Skip to main content

Advertisement

SpringerLink
Log in

Translational Comparison of the Human and Mouse Yolk Sac Development and Function

  • Review
  • Published:
Reproductive Sciences Aims and scope Submit manuscript

Abstract

The yolk sac (YS) is the oldest of the extraembryonic membranes in vertebrates. Considered a transitory structure in the human species, the importance of the YS for a successful pregnancy is often overlooked. Due to the general inaccessibility of healthy human YS tissue for research, the use of experimental animal models is of great value. In order to better understand whether the mouse could be used as a translational model for the study of the human YS under normal and pathological conditions, this review comprehensively describes key developmental aspects of the human and mouse YS, detailing their development and function. YS major similarities in both species comprise the following: (1) histological composition (both being composed of endoderm, mesoderm, and mesothelium layers); (2) endoderm endocytosis, synthesis, secretion, and transport capabilities; and (3) mesoderm onset of haematopoiesis and angiogenesis. Examples of main dissimilarities include (1) persistence across pregnancy (i.e. early pregnancy in humans vs term pregnancy in mice); (2) the existence of a secondary YS in humans; (3) the presence of proliferative primordial germ cells (PGCs) in the human versus their absence in mice; and (4) eversion of histological layers in the mouse. Although these differences should be considered when interpreting data from mouse-based studies, the overall morphofunctional similarities in the YS between these species indicate that the mouse can be potentially used as a translational model for the study of the human YS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data Availability

Not applicable.

Code Availability

Not applicable.

References

  1. Sheng G, Foley AC. Diversification and conservation of the extraembryonic tissues in mediating nutrient uptake during amniote development. Ann N Y Acad Sci. 2012;1271:97–103. https://doi.org/10.1111/j.1749-6632.2012.06726.x.

    Article  Google Scholar 

  2. Ferner K, Mess A. Evolution and development of fetal membranes and placentation in amniote vertebrates. Respir Physiol Neurobiol. 2011;178:39–50. https://doi.org/10.1016/j.resp.2011.03.029.

    Article  Google Scholar 

  3. Ross C, Boroviak TE. Origin and function of the yolk sac in primate embryogenesis. Nat Commun. 2020;11:3760. https://doi.org/10.1038/s41467-020-17575-w.

    Article  CAS  Google Scholar 

  4. Mamsen LS, Brøchner CB, Byskov AG, Møllgard K. The migration and loss of human primordial germ stem cells from the hind gut epithelium towards the gonadal ridge. Int J Dev Biol. 2012;56:771–8. https://doi.org/10.1387/ijdb.120202lm.

    Article  CAS  Google Scholar 

  5. Palis J. Yolk-sac hematopoiesis: the first blood cells of mouse and man. Exp Hematol. 2001;29:927–36. https://doi.org/10.1016/S0301-472X(01)00669-5.

    Article  CAS  Google Scholar 

  6. McGrath KE, Palis J. Hematopoiesis in the yolk sac: more than meets the eye. Exp Hematol. 2005;33:1021–8. https://doi.org/10.1016/j.exphem.2005.06.012.

    Article  Google Scholar 

  7. Golub R, Cumano A. Embryonic hematopoiesis. Blood Cells Mol Dis. 2013;51:226–31. https://doi.org/10.1016/j.bcmd.2013.08.004.

    Article  CAS  Google Scholar 

  8. Berdahl DM, Blaine J, Van Voorhis B, Dokras A. Detection of enlarged yolk sac on early ultrasound is associated with adverse pregnancy outcomes. Fertil Steril. 2010;94:1535–7. https://doi.org/10.1016/j.fertnstert.2009.12.064.

    Article  Google Scholar 

  9. Duan Y, Wang H, Mitchell-silbaugh K, Cai S, Fan F, Li Y, et al. Heat shock protein 60 regulates yolk sac erythropoiesis in mice. Cell Death Dis. 2019;10:766. https://doi.org/10.1038/s41419-019-2014-2.

    Article  CAS  Google Scholar 

  10. Zohn IE, Sarkar AA. The visceral yolk sac endoderm provides for absorption of nutrients to the embryo during neurulation. Birt Defects Res A Clin Mol Teratol. 2010;88:593–600. https://doi.org/10.1002/bdra.20705.

    Article  CAS  Google Scholar 

  11. Exalto N. Yolk sac abnormalities: a clinical review. In: Nogales FF, editor. Hum. Yolk sac yolk sac tumors, Berlin, Heidelberg: Springer Berlin Heidelberg; 1993, p. 126–34. https://doi.org/10.1007/978-3-642-77852-0_7.

