (2014) Selenium inhibits LPS-induced pro-inflammatory gene expression by modulating MAPK and NF-κB signaling pathways in mouse mammary epithelial cells in primary culture. Inflammation 37(2):478–485. https://doi.org/10.1007/s10753-013-9761-5

    Article  CAS  PubMed  Google Scholar 

  66. Mou D, Ding D, Yan H, Qin B, Dong Y, Li Z (2020) Maternal supplementation of organic selenium during gestation improves sows and offspring antioxidant capacity and inflammatory status and promotes embryo survival. Food Funct 11(9):7748–7761. https://doi.org/10.1039/d0fo00832j

    Article  CAS  PubMed  Google Scholar 

  67. Wang N, Liang H, Zen K (2014) Molecular mechanisms that influence the macrophage M1–M2 polarization balance. Front Immunol 5:614. https://doi.org/10.3389/fimmu.2014.00614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zhu J (2015) T helper 2 (Th2) cell differentiation, type 2 innate lymphoid cell (ILC2) development and regulation of interleukin-4 (IL-4) and IL-13 production. Cytokine 75(1):14–24. https://doi.org/10.1016/j.cyto.2015.05.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Laudenbach M, Tucker A, Runyon S, Carroll F, Pravetoni M (2015) The frequency of early-activated hapten-specific B cell subsets predicts the efficacy of vaccines for nicotine dependence. Vaccine 33(46):6332–6339. https://doi.org/10.1016/j.vaccine.2015.09.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Weinstein JS, Herman EI, Lainez B, Licona-Limón P, Esplugues E, Flavell R, Craft J (2016) TFH cells progressively differentiate to regulate the germinal center response. Nat Immunol 17(10):1197–1205. https://doi.org/10.1038/ni.3554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Tanaka T, Narazaki M, Kishimoto T (2014) IL-6 in inflammation, immunity, and disease. Cold Spring Harb Perspect Biol 6(10):a016295. https://doi.org/10.1101/cshperspect.a016295

    Article  PubMed  PubMed Central  Google Scholar 

  72. Leal IS, Flórido M, Andersen P, Appelberg R (2001) Interleukin-6 regulates the phenotype of the immune response to a tuberculosis subunit vaccine. Immunology 103(3):375–381. https://doi.org/10.1046/j.1365-2567.2001.01244.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Grases-Pintó B, Abril-Gil M, Torres-Castro P, Castell M, Rodríguez-Lagunas MJ, Pérez-Cano FJ, Franch À (2021) Rat milk and plasma immunological profile throughout lactation. Nutrients 13(4):1257. https://doi.org/10.3390/nu13041257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Torres-Castro P, Grases-Pintó B, Abril-Gil M, Castell M, Rodríguez-Lagunas MJ, Pérez-Cano FJ, Franch À (2020) Modulation of the systemic immune response in suckling rats by breast milk TGF-β2, EGF and FGF21 supplementation. Nutrients 12(6):1888. https://doi.org/10.3390/nu12061888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Okala SG, Darboe MK, Sosseh F, Sonko B, Faye-Joof T, Prentice AM, Moore SE (2019) Impact of nutritional supplementation during pregnancy on antibody responses to diphtheria-tetanus-pertussis vaccination in infants: a randomised trial in The Gambia. PLoS Med 16(8):e1002854. https://doi.org/10.1371/journal.pmed.1002854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Patel S, Akalkotkar A, Bivona JJ III, Lee J-Y, Park Y-K, Yu M et al (2016) Vitamin A or E and a catechin synergize as vaccine adjuvant to enhance immune responses in mice by induction of early interleukin-15 but not interleukin-1β responses. Immunology 148(4):352–362. https://doi.org/10.1111/imm.12614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Lewis ED, Meydani SN, Wu D (2019) Regulatory role of vitamin E in the immune system and inflammation. IUBMB Life 71(4):487–494. https://doi.org/10.1002/iub.1976

