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These T lymphocytes not only exert effector functions but also influence the development of the offspring's T lymphocytes in the thymus and the maturation of B lymphocytes in the lymph nodes. Furthermore, the migration of maternal leukocytes also facilitates the transfer of immune memory across generations. Maternal microchimerism has also been observed to address immunodeficiencies in the offspring. This review article focuses on investigating the impact of maternal cells transported within maternal microchimerism on the immune system development of the offspring, as well as elucidating the effector functions of maternal cells that migrate through the placenta and breast milk to reach the offspring.<\/jats:p>","DOI":"10.33549\/physiolres.935296","type":"journal-article","created":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T12:58:03Z","timestamp":1721221083000},"page":"315-332","source":"Crossref","is-referenced-by-count":13,"title":["Maternal-Fetal Microchimerism: Impacts on Offspring's Immune Development and Transgenerational Immune Memory Transfer"],"prefix":"10.33549","author":[{"given":"N","family":"Malinsk\u00e1","sequence":"first","affiliation":[{"name":"Laboratory of Cell Immunology, Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"V","family":"Grob\u00e1rov\u00e1","sequence":"additional","affiliation":[{"name":"Laboratory of Cell Immunology, Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"K","family":"Kn\u00ed\u017ekov\u00e1","sequence":"additional","affiliation":[{"name":"Laboratory of Cell Immunology, Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J","family":"\u010cern\u00fd","sequence":"additional","affiliation":[{"name":"Laboratory of Cell Immunology, Department of Cell Biology, Faculty of Science, Charles University, Prague, Czech Republic"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"19169","published-online":{"date-parts":[[2024,7,10]]},"reference":[{"key":"ref0","doi-asserted-by":"crossref","unstructured":"1.\tNelson JL. The otherness of self: microchimerism in health and disease. Trends Immunol 2012;33:421-427. https:\/\/doi.org\/10.1016\/j.it.2012.03.002","DOI":"10.1016\/j.it.2012.03.002"},{"key":"ref1","doi-asserted-by":"publisher","unstructured":"2.\tLoubi\u00e8re LS, Lambert NC, Flinn LJ, Erickson TD, Yan Z, Guthrie KA, Vickers KT, Nelson JL. Maternal microchimerism in healthy adults in lymphocytes, monocyte\/macrophages and NK cells. Lab Invest 2006;86:1185-1192. https:\/\/doi.org\/10.1038\/labinvest.3700471","DOI":"10.1038\/labinvest.3700471"},{"key":"ref2","doi-asserted-by":"publisher","unstructured":"3.\tVernochet C, Caucheteux SM, Kanellopoulos-Langevin C. Bi-directional Cell Trafficking Between Mother and Fetus in Mouse Placenta. Placenta 2007;28:639-649. https:\/\/doi.org\/10.1016\/j.placenta.2006.10.006","DOI":"10.1016\/j.placenta.2006.10.006"},{"key":"ref3","doi-asserted-by":"publisher","unstructured":"4.\tStelzer IA, Urbschat C, Schepanski S, Thiele K, Triviai I, Wieczorek A, Alawi M, ET AL. Vertically transferred maternal immune cells promote neonatal immunity against early life infections. Nat Commun 2021;12:4706. https:\/\/doi.org\/10.1038\/s41467-021-24719-z","DOI":"10.1038\/s41467-021-24719-z"},{"key":"ref4","doi-asserted-by":"publisher","unstructured":"5.\tWang Y, Iwatani H, Ito T, Horimoto N, Yamato M, Matsui I, Imai E, Hori M. Fetal cells in mother rats contribute to the remodeling of liver and kidney after injury. Biochem Biophys Res Commun 2004;325:961-967. https:\/\/doi.org\/10.1016\/j.bbrc.2004.10.105","DOI":"10.1016\/j.bbrc.2004.10.105"},{"key":"ref5","doi-asserted-by":"publisher","unstructured":"6.