  12. Dong J, Wen L, Guo X, Xiao X, Jiang F, Li B, et al. The increased expression of glucose transporters in human full-term placentas from assisted reproductive technology without changes of mTOR signaling. Placenta. 2019;86:4–10. https://doi.org/10.1016/j.placenta.2019.08.087.

    Article  CAS  Google Scholar 

  13. Nakamura T, Okamoto I, Sasaki K, Yabuta Y, Iwatani C, Tsuchiya H, et al. A developmental coordinate of pluripotency among mice, monkeys and humans. Nature. 2016;537:57–62. https://doi.org/10.1038/nature19096.

    Article  CAS  Google Scholar 

  14. Bianchi DW, Wilkins-Haug LE, Enders AC, Hay ED. Origin of extraembryonic mesoderm in experimental animals: relevance to chorionic mosaicism in humans. Am J Med Genet. 1993;46:542–50. https://doi.org/10.1002/ajmg.1320460517.

    Article  CAS  Google Scholar 

  15. Enders AC, King BF. Formation and differentiation of extraembryonic mesoderm in the rhesus monkey. Am J Anat. 1988;181:327–40. https://doi.org/10.1002/aja.1001810402.

    Article  CAS  Google Scholar 

  16. Tan S, Pektaş MK, Arslan H. Sonographic evaluation of the yolk sac. J Ultrasound Med. 2012;31:87–95. https://doi.org/10.7863/jum.2012.31.1.87.

    Article  Google Scholar 

  17. Freyer C, Renfree MB. The mammalian yolk sac placenta. J Exp Zoolog B Mol Dev Evol. 2009;312:545–54. https://doi.org/10.1002/jez.b.21239.

    Article  Google Scholar 

  18. Jones CJ, Jauniaux E. Ultrastructure of the materno-embryonic interface in the first trimester of pregnancy. Micron Oxf Engl. 1993;1995(26):145–73. https://doi.org/10.1016/0968-4328(95)00002-l.

    Article  Google Scholar 

  19. de Sousa Lopes SMC, Mummery CL. Differentiation in early development. Essent. Stem Cell Biol., Elsevier; 2014, p. 121–39. https://doi.org/10.1016/B978-0-12-409503-8.00010-X.

  20. Carter AM. IFPA Senior Award Lecture: mammalian fetal membranes. Placenta. 2016;48:S21-30. https://doi.org/10.1016/j.placenta.2015.10.012.

    Article  Google Scholar 

  21. Jauniaux E, Moscoso JG. Morphology and significance of the human yolk sac. In: Barnea ER, Hustin J, Jauniaux E, editors. First twelve weeks gestation, Berlin, Heidelberg: Springer Berlin Heidelberg; 1992, p. 192–213. https://doi.org/10.1007/978-3-642-84385-3_11.

  22. Sauerbrei E, Cooperberg PL, Poland BJ. Ultrasound demonstration of the normal fetal yolk sac. J Clin Ultrasound. 1980;8:217–20. https://doi.org/10.1002/jcu.1870080306.

    Article  CAS  Google Scholar 

  23. Crooij MJ, Westhuis M, Schoemaker J, Exalto N. Ultrasonographic measurement of the yolk sac. BJOG Int J Obstet Gynaecol. 1982;89:931–4. https://doi.org/10.1111/j.1471-0528.1982.tb05060.x.

    Article  CAS  Google Scholar 

  24. Barzilai M, Lyons EA, Levi CS, Lindsay DJ. Vitelline duct cyst or double yolk sac. J Ultrasound Med. 1989;8:523–6. https://doi.org/10.7863/jum.1989.8.9.523.

    Article  CAS  Google Scholar 

  25. Lindsay DJ, Lovett IS, Lyons EA, Levi CS, Zheng XH, Holt SC, et al. Yolk sac diameter and shape at endovaginal US: predictors of pregnancy outcome in the first trimester. Radiology. 1992;183:115–8. https://doi.org/10.1148/radiology.183.1.1549656.

    Article  CAS  Google Scholar 

  26. Pereda J, Monge JI, Niimi G. Two different pathways for the transport of primitive and definitive blood cells from the yolk sac to the embryo in humans. Microsc Res Tech. 2010;73:803–9. https://doi.org/10.1002/jemt.20823.

    Article  Google Scholar 

  27. Pereda J, Correr S, Motta PM. The structure of the human yolk sac: a scanning and transmission electron microscopic analysis. Arch Histol Cytol. 1994;57:107–17. https://doi.org/10.1679/aohc.57.107.

