1,938
Views
19
CrossRef citations to date
0
Altmetric
Research Paper

Associations between maternal lifetime stressors and negative events in pregnancy and breast milk-derived extracellular vesicle microRNAs in the programming of intergenerational stress mechanisms (PRISM) pregnancy cohort

ORCID Icon, , ORCID Icon, ORCID Icon, , , & show all
Pages 389-404 | Received 26 May 2020, Accepted 30 Jul 2020, Published online: 25 Aug 2020

References

  • Campbell RK, Devick KL, Coull BA, et al. Prenatal cortisol modifies the association between maternal trauma history and child cognitive development in a sex-specific manner in an urban pregnancy cohort. Stress. 2019;22(2):228–235. doi:10253890.2018.1553950.
  • Tamayo Y Ortiz M, Téllez-Rojo MM, Trejo-Valdivia B, et al. Maternal stress modifies the effect of exposure to lead during pregnancy and 24-month old children’s neurodevelopment. Environ Int. 2017;98:191–197.doi:10.1016/j.envint.2016.11.005.
  • Su Q, Zhang H, Zhang Y, et al. Maternal stress in gestation: Birth outcomes and stress-related hormone response of the neonates. Pediatr Neonatol. 2015;56(6):376–381.  doi:10.1016/j.pedneo.2015.02.002.
  • Keenan K, Hipwell AE, Class QA, et al. Extending the developmental origins of disease model: Impact of preconception stress exposure on offspring neurodevelopment. Dev Psychobiol. 2018;60(7):753–764. doi:10.1002/dev.21773.
  • Rondó PHC, Rezende G, Lemos JO, et al. Maternal stress and distress and child nutritional status. Eur J Clin Nutr. 2013;67(4):348–352.  doi:10.1038/ejcn.2013.28.
  • Lee AG, Chiu Y-HM, Rosa MJ, et al. Association of prenatal and early childhood stress with reduced lung function in 7-year-olds. Ann Allergy, Asthma Immunol. 2017;119(2):153–159. doi:10.1016/j.anai.2017.05.025.
  • Chiu Y-HM, Coull BA, Cohen S, et al. Prenatal and postnatal maternal stress and wheeze in urban children. Am J Respir Crit Care Med. 2012;186(2):147–154. doi:10.1164%2Frccm.201201-0162OC.
  • Rosa MJ, Just AC, Tamayo Y Ortiz M, et al. Prenatal and postnatal stress and wheeze in Mexican children. Ann Allergy, Asthma Immunol. 2016;116(4):306–312.e1. doi:10.1016%2Fj.anai.2015.12.025.
  • Lee A, Chiu Y-HM, Rosa MJ, et al. Prenatal and postnatal stress and asthma in children: Temporal- and sex-specific associations. J Allergy Clin Immunol. 2016;138(3):740–747.e3. doi:10.1016%2Fj.jaci.2016.01.014.
  • Hartwig IRV, Sly PD, Schmidt LA, et al. Prenatal adverse life events increase the risk for atopic diseases in children, which is enhanced in the absence of a maternal atopic predisposition. J Allergy Clin Immunol. 2014;134(1):160–169.e7. doi:10.1016/j.jaci.2014.01.033.
  • Bernt KM, Walker WA. Human milk as a carrier of biochemical messages. Acta Paediatr. 1999;88:27–41. doi:10.1111/j.1651-2227.1999.tb01298.x.
  • Zempleni J, Sukreet S, Zhou F, et al. Milk-derived exosomes and metabolic regulation. Annu Rev Anim Biosci. 2019;7(1):245–262. doi:10.1146/annurev-animal-020518-115300.
  • Ip S, Chung M, Raman G, et al. Breastfeeding and maternal and infant health outcomes in developed countries. Rockville, MD; 2007. (Evidence Report/Technology Assessment No. 153. AHRQ Publication No. 07-E007).
  • Karlsson O, Rodosthenous RS, Jara C, et al. Detection of long non-coding RNAs in human breastmilk extracellular vesicles: Implications for early child development. Epigenetics. 2016;11(10):721–729. doi:10.1080/15592294.2016.1216285
  • Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–297. doi:10.1016/s0092-8674(04)00045-5.
  • Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA Translation and Stability by microRNAs. Annu Rev Biochem. 2010;79(1):351–379. doi:10.1146/annurev-biochem-060308-103103.
