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Research Paper

Nitric oxide-related gene and microRNA expression in peripheral blood in pregnancy vary by self-reported race

, , , & ORCID Icon
Pages 731-745 | Received 23 Mar 2021, Accepted 15 Jul 2021, Published online: 24 Jul 2021

References

  • Manuck TA. Racial and ethnic differences in preterm birth: a complex, multifactorial problem. Semin Perinatol. 2017;41(8):511–518.
  • Martin JA, Hamilton BE, Osterman MJK, et al. Births: final data for 2018. November 27, 2019.
  • Martin JA, Hamilton BE, Osterman MJK, et al. Births: final data for 2018. Natl Vital Stat Rep. 2019;68(13):1–47.
  • Manuck TA, Rice MM, Bailit JL, et al. Preterm neonatal morbidity and mortality by gestational age: a contemporary cohort. Am J Obstet Gynecol. 2016;215(1):103e101–103 e114.
  • Manuck TA, Sheng X, Yoder BA, et al. Correlation between initial neonatal and early childhood outcomes following preterm birth. Am J Obstet Gynecol. 2014;210(5):426 e421–429.
  • Natarajan G, Shankaran S. Short- and Long-Term outcomes of moderate and late preterm infants. Am J Perinatol. 2016;33(3):305–317.
  • Bodeau-Livinec F, Marlow N, Ancel PY, et al. Impact of intensive care practices on short-term and long-term outcomes for extremely preterm infants: comparison between the British Isles and France. Pediatrics. 2008;122(5):e1014–1021.
  • Vohr B. Long-term outcomes of moderately preterm, late preterm, and early term infants. Clin Perinatol. 2013;40(4):739–751.
  • Singh GK, Siahpush M, Liu L, et al. Racial/Ethnic, nativity, and sociodemographic disparities in maternal hypertension in the United States, 2014-2015. Int J Hypertens. 2018;2018:7897189.
  • Thoma ME, Drew LB, Hirai AH, et al. Black-White disparities in preterm birth: geographic, social, and health determinants. Am J Prev Med. 2019;57(5):675–686.
  • Burris HH, Lorch SA, Kirpalani H, et al. Racial disparities in preterm birth in USA: a biosensor of physical and social environmental exposures. Arch Dis Child. 2019;104(10):931–935.
  • DeFranco EA, Hall ES, Muglia LJ. Racial disparity in previable birth. Am J Obstet Gynecol. 2016;214(3):394 e391–397.
  • Lo J, Mission JF, Caughey AB. Hypertensive disease of pregnancy and maternal mortality. Curr Opin Obstet Gynecol. 2013;25(2):124–132.
  • Lawn J, Blencowe H, Waiswa P, et al. Lancet ending preventable stillbirths series study group; lancet stillbirth epidemiology investigator group. stillbirths: rates, risk factors, and acceleration towards 2030. Lancet. 2016;387(10018):587–603.
  • Bujold E, Roberge S, Lacasse Y, et al. Prevention of preeclampsia and intrauterine growth restriction with aspirin started in early pregnancy: a meta-analysis. Obstet Gynecol. 2010;116(2.1):402–414.
  • Dole N, Savitz DA, Hertz-Picciotto I, et al. Maternal stress and preterm birth. Am J Epidemiol. 2003;157(1):14–24.
  • Dominguez TP, Dunkel-Schetter C, Glynn LM, et al. Racial differences in birth outcomes: the role of general, pregnancy, and racism stress. Health Psychol. 2008;27(2):194–203.
  • Dole N, Savitz DA, Siega-Riz AM, et al. Psychosocial factors and preterm birth among African American and white women in central North Carolina. Am J Public Health. 2004;94(8):1358–1365.
  • Chambers BD, Baer RJ, McLemore MR, et al. Using Index of concentration at the extremes as indicators of structural racism to evaluate the association with preterm birth and infant mortality-California, 2011-2012. J Urban Health. 2019;96(2):159–170.