    Article  CAS  Google Scholar 

  28. Cindrova-Davies T, Jauniaux E, Elliot MG, Gong S, Burton GJ, Charnock-Jones DS. RNA-seq reveals conservation of function among the yolk sacs of human, mouse, and chicken. Proc Natl Acad Sci. 2017;114:E4753–61. https://doi.org/10.1073/pnas.1702560114.

    Article  CAS  Google Scholar 

  29. Pereda TJ, Motta PM. New advances in human embryology: morphofunctional relationship between the embryo and the yolk sac. Med Electron Microsc Off J Clin Electron Microsc Soc Jpn. 1999;32:67–78. https://doi.org/10.1007/s007950050011.

    Article  Google Scholar 

  30. Jordan HE. A further study of the human umbilical vesicle. Anat Rec. 1910;4:341–53. https://doi.org/10.1002/ar.1090040903.

    Article  Google Scholar 

  31. Tavian M, Peault B. The changing cellular environments of hematopoiesis in human development in utero. Exp Hematol. 2005;33:1062–9. https://doi.org/10.1016/j.exphem.2005.06.025.

    Article  Google Scholar 

  32. Luckett WP. Origin and differentiation of the yolk sac and extraembryonic mesoderm in presomite human and rhesus monkey embryos. Am J Anat. 1978;152:59–97. https://doi.org/10.1002/aja.1001520106.

    Article  CAS  Google Scholar 

  33. Bloom W, Bartelmez GW. Hematopoiesis in young human embryos. Am J Anat. 1940;67:21–53. https://doi.org/10.1002/aja.1000670103.

    Article  Google Scholar 

  34. Takashina T. Histology of the secondary human yolk sac with special reference to hematopoiesis. In: Nogales FF, editor. Hum. Yolk sac yolk sac tumors, Berlin, Heidelberg: Springer Berlin Heidelberg; 1993, p. 48–69. https://doi.org/10.1007/978-3-642-77852-0_3.

  35. Ivanovs A, Rybtsov S, Ng ES, Stanley EG, Elefanty AG, Medvinsky A. Human haematopoietic stem cell development: from the embryo to the dish. Development. 2017;144:2323–37. https://doi.org/10.1242/dev.134866.

    Article  CAS  Google Scholar 

  36. Tavian M, Hallais MF, Péault B. Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Dev Camb Engl. 1999;126:793–803.

    CAS  Google Scholar 

  37. Reece EA, Pinter E, Naftolin F. Experimental models of injury in the mammalian yolk sac. In: Nogales FF, editor. Hum. Yolk sac yolk sac tumors, Berlin, Heidelberg: Springer Berlin Heidelberg; 1993, p. 135–60. https://doi.org/10.1007/978-3-642-77852-0_8.

  38. Fuss A. Über die Geschlechtszellen des Menschen und der Säugetiere. Arch Für Mikrosk Anat. 1912;81:a1-23. https://doi.org/10.1007/BF02980550.

    Article  Google Scholar 

  39. De Felici M. Origin, migration, and proliferation of human primordial germ cells. In: Coticchio G, Albertini DF, De Santis L, editors. Oogenesis, London: Springer London; 2013, p. 19–37. https://doi.org/10.1007/978-0-85729-826-3_2.

  40. Carter AM, Enders AC. Placentation in mammals: definitive placenta, yolk sac, and paraplacenta. Theriogenology. 2016;86:278–87. https://doi.org/10.1016/j.theriogenology.2016.04.041.

    Article  CAS  Google Scholar 

  41. Pereda J, Niimi G. Embryonic erythropoiesis in human yolk sac: two different compartments for two different processes. Microsc Res Tech. 2008;71:856–62. https://doi.org/10.1002/jemt.20627.

    Article  Google Scholar 

  42. Hesseldahl H, Larsen JF. Ultrastructure of human yolk sac: endoderm, mesenchyme, tubules and mesothelium. Am J Anat. 1969;126:315–35. https://doi.org/10.1002/aja.1001260306.

    Article  CAS  Google Scholar 

  43. Gitlin D, Perricelli A. Synthesis of serum albumin, prealbumin, α-foetoprotein, α1-antitrypsin and transferrin by the human yolk sac. Nature. 1970;228:995–7. https://doi.org/10.1038/228995a0.