  • Kiriakidou M, Nelson PT, Kouranov A, et al. A combined computational-experimental approach predicts human microRNA targets. Genes Dev. 2004;18(10):1165–1178. doi:10.1101/gad.1184704.
  • Alsaweed M, Lai CT, Hartmann PE, et al. Human milk miRNAs primarily originate from the mammary gland resulting in unique miRNA profiles of fractionated milk. Sci Rep. 2016;6(1):20680. doi:10.1038/srep20680.
  • Sauter ER, Reidy D. How exosomes in human breast milk may influence breast cancer risk. Transl Cancer Res. 2017;6(S8):S1384–8.
  • Raposo G, Stoorvogel W. Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383. doi:10.1083/jcb.201211138.
  • Melnik BC, Schmitz G. MicroRNAs: Milk’s epigenetic regulators. Best Pract Res Clin Endocrinol Metab. 2017;31(4):427–442. doi:10.1016/j.beem.2017.10.003.
  • Kahn S, Liao Y, Du X, et al. Exosomal microRNAs in milk from mothers delivering preterm infants survive in vitro digestion and are taken up by human intestinal cells. Mol Nutr Food Res. 2018;62(11):1701050. doi:10.1002/mnfr.201701050.
  • Zhou F, Paz H, Sadri M, et al. Dietary bovine milk exosomes elicit changes in bacterial communities in C57BL/6 mice. Am J Physiol Gastrointest Liver Physiol. 2019;317(5):G618–24. doi:10.1152/ajpgi.00160.2019.
  • Parry H, Mobley C, Mumford P, et al. Bovine milk extracellular vesicles (EVs) modification elicits skeletal muscle growth in rats. Front Physiol. 2019;10. doi.org/10.3389/fphys.2019.00436.
  • Mutai E, Zhou F, Zempleni J Depletion of dietary bovine milk exosomes impairs sensorimotor gating and spatial learning in C57BL/6 mice. FASEB J. 2017;31(S1). doi:10.1096/fasebj.31.1_supplement.150.4.
  • Na RS, GX E, Sun W, et al. Expressional analysis of immune-related miRNAs in breast milk. Genet Mol Res. 2015;14(3):11371–11376. doi:10.4238/2015.september.25.4.
  • Nordgren T, Heires A, Zempleni J, et al. Bovine milk-derived extracellular vesicles enhance inflammation and promote M1 polarization following agricultural dust exposure in mice. J Nutr Biochem. 2019;64:110–120. doi:10.1016/j.jnutbio.2018.10.017.
  • Stremmel W, Weiskirchen R, Melnik BC. Milk exosomes prevent intestinal inflammation in a genetic mouse model of ulcerative colitis: A pilot experiment. Inflamm Intest Dis. 2020;1–7.
  • Bryniarski K, Ptak W, Jayakumar A, et al. Antigen-specific, antibody-coated, exosome-like nanovesicles deliver suppressor T-cell microRNA-150 to effector T cells to inhibit contact sensitivity. J Allergy Clin Immunol. 2013;132(1):170. doi:10.1016/j.jaci.2013.04.048.
  • Zempleni J, Aguilar-Lozano A, Sadri M, et al. Biological activities of extracellular vesicles and their cargos from bovine and human milk in humans and implications for infants. J Nutr. 2017;147(1):3–10. doi:10.3945/jn.116.238949.
  • Kosaka N, Izumi H, Sekine K, et al. MicroRNA as a new immune-regulatory agent in breast milk. Silence. 2010;1(1):7. doi:10.1186/1758-907x-1-7
  • Zhou Q, Li M, Wang X, et al. Immune-related microRNAs are abundant in breast milk exosomes. Int J Biol Sci. 2012;8(1):118–123. doi:10.7150/ijbs.8.118.
  • Alsaweed M, Lai CT, Hartmann PE, et al. Human milk cells contain numerous miRNAs that may change with milk removal and regulate multiple physiological processes. Int J Mol Sci. 2016;17(6):956. doi:10.3390/ijms17060956.
  • Melnik BC, John SM, Carrera-Bastos P, et al. Milk: A postnatal imprinting system stabilizing FoxP3 expression and regulatory T cell differentiation. Clin Transl Allergy. 2016;6(1):18. doi:10.1186/s13601-016-0108-9.
  • Melnik BC, John SM, Schmitz G. Milk: An exosomal microRNA transmitter promoting thymic regulatory T cell maturation preventing the development of atopy? J Transl Med. 2014;12(1):43. doi:10.1186/1479-5876-12-43.