  • Bailey ZD, Krieger N, Agenor M, et al. Structural racism and health inequities in the USA: evidence and interventions. Lancet. 2017;389(10077):1453–1463.
  • Paradies Y, Ben J, Denson N, et al. Racism as a determinant of health: a systematic review and meta-Analysis. PLoS One. 2015;10(9):e0138511.
  • Sladek SM, Magness RR, Conrad KP. Nitric oxide and pregnancy. Am J Physiol. 1997;272(2 Pt 2):R441–463.
  • Selles J, Polini N, Alvarez C, et al. Nongenomic action of progesterone in rat aorta: role of nitric oxide and prostaglandins. Cell Signal. 2002;14(5):431–436.
  • Simoncini T, Mannella P, Fornari L, et al. Differential signal transduction of progesterone and medroxyprogesterone acetate in human endothelial cells. Endocrinology. 2004;145(12):5745–5756.
  • Simoncini T, Caruso A, Garibaldi S, et al. Activation of nitric oxide synthesis in human endothelial cells using nomegestrol acetate. Obstet Gynecol. 2006;108(4):969–978.
  • Pang Y, Dong J, Thomas P. Progesterone increases nitric oxide synthesis in human vascular endothelial cells through activation of membrane progesterone receptor-alpha. Am J Physiol Endocrinol Metab. 2015;308(10):E899–911.
  • Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J. 2012;33(7):829–837d.
  • Manuck TA, Watkins WS, Moore B, et al. Pharmacogenomics of 17-alpha hydroxyprogesterone caproate for recurrent preterm birth prevention. Am J Obstet Gynecol. 2014;210(4):321e321–321 e321.
  • Manuck TA, Watkins WS, Esplin MS, et al. Pharmacogenomics of 17-alpha hydroxyprogesterone caproate for recurrent preterm birth: a case-control study. BJOG. 2018;125(3):343–350.
  • Manuck TA, Smeester L, Martin EM, et al. Epigenetic regulation of the nitric oxide pathway, 17-alpha hydroxyprogesterone caproate, and recurrent preterm birth. Am J Perinatol. 2018;35(8):721–728.
  • Jiang F, Li J, Wu G, et al. Upregulation of microRNA335 and microRNA584 contributes to the pathogenesis of severe preeclampsia through downregulation of endothelial nitric oxide synthase. Mol Med Rep. 2015;12(4):5383–5390.
  • O’Brien J, Hayder H, Zayed Y, et al. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (Lausanne). 2018;9:402. doi: https://doi.org/10.3389/fendo.2018.00402.eCollection 2018.
  • Vasudevan S. Posttranscriptional upregulation by microRNAs. Wiley Interdiscip Rev RNA. 2012;3(3):311–330.
  • Giurgescu C, Engeland CG, Templin TN, et al. Racial discrimination predicts greater systemic inflammation in pregnant African American women. Appl Nurs Res. 2016;32:98–103.
  • Giurgescu C, Zenk SN, Engeland CG, et al. Racial discrimination and psychological wellbeing of pregnant women. MCN Am J Matern Child Nurs. 2017;42(1):8–13.
  • Szanton SL, Rifkind JM, Mohanty JG, et al. Racial discrimination is associated with a measure of red blood cell oxidative stress: a potential pathway for racial health disparities. Int J Behav Med. 2012;19(4):489–495.
  • Committee opinion no 611: method for estimating due date. Obstet Gynecol. 2014;124(4):863–866.
  • Harris PA, Taylor R, Thielke R, et al. Research electronic data capture (REDCap)–a metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform. 2009;42(2):377–381.
  • Leone A, Roca MS, Ciardiello C, et al. Oxidative stress gene expression profile correlates with cancer patient poor prognosis: identification of crucial pathways might select novel therapeutic approaches. Oxid Med Cell Longev. 2017;2017:2597581.
  • Sheikh IA, Ahmad E, Jamal MS, et al. Spontaneous preterm birth and single nucleotide gene polymorphisms: a recent update. BMC Genomics. 2016;17(Suppl 9):759.