    Article  CAS  PubMed  Google Scholar 

  78. Pieczyńska J, Grajeta H (2015) The role of selenium in human conception and pregnancy. J Trace Elem Med Biol 29:31–38. https://doi.org/10.1016/j.jtemb.2014.07.003

    Article  CAS  PubMed  Google Scholar 

  79. Gagné A, Wei SQ, Fraser WD, Julien P (2009) Absorption, transport, and bioavailability of vitamin E and its role in pregnant women. J Obstet Gynaecol Can 31(3):210–217. https://doi.org/10.1016/s1701-2163(16)34118-4

    Article  PubMed  Google Scholar 

  80. Rumbold A, Middleton P, Pan N, Crowther CA (2011) Vitamin supplementation for preventing miscarriage. Cochrane Database Syst Rev 1:CD004073. https://doi.org/10.1002/14651858.CD004073.pub3

    Article  Google Scholar 

  81. Shamim AA, Schulze K, Merrill RD, Kabir A, Christian P, Shaikh S et al (2015) First-trimester plasma tocopherols are associated with risk of miscarriage in rural Bangladesh. Am J Clin Nutr 101(2):294–301. https://doi.org/10.3945/ajcn.114.094920

    Article  CAS  PubMed  Google Scholar 

  82. Gombart AF, Pierre A, Maggini S (2020) A review of micronutrients and the immune system–working in harmony to reduce the risk of infection. Nutrients 12(1):236. https://doi.org/10.3390/nu12010236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Albers R, Bourdet-Sicard R, Braun D, Calder PC, Herz U, Lambert C et al (2013) Monitoring immune modulation by nutrition in the general population: identifying and substantiating effects on human health. Br J Nutr 110(Suppl 2):S1–S30. https://doi.org/10.1017/S0007114513001505

    Article  CAS  PubMed  Google Scholar 

  84. Sterndale S, Broomfield S, Currie A, Hancock S, Kearney GA, Lei J (2018) Supplementation of Merino ewes with vitamin E plus selenium increases α-tocopherol and selenium concentrations in plasma of the lamb but does not improve their immune function. Animal 12(5):998–1006. https://doi.org/10.1017/S1751731117002300

    Article  CAS  PubMed  Google Scholar 

  85. Labunskyy VM, Hatfield DL, Gladyshev VN (2014) Selenoproteins: molecular pathways and physiological roles. Physiol Rev 94(3):739–777. https://doi.org/10.1152/physrev.00039.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Cox AG, Tsomides A, Kim AJ, Saunders D, Hwang KL, Evason KJ (2016) Selenoprotein H is an essential regulator of redox homeostasis that cooperates with p53 in development and tumorigenesis. Proc Natl Acad Sci USA 113(38):E5562–E5571. https://doi.org/10.1073/pnas.1600204113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Rizvi S, Raza ST, Ahmed F, Ahmad A, Abbas S, Mahdi F (2014) The role of vitamin E in human health and some diseases. Sultan Qaboos Univ Med J 14(2):e157–e165

    PubMed  PubMed Central  Google Scholar 

  88. Traber MG, Atkinson J (2007) Vitamin E, antioxidant and nothing more. Free Radic Biol Med 43(1):4–15. https://doi.org/10.1016/j.freeradbiomed.2007.03.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Wang M, Li Y, Molenaar A, Li Q, Cao Y, Shen Y (2021) Vitamin E and selenium supplementation synergistically alleviate the injury induced by hydrogen peroxide in bovine granulosa cells. Theriogenology 170:91–106. https://doi.org/10.1016/j.theriogenology.2021.04.015

    Article  CAS  PubMed  Google Scholar 

  90. Dimri U, Ranjan R, Sharma MC, Varshney VP (2010) Effect of vitamin E and selenium supplementation on oxidative stress indices and cortisol level in blood in water buffaloes during pregnancy and early postpartum period. Trop Anim Health Prod 42:405–410