\tBoddy AM, Fortunato A, Wilson Sayres M, Aktipis A. Fetal microchimerism and maternal health: A review and evolutionary analysis of cooperation and conflict beyond the womb. BioEssays 2015;37:1106-1118. https:\/\/doi.org\/10.1002\/bies.201500059","DOI":"10.1002\/bies.201500059"},{"key":"ref6","doi-asserted-by":"publisher","unstructured":"7.\tRao AS, Thomson AW, Shapiro R, Starzl TE. Chimerism after whole organ transplantation: its relationship to graft rejection and tolerance induction: Curr Opin Nephrol Hypertens 1994;3:589-595. https:\/\/doi.org\/10.1097\/00041552-199411000-00005","DOI":"10.1097\/00041552-199411000-00005"},{"key":"ref7","doi-asserted-by":"crossref","unstructured":"8.\tStelzer IA, Thiele K, Solano ME. Maternal microchimerism: lessons learned from murine models. J Reprod Immunol 2015;108:12-25. https:\/\/doi.org\/10.1016\/j.jri.2014.12.007","DOI":"10.1016\/j.jri.2014.12.007"},{"key":"ref8","doi-asserted-by":"publisher","unstructured":"9.\tDutta P, Molitor-Dart M, Bobadilla JL, Roenneburg DA, Yan Z, Torrealba JR, Burlingham WJ. Microchimerism is strongly correlated with tolerance to noninherited maternal antigens in mice. Blood 2009;114:3578-3587. https:\/\/doi.org\/10.1182\/blood-2009-03-213561","DOI":"10.1182\/blood-2009-03-213561"},{"key":"ref9","doi-asserted-by":"publisher","unstructured":"10.\tCabinian A, Sinsimer D, Tang M, Zumba O, Mehta H, Toma A, Sant'Angelo D, ET AL. Transfer of Maternal Immune Cells by Breastfeeding: Maternal Cytotoxic T Lymphocytes Present in Breast Milk Localize in the Peyer's Patches of the Nursed Infant. PLoS One 2016;11:e0156762. https:\/\/doi.org\/10.1371\/journal.pone.0156762","DOI":"10.1371\/journal.pone.0156762"},{"key":"ref10","doi-asserted-by":"publisher","unstructured":"11.\tStevens AM, Hermes HM, Kiefer MM, Rutledge JC, Lee Nelson J. Chimeric Maternal Cells with Tissue-Specific Antigen Expression and Morphology Are Common in Infant Tissues. Pediatr Dev Pathol 2009;12:337-346. https:\/\/doi.org\/10.2350\/08-07-0499.1","DOI":"10.2350\/08-07-0499.1"},{"key":"ref11","doi-asserted-by":"publisher","unstructured":"12.\tHassiotou F, Heath B, Ocal O, Filgueira L, Geddes D, Hartmann P, Wilkie T. Breastmilk stem cell transfer from mother to neonatal organs. FASEB J 2014;28(Suppl 1):216.4. https:\/\/doi.org\/10.1096\/fasebj.28.1_supplement.216.4","DOI":"10.1096\/fasebj.28.1_supplement.216.4"},{"key":"ref12","doi-asserted-by":"publisher","unstructured":"13.\tDutta P, Burlingham WJ. Stem cell microchimerism and tolerance to non-inherited maternal antigens. Chimerism 2010;1:2-10. https:\/\/doi.org\/10.4161\/chim.1.1.12667","DOI":"10.4161\/chim.1.1.12667"},{"key":"ref13","doi-asserted-by":"publisher","unstructured":"14.\tCuddapah Sunku C, Gadi V, de Laval de Lacoste B, Guthrie KA, Nelson JL. Maternal and fetal microchimerism in granulocytes. Chimerism 2010;1:11-14. https:\/\/doi.org\/10.4161\/chim.1.1.13098","DOI":"10.4161\/chim.1.1.13098"},{"key":"ref14","doi-asserted-by":"publisher","unstructured":"15.\tMauer AM, Athens JW, Ashenbrucker H, Cartwright GE, Wintrobe MM. Leukokinetic Studies. Ii. A Method For Labeling Granulocytes In Vitro With Radioactive Diisopropylfluorophosphate (DFP32). J Clin Invest 1960;39:1481-1486. https:\/\/doi.org\/10.1172\/JCI104167","DOI":"10.1172\/jci104167"},{"key":"ref15","doi-asserted-by":"publisher","unstructured":"16.\tWrenshall LE, Stevens ET, Smith DR, Miller JD. Maternal microchimerism leads to the presence of interleukin-2 in interleukin-2 knock out mice: Implications for the role of interleukin-2 in thymic function. Cell Immunol 2007;245:80-90. https:\/\/doi.org\/10.1016\/j.cellimm.2007.04.002","DOI":"10.1016\/j.cellimm.2007.04.002"},{"key":"ref16","doi-asserted-by":"publisher","unstructured":"17.\tArvola M, Gustafsson E, Svensson L, Jansson L, Holmdahl R, Heyman B, Okabe M, Mattsson R. Immunoglobulin-Secreting Cells of Maternal Origin Can Be Detected in B Cell-Deficient Mice. Biol Reprod 2000;63:1817-1824. https:\/\/doi.org\/10.1095\/biolreprod63.6.1817","DOI":"10.1095\/biolreprod63.6.1817"},{"key":"ref17","doi-asserted-by":"publisher","unstructured":"18.