  • Shetty GA, Hattiangady B, Upadhya D, et al. Chronic oxidative stress, mitochondrial dysfunction, Nrf2 activation and inflammation in the hippocampus accompany heightened systemic inflammation and oxidative stress in an animal model of gulf war illness. Front Mol Neurosci. 2017;10:182.
  • Birben E, Sahiner UM, Sackesen C, et al. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012;5(1):9–19.
  • Musolino C, Allegra A, Innao V, et al. Inflammatory and Anti-Inflammatory equilibrium, proliferative and antiproliferative balance: the role of cytokines in multiple Myeloma. Mediators Inflamm. 2017;2017:1852517.
  • Carey AJ, Tan CK, Ulett GC. Infection-induced IL-10 and JAK-STAT: a review of the molecular circuitry controlling immune hyperactivity in response to pathogenic microbes. JAKSTAT. 2012;1(3):159–167.
  • Agarwal A, Aponte-Mellado A, Premkumar BJ, et al. The effects of oxidative stress on female reproduction: a review. Reprod Biol Endocrinol. 2012;10(1):49.
  • Lu TP, Lee CY, Tsai MH, et al. miRSystem: an integrated system for characterizing enriched functions and pathways of microRNA targets. PLoS One. 2012;7(8):e42390.
  • Rager JE, Auerbach SS, Chappell GA, et al. Benchmark dose modeling estimates of the concentrations of inorganic arsenic that induce changes to the neonatal transcriptome, proteome, and epigenome in a pregnancy cohort. Chem Res Toxicol. 2017;30(10):1911–1920.
  • Rager JE, Bailey KA, Smeester L, et al. Prenatal arsenic exposure and the epigenome: altered microRNAs associated with innate and adaptive immune signaling in newborn cord blood. Environ Mol Mutagen. 2014;55(3):196–208.
  • Rager JE, Moeller BC, Miller SK, et al. Formaldehyde-associated changes in microRNAs: tissue and temporal specificity in the rat nose, white blood cells, and bone marrow. Toxicol Sci. 2014;138(1):36–46.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550.
  • Costa-Silva J, Domingues D, Lopes FM. RNA-Seq differential expression analysis: an extended review and a software tool. PLoS One. 2017;12(12):e0190152.
  • Molania R, Gagnon-Bartsch JA, Dobrovic A, et al. A new normalization for Nanostring nCounter gene expression data. Nucleic Acids Res. 2019;47(12):6073–6083.
  • Gagnon-Bartsch JA, Speed TP. Using control genes to correct for unwanted variation in microarray data. Biostatistics. 2012;13(3):539–552.
  • De Magalhaes JP, Curado J, Church GM. Meta-analysis of age-related gene expression profiles identifies common signatures of aging. Bioinformatics. 2009;25(7):875–881.
  • Lian IA, Langaas M, Moses E, et al. Differential gene expression at the maternal-fetal interface in preeclampsia is influenced by gestational age. PLoS One. 2013;8(7):e69848.
  • Weissenbacher T, Laubender RP, Witkin SS, et al. Influence of maternal age, gestational age and fetal gender on expression of immune mediators in amniotic fluid. BMC Res Notes. 2012;5(1):375.
  • Menon R, Debnath C, Lai A, et al. Circulating exosomal miRNA profile during term and preterm birth pregnancies: a longitudinal study. Endocrinology. 2019;160(2):249–275.
  • miRSystem - An integrated miRNA analytical system for characterizing enriched functions and pathways. 2020. cited 2020 April 27. http://mirsystem.cgm.ntu.edu.tw/index.php.
  • Levine M, Ensom MH. Post hoc power analysis: an idea whose time has passed? Pharmacotherapy. 2001;21(4):405–409.
  • Sluiter F, Incollingo Rodriguez AC, Nephew BC, et al. Pregnancy associated epigenetic markers of inflammation predict depression and anxiety symptoms in response to discrimination. Neurobiol Stress. 2020;13:100273.