    Article  CAS  Google Scholar 

  44. Shi WK, Hopkins B, Thompson S, Heath JK, Luke BM, Graham CF. Synthesis of apolipoproteins, alphafoetoprotein, albumin, and transferrin by the human foetal yolk sack and other foetal organs. J Embryol Exp Morphol. 1985;85:191–206.

    CAS  Google Scholar 

  45. Gulbis B, Jauniaux E, Jurkovic D, Thiry P, Campbell S, Ooms HA. Determination of protein pattern in embryonic cavities of human early pregnancies: a means to understand materno-embryonic exchanges. Hum Reprod. 1992;7:886–9. https://doi.org/10.1093/oxfordjournals.humrep.a137755.

    Article  CAS  Google Scholar 

  46. Buffe D, Rimbaut C, Gaillard JA. α-Fetoprotein and other proteins in the human yolk sac. In: Nogales FF, editor. Hum. Yolk sac yolk sac tumors, Berlin, Heidelberg: Springer Berlin Heidelberg; 1993, p. 109–25. https://doi.org/10.1007/978-3-642-77852-0_6.

  47. Murray SA, Morgan JL, Kane C, Sharma Y, Heffner CS, Lake J, et al. Mouse gestation length is genetically determined. PLoS ONE. 2010;5: e12418. https://doi.org/10.1371/journal.pone.0012418.

    Article  CAS  Google Scholar 

  48. Jollie WP. Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology. 1990;41:361–81. https://doi.org/10.1002/tera.1420410403.

    Article  CAS  Google Scholar 

  49. Hafez S. Comparative placental anatomy. Prog. Mol. Biol. Transl. Sci., vol. 145, Elsevier; 2017, p. 1–28. https://doi.org/10.1016/bs.pmbts.2016.12.001.

  50. Beckman DA, Koszalka TR, Jensen M, Brent RL. Experimental manipulation of the rodent visceral yolk sac. Teratology. 1990;41:395–404. https://doi.org/10.1002/tera.1420410405.

    Article  CAS  Google Scholar 

  51. Bevilacqua E, Lorenzon AR, Bandeira CL, Hoshida MS. Biology of the ectoplacental cone. Guide Investig. Mouse Pregnancy, Elsevier; 2014, p. 113–24. https://doi.org/10.1016/B978-0-12-394445-0.00010-2.

  52. Carter AM, Pijnenborg R. Emil Selenka on the embryonic membranes of the mouse and placentation in gibbons and orangutans. Placenta. 2016;37:65–71. https://doi.org/10.1016/j.placenta.2015.11.005.

    Article  CAS  Google Scholar 

  53. Dobreva MP, Lhoest L, Pereira PNG, Umans L, Camus A, Chuva de Sousa Lopes SM, et al. Periostin as a biomarker of the amniotic membrane. Stem Cells Int 2012;2012:987185. https://doi.org/10.1155/2012/987185.

  54. Pereira PN, Dobreva MP, Graham L, Huylebroeck D, Lawson KA, Zwijsen A. Amnion formation in the mouse embryo: the single amniochorionic fold model. BMC Dev Biol. 2011;11:48. https://doi.org/10.1186/1471-213X-11-48.

    Article  CAS  Google Scholar 

  55. Dobreva MP, Pereira PNG, Deprest J, Zwijsen A. On the origin of amniotic stem cells: of mice and men. Int J Dev Biol. 2010;54:761–77. https://doi.org/10.1387/ijdb.092935md.

    Article  CAS  Google Scholar 

  56. King BF, Enders AC. Comparative development of the mammalian yolk sac. In: Nogales FF, editor. Hum. Yolk sac yolk sac tumors, Berlin, Heidelberg: Springer Berlin Heidelberg; 1993, p. 1–32. https://doi.org/10.1007/978-3-642-77852-0_1.

  57. Niimi G, Usuda N, Shinzato M, Nagamura Y. A light and electron microscopic study of the mouse visceral yolk sac endodermal cells in the middle and late embryonic periods, showing the possibility of definitive erythropoiesis. Ann Anat - Anat Anz. 2002;184:425–9. https://doi.org/10.1016/S0940-9602(02)80073-5.

    Article  Google Scholar 

  58. Zon L. Developmental biology of hematopoiesis. Blood. 1995;86:2876–91. https://doi.org/10.1182/blood.V86.8.2876.2876.