\tFujimoto K, Nakajima A, Hori S, Irie N. Whole embryonic detection of maternal microchimeric cells highlights significant differences in their numbers among individuals. PLoS One 2021;16:e0261357. https:\/\/doi.org\/10.1371\/journal.pone.0261357","DOI":"10.1371\/journal.pone.0261357"},{"key":"ref18","doi-asserted-by":"publisher","unstructured":"19.\tBerry SM, Hassan SS, Russell E, Kukuruga D, Land S, Kaplan J. Association of Maternal Histocompatibility at Class II HLA Loci with Maternal Microchimerism in the Fetus. Pediatr Res 2004;56:73-78. https:\/\/doi.org\/10.1203\/01.PDR.0000129656.10005.A6","DOI":"10.1203\/01.pdr.0000129656.10005.a6"},{"key":"ref19","doi-asserted-by":"publisher","unstructured":"20.\tKaplan J, Land S. Influence of Maternal-Fetal Histocompatibility and MHC Zygosity on Maternal Microchimerism. J Immunol 2005;174:7123-7128. https:\/\/doi.org\/10.4049\/jimmunol.174.11.7123","DOI":"10.4049\/jimmunol.174.11.7123"},{"key":"ref20","doi-asserted-by":"publisher","unstructured":"21.\tKinder JM, Jiang TT, Ertelt JM, Xin L, Strong BS, Shaaban AF, Way SS. Cross-Generational Reproductive Fitness Enforced by Microchimeric Maternal Cells. Cell 2015;162:505-515. https:\/\/doi.org\/10.1016\/j.cell.2015.07.006","DOI":"10.1016\/j.cell.2015.07.006"},{"key":"ref21","doi-asserted-by":"publisher","unstructured":"22.\tMold JE, Micha\u00eblsson J, Burt TD, Muench MO, Beckerman KP, Busch MP, Lee T-H, ET AL. Maternal Alloantigens Promote the Development of Tolerogenic Fetal Regulatory T Cells in Utero. Science 2008;322:1562-1565. https:\/\/doi.org\/10.1126\/science.1164511","DOI":"10.1126\/science.1164511"},{"key":"ref22","doi-asserted-by":"publisher","unstructured":"23.\tHossain S, Mihrshahi S. Exclusive Breastfeeding and Childhood Morbidity: A Narrative Review. Int J Environ Res Public Health 2022;19:14804. https:\/\/doi.org\/10.3390\/ijerph192214804","DOI":"10.3390\/ijerph192214804"},{"key":"ref23","doi-asserted-by":"publisher","unstructured":"24.\tKarlmark KR, Haddad ME, Donato X-C, Martin GV, Bretelle F, Lesavre N, Cocallemen J-F, ET AL. Grandmaternal cells in cord blood. eBioMedicine 2021;74:103721. https:\/\/doi.org\/10.1016\/j.ebiom.2021.103721","DOI":"10.1016\/j.ebiom.2021.103721"},{"key":"ref24","doi-asserted-by":"publisher","unstructured":"25.\tShimamura M, Ohta S, Suzuki R, Yamazaki K. Transmission of maternal blood cells to the fetus during pregnancy: detection in mouse neonatal spleen by immunofluorescence flow cytometry and polymerase chain reaction. Blood 1994;83:926-930. https:\/\/doi.org\/10.1182\/blood.V83.4.926.926","DOI":"10.1182\/blood.v83.4.926.bloodjournal834926"},{"key":"ref25","doi-asserted-by":"publisher","unstructured":"26.\tHall J, Lingenfelter P, Adams S, Lasser D, Hansen J, Bean M. Detection of maternal cells in human umbilical cord blood using fluorescence in situ hybridization. Blood 1995;86:2829-2832. https:\/\/doi.org\/10.1182\/blood.V86.7.2829.2829","DOI":"10.1182\/blood.v86.7.2829.2829"},{"key":"ref26","doi-asserted-by":"publisher","unstructured":"27.\tPiotrowski P, Croy BA. Maternal Cells are Widely Distributed in Murine Fetuses in Utero1. Biol Reprod 1996;54:1103-1110. https:\/\/doi.org\/10.1095\/biolreprod54.5.1103","DOI":"10.1095\/biolreprod54.5.1103"},{"key":"ref27","doi-asserted-by":"publisher","unstructured":"28.\tSu EC, Johnson KL, Tighiouart H, Bianchi DW. Murine Maternal Cell Microchimerism: Analysis Using Real-Time PCR and In Vivo Imaging. Biol Reprod 2008;78:883-887. https:\/\/doi.org\/10.1095\/biolreprod.107.063305","DOI":"10.1095\/biolreprod.107.063305"},{"key":"ref28","doi-asserted-by":"publisher","unstructured":"29.\tDarby MG, Chetty A, Mrjden D, Rolot M, Smith K, Mackowiak C, Sedda D, ET AL. Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring. Sci Adv 2019;5:eaav3058. https:\/\/doi.org\/10.1126\/sciadv.aav3058","DOI":"10.1126\/sciadv.aav3058"},{"key":"ref29","doi-asserted-by":"publisher","unstructured":"30.\tSt\u00e5hlberg A, El-Heliebi A, Sedlmayr P, Kroneis T. Unravelling the biological secrets of microchimerism by single-cell analysis. Brief Funct Genomics 2018;17:255-264. https:\/\/doi.org\/10.1093\/bfgp\/elx027","DOI":"10.1093\/bfgp\/elx027"},{"key":"ref30","doi-asserted-by":"publisher","unstructured":"31.\tFujimoto K, Nakajima A, Hori S, Tanaka Y, Shirasaki Y, Uemura S, Irie N. Whole-embryonic identification of maternal microchimeric cell types in mouse using single-cell RNA sequencing. Sci Rep 2022;12:18313. https:\/\/doi.org\/10.1038\/s41598-022-20781-9","DOI":"10.21203\/rs.3.rs-1549180\/v2"},{"key":"ref31","doi-asserted-by":"publisher","unstructured":"32.\tCamacho-Morales A, Caba M, Garc\u00eda-Ju\u00e1rez M, Caba-Flores MD, Viveros-Contreras R, Mart\u00ednez-Valenzuela C. Breastfeeding Contributes to Physiological Immune Programming in the Newborn. Front Pediatr 2021;9:744104. https:\/\/doi.org\/10.3389\/fped.2021.744104","DOI":"10.3389\/fped.2021.744104"},{"key":"ref32","doi-asserted-by":"publisher","unstructured":"33.\tRoss SH, Cantrell DA. Signaling and Function of Interleukin-2 in T Lymphocytes. Annu Rev Immunol 2018;36:411-433. https:\/\/doi.org\/10.1146\/annurev-immunol-042617-053352","DOI":"10.1146\/annurev-immunol-042617-053352"},{"key":"ref33","doi-asserted-by":"publisher","unstructured":"34.\tSchorle H, Holtschke T, H\u00fcnig T, Schimpl A, Horak I. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature 1991;352:621-624. https:\/\/doi.org\/10.1038\/352621a0","DOI":"10.1038\/352621a0"},{"key":"ref34","doi-asserted-by":"publisher","unstructured":"35.\tLetterio JJ, Geiser AG, Kulkarni AB, Roche NS, Sporn MB, Roberts AB. Maternal Rescue of Transforming Growth Factor-\u03b2 1 Null Mice. Science 1994;264:1936-1938. https:\/\/doi.org\/10.1126\/science.8009224","DOI":"10.1126\/science.8009224"},{"key":"ref35","doi-asserted-by":"publisher","unstructured":"36.\tKanaan SB, Gammill HS, Harrington WE, De Rosa SC, Stevenson PA, Forsyth AM, Allen J, ET AL. Maternal microchimerism is prevalent in cord blood in memory T cells and other cell subsets, and persists post-transplant. Oncoimmunology 2017;6:e1311436. https:\/\/doi.org\/10.1080\/2162402X.2017.1311436","DOI":"10.1080\/2162402x.2017.1311436"},{"key":"ref36","doi-asserted-by":"publisher","unstructured":"37.\tKanold AMJ, Westgren M, G\u00f6therstr\u00f6m C. Cellular Subsets of Maternal Microchimerism in Umbilical Cord Blood. Cell Transplant 2019;28:522-528. https:\/\/doi.org\/10.1177\/0963689718779783","DOI":"10.1177\/0963689718779783"},{"key":"ref37","doi-asserted-by":"publisher","unstructured":"38.\tBertrand JY, Jalil A, Klaine M, Jung S, Cumano A, Godin I. Three pathways to mature macrophages in the early mouse yolk sac. Blood 2005;106:3004-3011. https:\/\/doi.org\/10.1182\/blood-2005-02-0461","DOI":"10.1182\/blood-2005-02-0461"},{"key":"ref38","doi-asserted-by":"publisher","unstructured":"39.\tBalounov\u00e1 J, \u0160pl\u00edchalov\u00e1 I, Dobe\u0161ov\u00e1 M, Kol\u00e1\u0159 M, Fi\u0161er K, Proch\u00e1zka J, Sedlacek R, ET AL. Toll-like receptor 2 expression on c-kit+ cells tracks the emergence of embryonic definitive hematopoietic progenitors. Nat Commun 2019;10:5176. https:\/\/doi.org\/10.1038\/s41467-019-13150-0","DOI":"10.1038\/s41467-019-13150-0"},{"key":"ref39","doi-asserted-by":"publisher","unstructured":"40.\tWitkowska-Zimny M, Kaminska-El-Hassan E. Cells of human breast milk. Cell Mol Biol Lett 2017;22:11. https:\/\/doi.org\/10.1186\/s11658-017-0042-4","DOI":"10.1186\/s11658-017-0042-4"},{"key":"ref40","doi-asserted-by":"publisher","unstructured":"41.