    Article  PubMed  Google Scholar 

  91. Guney M, Erdemoglu E, Mungan T (2011) Selenium–vitamin E combination and melatonin modulates diabetes-induced blood oxidative damage and fetal outcomes in pregnant rats. Biol Trace Elem Res 143(2):1091–1102. https://doi.org/10.1007/s12011-010-8951-3

    Article  CAS  PubMed  Google Scholar 

  92. Bermejo-Haro MY, Camacho-Pacheco RT, Brito-Pérez Y, Mancilla-Herrera I (2023) The hormonal physiology of immune components in breast milk and their impact on the infant immune response. Mol Cell Endocrinol 572:111956. https://doi.org/10.1016/j.mce.2023.111956

    Article  CAS  PubMed  Google Scholar 

  93. Ames SR, Lotoski LC, Azad MB (2023) Comparing early life nutritional sources and human milk feeding practices: personalized and dynamic nutrition supports infant gut microbiome development and immune system maturation. Gut Microbes 15(1):2190305. https://doi.org/10.1080/19490976.2023.2190305

    Article  PubMed  PubMed Central  Google Scholar 

  94. Saran Netto A, Salles MSV, Roma Júnior LC, Cozzolino SMF, Gonçalves MTM, Freitas Júnior JE, Zanetti MA (2019) Increasing selenium and vitamin E in dairy cow milk improves the quality of the milk as food for children. Nutrients 11(6):1218. https://doi.org/10.3390/nu11061218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Nan YM, Wu WJ, Fu N, Liang BL, Wang RQ, Li LX (2009) Antioxidants vitamin E and 1-aminobenzotriazole prevent experimental non-alcoholic steatohepatitis in mice. Scand J Gastroenterol 44(9):1121–1131. https://doi.org/10.1080/00365520903114912

    Article  CAS  PubMed  Google Scholar 

  96. Ryan MJ, Dudash HJ, Docherty M, Geronilla KB, Baker BA, Haff GG (2010) Vitamin E and C supplementation reduces oxidative stress, improves antioxidant enzymes and positive muscle work in chronically loaded muscles of aged rats. Exp Gerontol 45(11):882–895. https://doi.org/10.1016/j.exger.2010.08.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Hofstee P, McKeating DR, Bartho LA, Anderson ST, Perkins AV, Cuffe JS (2020) Maternal selenium deficiency in mice alters offspring glucose metabolism and thyroid status in a sexually dimorphic manner. Nutrients 12(1):267. https://doi.org/10.3390/nu12010267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Wu Y, Zhang Q, **ao X (2021) The effect and potential mechanism of maternal micronutrient intake on offspring glucose metabolism: an emerging field. Front Nutr 8:763809. https://doi.org/10.3389/fnut.2021.763809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We acknowledge our reviewers and colleagues for their valuable comments, and suggestions, for the manuscript improvement. A special thanks to Dr. Teketay Wassie (School of Medicine, Oregon Health & Science University, USA) for proofreading and English language editing.

Funding

This work was supported by Scientific and Technological Innovation 2030—Major Agricultural Biological Breeding Project (2022ZD0401403), China Agriculture Research System of MOF and MARA (No. CARS-38), Germplasm Innovation Project of Prolificacy Sheep in ** Jiang

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    X. P and G. L: Conceptualization, Data curation, Resources, Supervision, and Final review & editing; S. A: Experimentation, Data curation, Methodology, and Writing – original draft; D.Y, M. A and U. F: Formal analysis, and Methodology; S. Y, L. Y and A. S: Data Analysis, Visualization, and Writing – review & editing. H. Y and W. X: Data Analysis, Validation and Writing – review & editing.

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    Correspondence to Xun** Jiang.

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    Ahmed, S., Liu, G., Sadiq, A. et al. Synergistic Effect of Maternal Micronutrient Supplementation on ORFV DNA Vaccine Immune Response in a Pregnant Model. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-024-04263-9

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