Scientific Papers

Sex-specific phenotypical, functional and metabolic profiles of human term placenta macrophages | Biology of Sex Differences


  • Mitchell AM, Palettas M, Christian LM. Fetal sex is associated with maternal stimulated cytokine production, but not serum cytokine levels, in human pregnancy. Brain Behav Immun. 2017;60:32–7.

    Article 
    CAS 

    Google Scholar
     

  • O’Callaghan JL, Clifton VL, Prentis P, Ewing A, Saif Z, Pelzer ES. Sex-dependent differential transcript expression in the placenta of growth restricted infants. Placenta. 2022;128:1–8.

    Article 

    Google Scholar
     

  • Eriksson JG, Kajantie E, Osmond C, Thornburg K, Barker DJP. Boys live dangerously in the womb. Am J Hum Biology. 2010;22:330–5.

    Article 

    Google Scholar
     

  • Sun T, Gonzalez TL, Deng N, DiPentino R, Clark EL, Lee B et al. Sexually Dimorphic Crosstalk at the Maternal-Fetal Interface. J Clin Endocrinol Metab [Internet]. 2020;105:e4831-47. http://www.ncbi.nlm.nih.gov/pubmed/32772088

  • Braun AE, Mitchel OR, Gonzalez TL, Sun T, Flowers AE, Pisarska MD, et al. Sex at the interface: the origin and impact of sex differences in the developing human placenta. Biol Sex Differ. BioMed Central Ltd; 2022.

  • Melamed N, Yogev Y, Glezerman M. Fetal gender and pregnancy outcome. J Matern Fetal Neonatal Med. 2010;23:338–44.

    Article 

    Google Scholar
     

  • Verburg PE, Tucker G, Scheil W, Erwich JJHM, Dekker GA, Roberts CT. Sexual dimorphism in adverse pregnancy outcomes – A retrospective Australian population study 1981–2011. PLoS ONE. 2016;11.

  • Gonzalez TL, Sun T, Koeppel AF, Lee B, Wang ET, Farber CR et al. Sex differences in the late first trimester human placenta transcriptome. Biol Sex Differ. 2018;9.

  • Elsmén E, Källén K, Maršál K, Hellström-Westas L. Fetal gender and gestational-age-related incidence of pre-eclampsia. Acta Obstet Gynecol Scand. 2006;85:1285–91.

    Article 

    Google Scholar
     

  • Zazara DE, Arck PC. Developmental origin and sex-specific risk for infections and immune diseases later in life. Semin Immunopathol. Springer Verlag; 2019. pp. 137–51.

  • Beilby KH, Kneebone E, Roseboom TJ, van Marrewijk IM, Thompson JG, Norman RJ, et al. Offspring physiology following the use of IVM, IVF and ICSI: a systematic review and meta-analysis of animal studies. Hum Reprod Update. 2023;29:272–90.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Gabory A, Roseboom TJ, Moore T, Moore LG, Junien C. Placental contribution to the origins of sexual dimorphism in health and diseases: sex chromosomes and epigenetics. Biol Sex Differ. 2013.

  • Maxwell A, Adzibolosu N, Hu A, You Y, Stemmer PM, Ruden DM et al. Intrinsic sexual dimorphism in the placenta determines the differential response to benzene exposure. iScience. 2023;26.

  • Falahi S, Abdoli A, Kenarkoohi A. Maternal COVID-19 infection and the fetus: immunological and neurological perspectives. New Microbes New Infect. 2023;53:101135.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Olin A, Henckel E, Chen Y, Lakshmikanth T, Pou C, Mikes J, et al. Stereotypic Immune System Development in Newborn Children. Cell. 2018;174:1277–e129214.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Forsen T, Eriksson JG, Tuomilehto J, Osmond C, Barker DJP. Growth in utero and during childhood among women who develop coronary heart disease: longitudinal study. BMJ. 1999;319:1403–7.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Taylor BD, Ness RB, Klebanoff MA, Tang G, Roberts JM, Hougaard DM, et al. The impact of female fetal sex on preeclampsia and the maternal immune milieu. Pregnancy Hypertens. 2018;12:53–7.