\tLaouar A. Maternal Leukocytes and Infant Immune Programming during Breastfeeding. Trends Immunol 2020;41:225-239. https:\/\/doi.org\/10.1016\/j.it.2020.01.005","DOI":"10.1016\/j.it.2020.01.005"},{"key":"ref41","doi-asserted-by":"publisher","unstructured":"42.\tBoes M, Cerny J, Massol R, den Brouw MO, Kirchhausen T, Chen J, Ploegh HL. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature 2002;418:983-988. https:\/\/doi.org\/10.1038\/nature01004","DOI":"10.1038\/nature01004"},{"key":"ref42","doi-asserted-by":"publisher","unstructured":"43.\tPa\u010des J, Kn\u00ed\u017ekov\u00e1 K, Tu\u0161kov\u00e1 L, Grob\u00e1rov\u00e1 V, Zadra\u017eil Z, Boes M, \u010cern\u00fd J. MHC II - EGFP knock-in mouse model is a suitable tool for systems and quantitative immunology. Immunol Lett 2022;251-252:75-85. https:\/\/doi.org\/10.1016\/j.imlet.2022.10.007","DOI":"10.1016\/j.imlet.2022.10.007"},{"key":"ref43","doi-asserted-by":"publisher","unstructured":"44.\tMuzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007;45:593-605. https:\/\/doi.org\/10.1002\/dvg.20335","DOI":"10.1002\/dvg.20335"},{"key":"ref44","unstructured":"45.\tCrago SS, Prince SJ, Pretlow TG, McGhee JR, Mestecky J. Human colostral cells. I. Separation and characterization. Clin Exp Immunol 1979;38:585-597."},{"key":"ref45","doi-asserted-by":"publisher","unstructured":"46.\tBabu ST, Niu X, Raetz M, Savani RC, Hooper LV, Mirpuri J. Maternal high-fat diet results in microbiota-dependent expansion of ILC3s in mice offspring. JCI Insight 2018;3:e99223. https:\/\/doi.org\/10.1172\/jci.insight.99223","DOI":"10.1172\/jci.insight.99223"},{"key":"ref46","doi-asserted-by":"publisher","unstructured":"47.\tHassiotou F, Hepworth AR, Metzger P, Lai CT, Trengove N, Hartmann PE, Filgueira L. Maternal and infant infections stimulate a rapid leukocyte response in breastmilk. Clin Transl Immunol 2013;2:e3. https:\/\/doi.org\/10.1038\/cti.2013.1","DOI":"10.1038\/cti.2013.1"},{"key":"ref47","doi-asserted-by":"publisher","unstructured":"48.\tMol\u00e8s JP, Tuaillon E, Kankasa C, Bedin A-S, Nagot N, Marchant A, McDermid JM, Van de Perre P. Breastmilk cell trafficking induces microchimerism-mediated immune system maturation in the infant. Pediatr Allergy Immunol 2018;29:133-143. https:\/\/doi.org\/10.1111\/pai.12841","DOI":"10.1111\/pai.12841"},{"key":"ref48","doi-asserted-by":"publisher","unstructured":"49.\tBasha S, Surendran N, Pichichero M. Immune responses in neonates. Expert Rev Clin Immunol 2014;10:1171-1184. https:\/\/doi.org\/10.1586\/1744666X.2014.942288","DOI":"10.1586\/1744666x.2014.942288"},{"key":"ref49","doi-asserted-by":"publisher","unstructured":"50.\tHassiotou F, Geddes DT, Hartmann PE. Cells in Human Milk: State of the Science. J Hum Lact 2013;29:171-182. https:\/\/doi.org\/10.1177\/0890334413477242","DOI":"10.1177\/0890334413477242"},{"key":"ref50","doi-asserted-by":"publisher","unstructured":"51.\tValverde-Villegas JM, Durand M, Bedin A-S, Rutagwera D, Kankasa C, Tuaillon E, Nagot N, ET AL. Large Stem\/Progenitor-Like Cell Subsets can Also be Identified in the CD45 - and CD45 +\/High Populations in Early Human Milk. J Hum Lact 2020;36:303-309. https:\/\/doi.org\/10.1177\/0890334419885315","DOI":"10.1177\/0890334419885315"},{"key":"ref51","doi-asserted-by":"publisher","unstructured":"52.\tSabbaj S, Ghosh MK, Edwards BH, Leeth R, Don Decker W, Goepfert PA, Aldrovandi GM. Breast Milk-Derived Antigen-Specific CD8+ T Cells: An Extralymphoid Effector Memory Cell Population in Humans. J Immunol 2005;174:2951-2956. https:\/\/doi.org\/10.4049\/jimmunol.174.5.2951","DOI":"10.4049\/jimmunol.174.5.2951"},{"key":"ref52","doi-asserted-by":"publisher","unstructured":"53.