  • Munch EM, Harris RA, Mohammad M, et al. Transcriptome profiling of microRNA by next-gen deep sequencing reveals known and novel miRNA species in the lipid fraction of human breast milk. PLoS One. 2013;8(2):e50564. doi:10.1371/journal.pone.0050564.
  • Kanehisa M, Goto S, Sato Y, et al. Data, information, knowledge and principle: Back to metabolism in KEGG. Nucleic Acids Res. 2014;42(D1):D199–205. doi:10.1093/nar/gkt1076.
  • Brunst KJ, Wright RORJ, DiGioia K, et al. Racial/ethnic and sociodemographic factors associated with micronutrient intakes and inadequacies among pregnant women in an urban US population. Public Health Nutr. 2014;17(9):1960–1970. doi:10.1017/s1368980013003224.
  • Wolfe J, Kimerling R. Gender issues in the assessment of posttraumatic stress disorder. In: Wilson JP, Keane TM, editors. Assessing psychological trauma and PTSD. New York, NY: Guilford Press; 1997. p. 192–238.
  • McHugo GJ, Caspi Y, Kammerer N, et al. The assessment of trauma history in women with co-occurring substance abuse and mental disorders and a history of interpersonal violence. J Behav Heal Serv Res. 2005;32:13–27. doi:10.1007/bf02287261
  • Shalowitz MU, Berry CA, Rasinski KA, et al. A new measure of contemporary life stress: Development, validation, and reliability of the CRISYS. Heal Serv Res. 1998;33:1381–1402.
  • Berry CA, Quinn KA, Portillo N, et al. Reliability and validity of the Spanish version of the Crisis in family systems-revised. Psychol Rep. 2006;98(1):123–132. doi:10.2466/pr0.98.1.123-132.
  • Qiagen. exoEasy maxi kit handbook; 1090293 HB-1953-001. Valencia (CA): Qiagen; 2015.
  • Zhong J, Karlsson O, Wang G, et al. B vitamins attenuate the epigenetic effects of ambient fine particles in a pilot human intervention trial. Proc Natl Acad Sci. 2017;114(13):3503–3508. doi:10.1073/pnas.1618545114.
  • Vlachos IS, Zagganas K, Paraskevopoulou MD, et al. DIANA-miRPath v3.0: Deciphering microRNA function with experimental support. Nucleic Acids Res. 2015;43(W1):W460–6.
  • R Core Team. R: A language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing.; 2015. Available from: https://www.r-project.org/
  • Bowers ME, Yehuda R. Intergenerational transmission of stress in humans. Neuropsychopharmacology. 2016;41(1):232–244. doi:10.1038/npp.2015.247.
  • Hahn-Holbrook J, Le TB, Chung A, et al. Cortisol in human milk predicts child BMI. Obesity. 2016;24(12):2471–2474. doi:10.1002/oby.21682.
  • Glynn LM, Davis EP, Schetter CD, et al. Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Hum Dev. 2007;83(10):675–681. doi:10.1016/j.earlhumdev.2007.01.003.
  • Wiegand C, Heusser P, Klinger C, et al. Stress-associated changes in salivary microRNAs can be detected in response to the trier social stress tesct: An exploratory study. Sci Rep. 2018;8(1):7112. doi:10.1038/s41598-018-25554-x.
  • Misra JR, Irvine KD. The Hippo signaling network and its biological functions. Annu Rev Genet. 2018;52(1):65–87. doi:10.1146/annurev-genet-120417-031621.
  • Ardestani A, Lupse B, Maedler K. Hippo signaling: Key emerging pathway in cellular and whole-body metabolism. Trends Endocrinol Metab. 2018;29(7):492–509. doi:10.1016/j.tem.2018.04.006.
  • Stepan J, Anderzhanova E, Gassen NC. Hippo signaling: Emerging pathway in stress-related psychiatric disorders? Front Psychiatry. 2018;9:715. doi:10.3389/fpsyt.2018.00715.
  • Macfarlane DP, Forbes S, Walker BR. Glucocorticoids and fatty acid metabolism in humans: Fuelling fat redistribution in the metabolic syndrome. J Endocrinol. 2008;197(2):189–204. doi:10.1677/joe-08-0054.
  • Peng S. Foxo in the immune system. Oncogene. 2008;27(16):2337–2344. doi:10.1038/onc.2008.26.