    Article 
    PubMed Central 

    Google Scholar
     

  • Miremberg H, Ganer Herman H, Bustan M, Weiner E, Schreiber L, Bar J, et al. Placental vascular lesions differ between male and female fetuses in early-onset preeclampsia. Arch Gynecol Obstet. 2022;306:717–22.

    Article 

    Google Scholar
     

  • Reyes L, Golos TG. Hofbauer cells: their role in healthy and complicated pregnancy. Front Immunol. Frontiers Media S.A.; 2018.

  • Seval Y, Korgun ET, Demir R. Hofbauer Cells in early human placenta: possible implications in Vasculogenesis and angiogenesis. Placenta. 2007;28:841–5.

    Article 
    CAS 

    Google Scholar
     

  • Ingman K, Cookson VJKW, Jones CJP, Aplin JD. Characterisation of Hofbauer Cells in First and Second Trimester Placenta: incidence, phenotype, survival in vitro and motility. Placenta. 2010;31:535–44.

    Article 
    CAS 

    Google Scholar
     

  • Thomas JR, Naidu P, Appios A, McGovern N. The Ontogeny and function of placental macrophages. Front Immunol. Frontiers Media S.A.; 2021.

  • Zulu MZ, Martinez FO, Gordon S, Gray CM. The elusive role of placental macrophages: the Hofbauer cell. J Innate Immun. S. Karger AG; 2019.

  • Thomas JR, Appios A, Zhao X, Dutkiewicz R, Donde M, Lee CYC et al. Phenotypic and functional characterization of first-trimester human placental macrophages, Hofbauer cells. J Exp Med. 2020;218.

  • Megli CJ, Coyne CB. Infections at the maternal–fetal interface: an overview of pathogenesis and defence. Nat Rev Microbiol Nat Res; 2022. pp. 67–82.

  • Tauber Z, Chroma K, Baranova R, Cizkova K. The expression patterns of IL-1β and IL-10 and their relation to CYP epoxygenases in normal human placenta. Annals Anat. 2021;236.

  • Schliefsteiner C, Ibesich S, Wadsack C. Placental hofbauer cell polarization resists inflammatory cues in vitro. Int J Mol Sci. 2020;21.

  • Pantazi P, Kaforou M, Tang Z, Abrahams VM, McArdle A, Guller S et al. Placental macrophage responses to viral and bacterial ligands and the influence of fetal sex. iScience. 2022;25.

  • O’Neill LAJ, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol Nat Publishing Group; 2016. pp. 553–65.

  • Tabas I, Bornfeldt KE. Intracellular and intercellular aspects of macrophage immunometabolism in atherosclerosis. Circ Res. 2020;126:1209–27.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Wculek SK, Heras-Murillo I, Mastrangelo A, Mañanes D, Galán M, Miguel V, et al. Oxidative phosphorylation selectively orchestrates tissue macrophage homeostasis. Immunity. 2023;56:516–e5309.

    Article 
    CAS 

    Google Scholar
     

  • Wculek SK, Dunphy G, Heras-Murillo I, Mastrangelo A, Sancho D. Metabolism of tissue macrophages in homeostasis and pathology. Cell Mol Immunol. Springer Nature; 2022. pp. 384–408.

  • Sheng YR, Hu WT, Shen HH, Wei CY, Liu YK, Ma XQ et al. An imbalance of the IL-33/ST2-AXL-efferocytosis axis induces pregnancy loss through metabolic reprogramming of decidual macrophages. Cell Mol Life Sci. 2022;79.

  • Merech F, Gori S, Calo G, Hauk V, Paparini D, Rios D, et al. Monocyte immunometabolic reprogramming in human pregnancy: contribution of trophoblast cells. Am J Physiol Endocrinol Metab. 2024;326:E215–25.