\tTuaillon E, Val\u00e9a D, Becquart P, Al Tabaa Y, Meda N, Bollore K, Van de Perre P, Vendrell J-P. Human milk-derived B cells: a highly activated switched memory cell population primed to secrete antibodies. J Immunol 2009;182:7155-7162. https:\/\/doi.org\/10.4049\/jimmunol.0803107","DOI":"10.4049\/jimmunol.0803107"},{"key":"ref53","doi-asserted-by":"publisher","unstructured":"54.\tPa\u010des J, Grob\u00e1rov\u00e1 V, Zadra\u017eil Z, Kn\u00ed\u017ekov\u00e1 K, Malinsk\u00e1 N, Tu\u0161kov\u00e1 L, Boes M, \u010cern\u00fd J. MHC II-EGFP Knock\u2010in Mouse Model. Curr Protoc 2023;3:e925. https:\/\/doi.org\/10.1002\/cpz1.925","DOI":"10.1002\/cpz1.925"},{"key":"ref54","doi-asserted-by":"publisher","unstructured":"55.\tIkebuchi R, Fujimoto M, Moriya T, Kusumoto Y, Kobayashi K, Tomura M. T cells are the main population in mouse breast milk and express similar profiles of tight junction proteins as those in mammary alveolar epithelial cells. J Reprod Immunol 2020;140:103137. https:\/\/doi.org\/10.1016\/j.jri.2020.103137","DOI":"10.1016\/j.jri.2020.103137"},{"key":"ref55","doi-asserted-by":"publisher","unstructured":"56.\tWirt DP, Adkins LT, Palkowetz KH, Schmalstieg FC, Goldman AS. Activated and memory T lymphocytes in human milk. Cytometry 1992;13:282-290. https:\/\/doi.org\/10.1002\/cyto.990130310","DOI":"10.1002\/cyto.990130310"},{"key":"ref56","doi-asserted-by":"publisher","unstructured":"57.\tPillay J, Den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JAM, Tesselaar K, Koenderman L. In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 2010;116:625-627. https:\/\/doi.org\/10.1182\/blood-2010-01-259028","DOI":"10.1182\/blood-2010-01-259028"},{"key":"ref57","doi-asserted-by":"publisher","unstructured":"58.\tYu JC, Khodadadi H, Malik A, Davidson B, da Silva Lopes Salles \u00c9, Bhatia J, Hale VL, Baban B. Innate Immunity of Neonates and Infants. Front Immunol 2018;9:1759. https:\/\/doi.org\/10.3389\/fimmu.2018.01759","DOI":"10.3389\/fimmu.2018.01759"},{"key":"ref58","doi-asserted-by":"publisher","unstructured":"59.\tWeinberger B, Laskin DL, Mariano TM, Sunil VR, DeCoste CJ, Heck DE, Gardner CR, Laskin JD. Mechanisms underlying reduced responsiveness of neonatal neutrophils to distinct chemoattractants. J Leukoc Biol 2001;70:969-976. https:\/\/doi.org\/10.1189\/jlb.70.6.969","DOI":"10.1189\/jlb.70.6.969"},{"key":"ref59","doi-asserted-by":"publisher","unstructured":"60.\tYost CC, Cody MJ, Harris ES, Thornton NL, McInturff AM, Martinez ML, Chandler NB, ET AL. 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Immunology 2003;108:189-195. https:\/\/doi.org\/10.1046\/j.1365-2567.2003.01572.x","DOI":"10.1046\/j.1365-2567.2003.01572.x"},{"key":"ref62","doi-asserted-by":"publisher","unstructured":"63.\tGeissmann F, Jung S, Littman DR. Blood Monocytes Consist of Two Principal Subsets with Distinct Migratory Properties. Immunity 2003;19:71-82. https:\/\/doi.org\/10.1016\/S1074-7613(03)00174-2","DOI":"10.1016\/s1074-7613(03)00174-2"},{"key":"ref63","doi-asserted-by":"publisher","unstructured":"64.\tZheng Y, Corr\u00eaa-Silva S, de Souza EC, Rodrigues RM, da Fonseca FAM, Gilio AE, Carneiro-Sampaio M, Palmeira P. Macrophage profile and homing into breast milk in response to ongoing respiratory infections in the nursing infant. Cytokine 2020;129:155045. https:\/\/doi.org\/10.1016\/j.cyto.2020.155045","DOI":"10.1016\/j.cyto.2020.155045"},{"key":"ref64","doi-asserted-by":"publisher","unstructured":"65.\tMedzhitov R, Schneider DS, Soares MP. Disease Tolerance as a Defense Strategy. Science 2012;335:936-941. https:\/\/doi.org\/10.1126\/science.1214935","DOI":"10.1126\/science.1214935"},{"key":"ref65","doi-asserted-by":"publisher","unstructured":"66.\tLeyva-Cobi\u00e1n F, Clemente J. Phenotypic characterization and functional activity of human milk macrophages. Immunol Lett 1984;8:249-256. https:\/\/doi.org\/10.1016\/0165-2478(84)90004-X","DOI":"10.1016\/0165-2478(84)90004-x"},{"key":"ref66","doi-asserted-by":"publisher","unstructured":"67.