  • Xie S, Chen M, Yan B, et al. Identification of a role for the PI3K/AKT/mTOR signaling pathway in innate immune cells. PLoS One. 2014;9(4):e94496. doi:10.1371/journal.pone.0094496.
  • Garcia DM, Baek D, Shin C, et al. Weak seed-pairing stability and high target-site abundance decrease the proficiency of lsy-6 and other microRNAs. Nat Struct Mol Biol. 2010;18(10):1139–1146. doi:10.1038/nsmb.2115.
  • Zhang Y, Huang B, Wang HY, et al. Emerging role of microRNAs in mTOR signaling. Cell Mol Life Sci. 2017;74(14):2613–2625. doi:10.1007/s00018-017-2485-1.
  • Saxton RA, Sabatini DM. mTOR signaling in growth, metabolism, and disease. Cell. 2017;168(6):960–976.  doi:10.1016/j.cell.2017.02.004.
  • Melnik BC. Milk exosomal miRNAs: Potential drivers of AMPK-To-mTORC1 switching in β-cell de-differentiation of type 2 diabetes mellitus. Nutr. Metab.2019;16(1):1–13. doi:10.1186/s12986-019-0412-1.
  • Melnik BC. Milk—a nutrient system of mammalian evolution promoting mTORC1-dependent translation. Int J Mol Sci. 2015;16(8):17048–17087. doi:10.3390/ijms160817048.
  • Melnik BC, John SM, Schmitz G. Milk is not just food but most likely a genetic transfection system activating mTORC1 signaling for postnatal growth. Nutr J. 2013;12(1):103. doi:10.1186/1475-2891-12-103.
  • Melnik BC, John S, Schmitz G. Milk: An epigenetic amplifier of FTO-mediated transcription? Implications for Western diseases. J Transl Med. 2015;13(1):13. doi:10.1186/s12967-015-0746-z.
  • Ota KT, Liu RJ, Voleti B, et al. REDD1 is essential for stress-induced synaptic loss and depressive behavior. Nat Med. 2014;20(5):531–535. doi:10.1038/nm.3513.
  • Maes M, Song C, Lin A, et al. The effects of psychological stress on humans: Increased production of pro-inflammatory cytokines and th1-like response in stress-induced anxiety. Cytokine. 1998;10(4):313–318. doi:10.1006/cyto.1997.0290.
  • Sun L, Ji S, Xing J. Inhibition of microRNA-155 alleviates neurological dysfunction following transient global ischemia and contribution of neuroinflammation and oxidative stress in the hippocampus. Curr Pharm Des. 2020;25(40):4310–4317. doi:10.2174/1381612825666190926162229.
  • van Herwijnen MJC, Driedonks TAP, Snoek BL, et al. Abundantly present miRNAs in milk-derived extracellular vesicles are conserved between mammals. Front Nutr. 2018;5:81. doi:10.3389/fnut.2018.00081.
  • Zhou Q, Li M, Wang X, et al. Immune-related microRNAs are abundant in breast milk exosomes. Int J Biol Sci. 2012;8(1):118–123. doi:10.7150/ijbs.8.118.
  • Simpson MR, Brede G, Johansen J, et al. Human breast milk miRNA, maternal probiotic supplementation and atopic dermatitis in offspring. PLoS One. 2015;10(12):e0143496. doi:10.1371/journal.pone.0143496.
  • Liao Y, Du X, Li J, et al. Human milk exosomes and their microRNAs survive digestion in vitro and are taken up by human intestinal cells. Mol Nutr Food Res. 2017;61(11):1700082. doi:10.1002/mnfr.201700082.
  • Farr RJ, Januszewski AS, Joglekar MV, et al. A comparative analysis of high-throughput platforms for validation of a circulating microRNA signature in diabetic retinopathy. Sci Rep. 2015;5(1):10375. doi:10.1038/srep10375.
  • Tomé-Carneiro J, Fernández-Alonso N, Tomás-Zapico C, et al. Breast milk microRNAs harsh journey towards potential effects in infant development and maturation. Lipid encapsulation can help. Pharmacol Res. 2018;132:21–32. doi:10.1016/j.phrs.2018.04.003.
  • Small J, Alexander R, Balaj L. Overview of protocols for studying extracellular RNA and extracellular vesicles. In: Methods in Molecular Biology. New York (NY): Humana Press.; 2018. p. 17–21. doi:10.1007%2F978-1-4939-7652-2_2.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.