    Article 
    CAS 

    Google Scholar
     

  • Gao L, Xu QH, Ma LN, Luo J, Muyayalo KP, Wang LL, et al. Trophoblast-derived lactic acid orchestrates decidual macrophage differentiation via SRC/LDHA Signaling in early pregnancy. Int J Biol Sci. 2022;18:599–616.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Paparini DE, Choudhury RH, Vota DM, Karolczak-Bayatti M, Finn-Sell S, Grasso EN et al. Vasoactive intestinal peptide shapes first-trimester placenta trophoblast, vascular, and immune cell cooperation. Br J Pharmacol [Internet]. 2019;176:964–80. http://www.ncbi.nlm.nih.gov/pubmed/30726565

  • Paparini DE, Grasso E, Fernandez LDC, Merech F, Weingrill-Barbano R, Correa-Silva S, et al. Decidual factors and vasoactive intestinal peptide guide monocytes to higher migration, efferocytosis and wound healing in term human pregnancy. Acta Physiol (Oxf). 2021;232:e13579.

    Article 
    CAS 

    Google Scholar
     

  • Wetzka B, Clark DE, Charnock-Jones DS, Zahradnik HP, Smith SK, Kaufmann. Isolation of macrophages (Hofbauer cells) from human term placenta and their prostaglandin E 2 and thromboxane production (MHC) class I and II antigens (Castellucci. Human Reproduction vol. 1997.

  • Appios A, Thomas JR, McGovern N. Isolation of first-trimester and full-term human placental Hofbauer cells. Bio Protoc. 2021;11.

  • Paparini D, Gori S, Grasso E, Scordo W, Calo G, Pérez Leirós C et al. Acetylcholine contributes to control the physiological inflammatory response during the peri-implantation period. Acta Physiol. 2015;214.

  • Kolahi K, Louey S, Varlamov O, Thornburg K. Real-time tracking of BODIPY-C12 long-chain fatty acid in Human Term Placenta Reveals Unique Lipid Dynamics in Cytotrophoblast Cells. PLoS ONE. 2016;11:e0153522.

    Article 
    PubMed Central 

    Google Scholar
     

  • Paparini D, Grasso E, Calo G, Vota D, Hauk V, Ramhorst R et al. Trophoblast cells primed with vasoactive intestinal peptide enhance monocyte migration and apoptotic cell clearance through αvβ3 integrin portal formation in a model of maternal–placental interaction. Mol Hum Reprod [Internet]. 2015;21:930–41. http://www.molehr.oxfordjournals.org/lookup/doi/https://doi.org/10.1093/molehr/gav059

  • Calo G, Sabbione F, Vota D, Paparini D, Ramhorst R, Trevani A et al. Trophoblast cells inhibit neutrophil extracellular trap formation and enhance apoptosis through vasoactive intestinal peptide-mediated pathways. Hum Reprod. 2017;32.

  • Calo G, Sabbione F, Pascuali N, Keitelman I, Vota D, Paparini D, et al. Interplay between neutrophils and trophoblast cells conditions trophoblast function and triggers vascular transformation signals. J Cell Physiol. 2020;235:3592–603.

    Article 
    CAS 

    Google Scholar
     

  • Svensson J, Jenmalm MC, Matussek A, Geffers R, Berg G, Ernerudh J. Macrophages at the fetal-maternal interface express markers of alternative activation and are induced by M-CSF and IL-10. J Immunol [Internet]. 2011;187:3671–82. http://www.jimmunol.org/cgi/doi/https://doi.org/10.4049/jimmunol.1100130

  • Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet. 2006;38:500–1.

    Article 
    CAS 

    Google Scholar
     

  • R Core Team. R Core Team. (2022) R: A language and environment for statistical computing. Vienna; 2022.