\tGeijtenbeek TBH, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GC, Middel J, Cornelissen IL, ET AL. DC-SIGN, a Dendritic Cell-Specific HIV-1-Binding Protein that Enhances trans-Infection of T Cells. Cell 2000;100:587-597. https:\/\/doi.org\/10.1016\/S0092-8674(00)80694-7","DOI":"10.1016\/s0092-8674(00)80694-7"},{"key":"ref67","doi-asserted-by":"publisher","unstructured":"68.\tSallusto F, Lanzavecchia A. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte\/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J Exp Med 1994;179:1109-1118. https:\/\/doi.org\/10.1084\/jem.179.4.1109","DOI":"10.1084\/jem.179.4.1109"},{"key":"ref68","doi-asserted-by":"publisher","unstructured":"69.\tBedin A, Mol\u00e8s J, Rutagwera D, Nagot N, Kankasa C, Tyllesk\u00e4r T, Valverde-Villegas JM, ET AL. MAIT cells, TCR \u03b3\u03b4+ cells and ILCs cells in human breast milk and blood from HIV infected and uninfected women. Pediatr Allergy Immunol 2019;30:479-487. https:\/\/doi.org\/10.1111\/pai.13037","DOI":"10.1111\/pai.13037"},{"key":"ref69","doi-asserted-by":"publisher","unstructured":"70.\tC\u00e9rbulo-V\u00e1zquez A, Hern\u00e1ndez-Pel\u00e1ez G, Arriaga-Pizano LA, Bautista-P\u00e9rez P, Romero-Venado J, Flores-Gonz\u00e1lez JC, Figueroa-Damian R, ET AL. Characterization of CD127 \u2212 CD25 ++ Treg from human colostrum. Am J Reprod Immunol 2018;79:e12806. https:\/\/doi.org\/10.1111\/aji.12806","DOI":"10.1111\/aji.12806"},{"key":"ref70","doi-asserted-by":"publisher","unstructured":"71.\tRudloff HE, Schmalstieg FC, Mushtaha AA, Palkowetz KH, Liu SK, Goldman AS. Tumor Necrosis Factor-\u03b1 in Human Milk. Pediatr Res 1992;31:29-33. https:\/\/doi.org\/10.1203\/00006450-199201000-00005","DOI":"10.1203\/00006450-199201000-00005"},{"key":"ref71","doi-asserted-by":"publisher","unstructured":"72.\tHawkes JS, Bryan DL, James MJ, Gibson RA. Cytokines (IL-1\u03b2, IL-6, TNF-\u03b1, TGF-\u03b21, and TGF-\u03b22) and Prostaglandin E2 in Human Milk during the First Three Months Postpartum. Pediatr Res 1999;46:194-199. https:\/\/doi.org\/10.1203\/00006450-199908000-00012","DOI":"10.1203\/00006450-199908000-00012"},{"key":"ref72","doi-asserted-by":"publisher","unstructured":"73.\tHackett RJ, Davis LS, Lipsky PE. Comparative effects of tumor necrosis factor-alpha and IL-1 beta on mitogen-induced T cell activation. J Immunol 1988;140:2639-2644. https:\/\/doi.org\/10.4049\/jimmunol.140.8.2639","DOI":"10.4049\/jimmunol.140.8.2639"},{"key":"ref73","doi-asserted-by":"publisher","unstructured":"74.\tSabbaj S, Edwards BH, Ghosh MK, Semrau K, Cheelo S, Thea DM, Kuhn L, ET AL. Human Immunodeficiency Virus-Specific CD8(+) T Cells in Human Breast Milk. J Virol 2002;76:7365-7373. https:\/\/doi.org\/10.1128\/JVI.76.15.7365-7373.2002","DOI":"10.1128\/jvi.76.15.7365-7373.2002"},{"key":"ref74","doi-asserted-by":"publisher","unstructured":"75.\tTatematsu M, Takahashi M, Tsuda H, Hirose M, Furihata C, Sugimura T. Precocious differentiation of immature chief cells in fundic mucosa of infant rats induced by hydrocortisone. Cell Differ 1975;4:285-294. https:\/\/doi.org\/10.1016\/0045-6039(75)90013-5","DOI":"10.1016\/0045-6039(75)90013-5"},{"key":"ref75","doi-asserted-by":"publisher","unstructured":"76.\tMa LJ, Walter B, DeGuzman A, Muller HK, Walker AM. Trans-Epithelial Immune Cell Transfer during Suckling Modulates Delayed-Type Hypersensitivity in Recipients as a Function of Gender. PLoS One 2008;3:e3562. https:\/\/doi.org\/10.1371\/journal.pone.0003562","DOI":"10.1371\/journal.pone.0003562"},{"key":"ref76","doi-asserted-by":"publisher","unstructured":"77.\tTuboly S, Bern\u00e1th S. Intestinal Absorption of Colostral Lymphoid Cells in Newborn Animals. Adv Exp Med Biol 2002;503:107-114. https:\/\/doi.org\/10.1007\/978-1-4615-0559-4_12","DOI":"10.1007\/978-1-4615-0559-4_12"},{"key":"ref77","doi-asserted-by":"publisher","unstructured":"78.