    Article  CAS  Google Scholar 

  59. Yamane T. Mouse yolk sac hematopoiesis. Front Cell Dev Biol. 2018;6:80. https://doi.org/10.3389/fcell.2018.00080.

    Article  Google Scholar 

  60. Tober J, Koniski A, McGrath KE, Vemishetti R, Emerson R, de Mesy-Bentley KKL, et al. The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood. 2007;109:1433–41. https://doi.org/10.1182/blood-2006-06-031898.

    Article  CAS  Google Scholar 

  61. Palis J, Robertson S, Kennedy M, Wall C, Keller G. Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Dev Camb Engl. 1999;126:5073–84.

    CAS  Google Scholar 

  62. Takahashi K, Yamamura F, Naito M. Differentiation, maturation, and proliferation of macrophages in the mouse yolk sac: a light-microscopic, enzyme-cytochemical, immunohistochemical, and ultrastructural study. J Leukoc Biol. 1989;45:87–96. https://doi.org/10.1002/jlb.45.2.87.

    Article  CAS  Google Scholar 

  63. Yamane T. Cellular Basis of Embryonic Hematopoiesis and its implications in prenatal erythropoiesis. Int J Mol Sci. 2020;21:9346. https://doi.org/10.3390/ijms21249346.

    Article  CAS  Google Scholar 

  64. Jaffredo T, Nottingham W, Liddiard K, Bollerot K, Pouget C, Debruijn M. From hemangioblast to hematopoietic stem cell: an endothelial connection? Exp Hematol. 2005;33:1029–40. https://doi.org/10.1016/j.exphem.2005.06.005.

    Article  Google Scholar 

  65. Neo WH, Meng Y, Rodriguez-Meira A, Fadlullah MZH, Booth CAG, Azzoni E, et al. Ezh2 is essential for the generation of functional yolk sac derived erythro-myeloid progenitors. Nat Commun. 2021;12:7019. https://doi.org/10.1038/s41467-021-27140-8.

    Article  CAS  Google Scholar 

  66. Brent RL, Beckman DA, Jensen M, Koszalka TR. Experimental yolk sac dysfunction as a model for studying nutritional disturbances in the embryo during early organogenesis. Teratology. 1990;41:405–13. https://doi.org/10.1002/tera.1420410406.

    Article  CAS  Google Scholar 

  67. Farese RV, Ruland SL, Flynn LM, Stokowski RP, Young SG. Knockout of the mouse apolipoprotein B gene results in embryonic lethality in homozygotes and protection against diet-induced hypercholesterolemia in heterozygotes. Proc Natl Acad Sci. 1995;92:1774–8. https://doi.org/10.1073/pnas.92.5.1774.

    Article  CAS  Google Scholar 

  68. Bielinska M, Narita N, Wilson DB. Distinct roles for visceral endoderm during embryonic mouse development. Int J Dev Biol. 1999;43:183–205.

    CAS  Google Scholar 

  69. Terasawa Y, Cases SJ, Wong JS, Jamil H, Jothi S, Traber MG, et al. Apolipoprotein B-related gene expression and ultrastructural characteristics of lipoprotein secretion in mouse yolk sac during embryonic development. J Lipid Res. 1999;40:1967–77.

    Article  CAS  Google Scholar 

  70. Ekblom P, Thesleff I. Control of kidney differentiation by soluble factors secreted by the embryonic liver and the yolk sac. Dev Biol. 1985;110:29–38. https://doi.org/10.1016/0012-1606(85)90060-0.

    Article  CAS  Google Scholar 

  71. Salbaum JM, Finnell RH, Kappen C. Regulation of folate receptor 1 gene expression in the visceral endoderm. Birt Defects Res A Clin Mol Teratol. 2009;85:303–13. https://doi.org/10.1002/bdra.20537.

    Article  CAS  Google Scholar 

  72. Seo MJ, Lim JH, Kim D-H, Bae H-R. Loss of aquaporin-3 in placenta and fetal membranes induces growth restriction in mice. Dev Reprod. 2018;22:263–73. https://doi.org/10.12717/DR.2018.22.3.263.

    Article  Google Scholar 

  73. Kim J, Mohanty S, Ganesan LP, Hua K, Jarjoura D, Hayton WL, et al. FcRn in the yolk sac endoderm of mouse is required for IgG transport to fetus. J Immunol. 2009;182:2583–9. https://doi.org/10.4049/jimmunol.0803247.

    Article  CAS  Google Scholar 

  74. Burton GJ, Hempstock J, Jauniaux E. Nutrition of the human fetus during the first trimester—a review. Placenta. 2001;22:S70–7. https://doi.org/10.1053/plac.2001.0639.