  • Carroll JE, Rentscher KE, Cole SW, et al. Sleep disturbances and inflammatory gene expression among pregnant women: differential responses by race. Brain Behav Immun. 2020;88:654–660.
  • Fortunato SJ, Lombardi SJ, Menon R. Racial disparity in membrane response to infectious stimuli: a possible explanation for observed differences in the incidence of prematurity. Community award paper. Am J Obstet Gynecol. 2004;190(6):1557–1562. discussion 1562-1553.
  • Diaz G, Zamboni F, Tice A, et al. Integrated ordination of miRNA and mRNA expression profiles. BMC Genomics. 2015;16(1):767.
  • Cascione L, Gasparini P, Lovat F, et al. Integrated microRNA and mRNA signatures associated with survival in triple negative breast cancer. PLoS One. 2013;8(2):e55910.
  • Nunez-Iglesias J, Liu CC, Morgan TE, et al. Joint genome-wide profiling of miRNA and mRNA expression in Alzheimer’s disease cortex reveals altered miRNA regulation. PLoS One. 2010;5(2):e8898.
  • Ekeke P, Mendez DD, Yanowitz TD, et al. Racial Differences in the Biochemical Effects of Stress in Pregnancy. Int J Environ Res Public Health. 2020;17(19):6941.
  • Menon R, Williams SM, Fortunato SJ. Amniotic fluid interleukin-1beta and interleukin-8 concentrations: racial disparity in preterm birth. Reprod Sci. 2007;14(3):253–259.
  • Menon R, Dunlop AL, Kramer MR, et al. An overview of racial disparities in preterm birth rates: caused by infection or inflammatory response? Acta Obstet Gynecol Scand. 2011;90(12):1325–1331.
  • Okabe H, Makino S, Kato K, et al. The effect of progesterone on genes involved in preterm labor. J Reprod Immunol. 2014;104-105:80–91.
  • Capece A, Vasieva O, Meher S, et al. Pathway analysis of genetic factors associated with spontaneous preterm birth and pre-labor preterm rupture of membranes. PLoS One. 2014;9(9):e108578.
  • Najjar I, Fagard R. STAT1 and pathogens, not a friendly relationship. Biochimie. 2010;92(5):425–444.
  • Strom CM, Crossley B, Buller-Buerkle A, et al. Cystic fibrosis testing 8 years on: lessons learned from carrier screening and sequencing analysis. Genet Med. 2011;13(2):166–172.
  • Webb AR, Kazantzidis A, Kift RC, et al. Colour Counts: sunlight and skin type as drivers of vitamin D Deficiency at UK Latitudes. Nutrients. 2018;10(4):457.
  • Wolf ST, Jablonski NG, Ferguson SB, et al. Four weeks of vitamin D supplementation improves nitric oxide-mediated microvascular function in college-aged African Americans. Am J Physiol Heart Circ Physiol. 2020;319(4):H906–H914.
  • Liu PT, Stenger S, Li H, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science. 2006;311(5768):1770–1773.
  • Rafaeli-Yehudai T, Imterat M, Douvdevani A, et al. Maternal total cell-free DNA in preeclampsia and fetal growth restriction: evidence of differences in maternal response to abnormal implantation. PLoS One. 2018;13(7):e0200360.
  • Ribeiro VR, Romao-Veiga M, Romagnoli GG, et al. Association between cytokine profile and transcription factors produced by T-cell subsets in early- and late-onset pre-eclampsia. Immunology. 2017;152(1):163–173.
  • Giorgi VS, Witkin SS, Bannwart-Castro CF, et al. Elevated circulating adenosine deaminase activity in women with preeclampsia: association with pro-inflammatory cytokine production and uric acid levels. Pregnancy Hypertens. 2016;6(4):400–405.
  • Savitz DA, Blackmore CA, Thorp JM. Epidemiologic characteristics of preterm delivery: etiologic heterogeneity. Am J Obstet Gynecol. 1991;164(2):467–471.

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