\tRose EC, Odle J, Blikslager AT, Ziegler AL. Probiotics, Prebiotics and Epithelial Tight Junctions: A Promising Approach to Modulate Intestinal Barrier Function. Int J Mol Sci 2021;22:6729. https:\/\/doi.org\/10.3390\/ijms22136729","DOI":"10.3390\/ijms22136729"},{"key":"ref78","doi-asserted-by":"publisher","unstructured":"79.\tCatassi C, Bonucci A, Coppa GV, Carlucci A, Giorgi PL. Intestinal Permeability. Changes during the First Month: Effect of Natural versus Artificial Feeding. J Pediatr Gastroenterol Nutr 1995;21:383-386. https:\/\/doi.org\/10.1002\/j.1536-4801.1995.tb11955.x","DOI":"10.1002\/j.1536-4801.1995.tb11955.x"},{"key":"ref79","doi-asserted-by":"publisher","unstructured":"80.\tRoux ME, McWilliams M, Phillips-Quagliata JM, Weisz-Carrington P, Lamm ME. Origin of IgA-secreting plasma cells in the mammary gland. J Exp Med 1977;146:1311-1322. https:\/\/doi.org\/10.1084\/jem.146.5.1311","DOI":"10.1084\/jem.146.5.1311"},{"key":"ref80","unstructured":"81.\tRose ML, Parrott DM, Bruce RG. The accumulation of immunoblasts in extravascular tissues including mammary gland, peritoneal cavity, gut and skin. Immunology 1978;35:415-423."},{"key":"ref81","doi-asserted-by":"publisher","unstructured":"82.\tRamanan D, Sefik E, Galv\u00e1n-Pe\u00f1a S, Wu M, Yang L, Yang Z, Kostic A, ET AL. An Immunologic Mode of Multigenerational Transmission Governs a Gut Treg Setpoint. Cell 2020;181:1276-1290.e13. https:\/\/doi.org\/10.1016\/j.cell.2020.04.030","DOI":"10.1016\/j.cell.2020.04.030"},{"key":"ref82","doi-asserted-by":"publisher","unstructured":"83.\tGhosh MK, Nguyen V, Muller HK, Walker AM. Maternal Milk T Cells Drive Development of Transgenerational Th1 Immunity in Offspring Thymus. J Immunol 2016;197:2290-2296. https:\/\/doi.org\/10.4049\/jimmunol.1502483","DOI":"10.4049\/jimmunol.1502483"},{"key":"ref83","doi-asserted-by":"publisher","unstructured":"84.\tTanneau GM, Oyant LHS, Chevaleyre CC, Salmon HP. Differential Recruitment of T- and IgA B-lymphocytes in the Developing Mammary Gland in Relation to Homing Receptors and Vascular Addressins. J Histochem Cytochem 1999;47:1581-1592. https:\/\/doi.org\/10.1177\/002215549904701210","DOI":"10.1177\/002215549904701210"},{"key":"ref84","doi-asserted-by":"publisher","unstructured":"85.\tLokossou GAG, Kouakanou L, Schumacher A, Zenclussen AC. Human Breast Milk: From Food to Active Immune Response With Disease Protection in Infants and Mothers. Front Immunol 2022;13:849012. https:\/\/doi.org\/10.3389\/fimmu.2022.849012","DOI":"10.3389\/fimmu.2022.849012"},{"key":"ref85","doi-asserted-by":"publisher","unstructured":"86.\tLi S, Zhang L, Zhou Q, Jiang S, Yang Y, Cao Y. Characterization of Stem Cells and Immune Cells in Preterm and Term Mother's Milk. J Hum Lact 2019;35:528-534. https:\/\/doi.org\/10.1177\/0890334419838986","DOI":"10.1177\/0890334419838986"},{"key":"ref86","doi-asserted-by":"publisher","unstructured":"87.\tFan Y, Chong YS, Choolani MA, Cregan MD, Chan JKY. Unravelling the Mystery of Stem\/Progenitor Cells in Human Breast Milk. 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Curr Opin Immunol 2010;22:552-559. https:\/\/doi.org\/10.1016\/j.coi.2010.08.005","DOI":"10.1016\/j.coi.2010.08.005"},{"key":"ref90","doi-asserted-by":"publisher","unstructured":"91.\tChappert P, Leboeuf M, Rameau P, Lalfer M, Desbois S, Liblau RS, Danos O, ET AL. Antigen-specific Treg impair CD8 + T-cell priming by blocking early T-cell expansion. Eur J Immunol 2010;40:339-350. https:\/\/doi.org\/10.1002\/eji.200839107","DOI":"10.1002\/eji.200839107"},{"key":"ref91","doi-asserted-by":"publisher","unstructured":"92.\tCarter AM. Animal models of human pregnancy and placentation: alternatives to the mouse. 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