  • Smyth G, [cre. aut]. limma. Linear Models for Microarray Data. 2017.

  • Fang Z, Liu X, Peltz G. GSEApy: a comprehensive package for performing gene set enrichment analysis in Python. Bioinformatics. 2023;39.

  • Freemerman AJ, Johnson AR, Sacks GN, Milner JJ, Kirk EL, Troester MA, et al. Metabolic reprogramming of macrophages: glucose transporter 1 (GLUT1)-mediated glucose metabolism drives a proinflammatory phenotype. J Biol Chem. 2014;289:7884–96.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Van den Bossche J, O’Neill LA, Menon D. Macrophage immunometabolism: where are we (going)? Trends Immunol. Elsevier Ltd; 2017. pp. 395–406.

  • Verberk SGS, de Goede KE, Gorki FS, van Dierendonck XAMH, Argüello RJ. Van Den Bossche J. An integrated toolbox to profile macrophage immunometabolism. Cell Rep Methods. 2022;2.

  • Hetz C. The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012. pp. 89–102.

  • Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science. 2011;334:1081–6.

    Article 
    PubMed 
    CAS 

    Google Scholar
     

  • Ribeiro CMP, Lubamba BA. Role of IRE1α/XBP-1 in cystic fibrosis airway inflammation. Int J Mol Sci. MDPI AG; 2017.

  • Huang S, Xing Y, Liu Y. Emerging roles for the ER stress sensor IRE1 in metabolic regulation and disease. J Biol Chem. 2019;294:18726–41.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Schurz H, Salie M, Tromp G, Hoal EG, Kinnear CJ, Möller M. The X chromosome and sex-specific effects in infectious disease susceptibility. Hum Genomics. 2019;13:2.

    Article 
    PubMed Central 

    Google Scholar
     

  • Capone I, Marchetti P, Ascierto PA, Malorni W, Gabriele L. Sexual dimorphism of Immune responses: a new perspective in cancer immunotherapy. Front Immunol. 2018;9.

  • Dearden L, Bouret SG, Ozanne SE. Sex and gender differences in developmental programming of metabolism. Mol Metab. Elsevier GmbH; 2018. pp. 8–19.

  • Bouman A, Heineman MJ, Faas MM. Sex hormones and the immune response in humans. Hum Reprod Update. 2005;11:411–23.

    Article 
    CAS 

    Google Scholar
     

  • Markle JG, Fish EN. SeXX matters in immunity. Trends Immunol. 2014;35:97–104.

    Article 
    CAS 

    Google Scholar
     

  • Trigunaite A, Dimo J, Jørgensen TN. Suppressive effects of androgens on the immune system. Cell Immunol. 2015;294:87–94.

    Article 
    CAS 

    Google Scholar
     

  • Dolfi B, Gallerand A, Firulyova MM, Xu Y, Merlin J, Dumont A, et al. Unravelling the sex-specific diversity and functions of adrenal gland macrophages. Cell Rep. 2022;39:110949.

    Article 
    PubMed Central 
    CAS 

    Google Scholar
     

  • Doran AC, Yurdagul A, Tabas I. Efferocytosis in health and disease. Nat Rev Immunol Nat Res; 2020. pp. 254–67.

  • Feng J, Han J, Pearce SF, Silverstein RL, Gotto AM, Hajjar DP, et al. Induction of CD36 expression by oxidized LDL and IL-4 by a common signaling pathway dependent on protein kinase C and PPAR-gamma. J Lipid Res. 2000;41:688–96.

    Article 
    CAS 

    Google Scholar
     

  • Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal. 2009;2:re3.

    Article 
    PubMed Central 

    Google Scholar
     

  • Wei Y, Ding J, Li J, Cai S, Liu S, Hong L, et al. Metabolic reprogramming of Immune cells at the maternal-fetal interface and the development of techniques for Immunometabolism. Front Immunol. Frontiers Media S.A.; 2021.



  • Source link