    Article  Google Scholar 

  75. Campbell J, Wathen N, Perry G, Soneji S, Sourial N, Chard T. The coelomic cavity: an important site of materno-fetal nutrient exchange in the first trimester of pregnancy. BJOG Int J Obstet Gynaecol. 1993;100:765–7. https://doi.org/10.1111/j.1471-0528.1993.tb14271.x.

    Article  CAS  Google Scholar 

  76. Bloise E, Ortiga-Carvalho TM, Reis FM, Lye SJ, Gibb W, Matthews SG. ATP-binding cassette transporters in reproduction: a new frontier. Hum Reprod Update 2015:dmv049. https://doi.org/10.1093/humupd/dmv049.

  77. Imperio GE, Javam M, Lye P, Constantinof A, Dunk CE, Reis FM, et al. Gestational age-dependent gene expression profiling of ATP-binding cassette transporters in the healthy human placenta. J Cell Mol Med. 2019;23:610–8. https://doi.org/10.1111/jcmm.13966.

    Article  CAS  Google Scholar 

  78. Fontes KN, Reginatto MW, Silva NL, Andrade CBV, Bloise FF, Monteiro VRS, et al. Dysregulation of placental ABC transporters in a murine model of malaria-induced preterm labor. Sci Rep. 2019;9:11488. https://doi.org/10.1038/s41598-019-47865-3.

    Article  CAS  Google Scholar 

  79. Eustaquio Do Imperio G, Lye P, Bloise E, Matthews SG. Function of multidrug resistance transporters is disrupted by infection mimics in human brain endothelial cells. Tissue Barriers. 2021;9:1860616. https://doi.org/10.1080/21688370.2020.1860616.

    Article  CAS  Google Scholar 

  80. Bloise E, Matthews SG. Multidrug resistance P-glycoprotein (P-gp), glucocorticoids, and the stress response. Stress Physiol. Biochem. Pathol., Elsevier; 2019, p. 227–41. https://doi.org/10.1016/B978-0-12-813146-6.00019-9.

  81. Martinelli LM, Fontes KN, Reginatto MW, Andrade CBV, Monteiro VRS, Gomes HR, et al. Malaria in pregnancy regulates P-glycoprotein (P-gp/Abcb1a) and ABCA1 efflux transporters in the mouse visceral yolk sac. J Cell Mol Med. 2020;24:10636–47. https://doi.org/10.1111/jcmm.15682.

    Article  CAS  Google Scholar 

  82. Martinelli LM, Reginatto MW, Fontes KN, Andrade CBV, Monteiro VRS, Gomes HR, et al. Breast cancer resistance protein (Bcrp/Abcg2) is selectively modulated by lipopolysaccharide (LPS) in the mouse yolk sac. Reprod Toxicol. 2020;98:82–91. https://doi.org/10.1016/j.reprotox.2020.09.001.

    Article  CAS  Google Scholar 

  83. Bloise E, Bhuiyan M, Audette MC, Petropoulos S, Javam M, Gibb W, et al. Prenatal endotoxemia and placental drug transport in the mouse: placental size-specific effects. PLoS ONE. 2013;8: e65728. https://doi.org/10.1371/journal.pone.0065728.

    Article  CAS  Google Scholar 

  84. Reginatto MW, Fontes KN, Monteiro VRS, Silva NL, Andrade CBV, Gomes HR, et al. Effect of sublethal prenatal endotoxaemia on murine placental transport systems and lipid homeostasis. Front Microbiol. 2021;12: 706499. https://doi.org/10.3389/fmicb.2021.706499.

    Article  Google Scholar 

  85. Brent RL, Fawcett LB. Nutritional studies of the embryo during early organogenesis with normal embryos and embryos exhibiting yolk sac dysfunction. J Pediatr. 1998;132:S6-16. https://doi.org/10.1016/S0022-3476(98)70522-0.

    Article  CAS  Google Scholar 

  86. Mony VK, Benjamin S, O’Rourke EJ. A lysosome-centered view of nutrient homeostasis. Autophagy. 2016;12:619–31. https://doi.org/10.1080/15548627.2016.1147671.

    Article  CAS  Google Scholar 

  87. Jones CJP, Choudhury RH, Aplin JD. Tracking nutrient transfer at the human maternofetal interface from 4 weeks to term. Placenta. 2015;36:372–80. https://doi.org/10.1016/j.placenta.2015.01.002.

    Article  CAS  Google Scholar 

  88. Saitou M, Yamaji M. Primordial germ cells in mice. 2012;4. https://doi.org/10.1101/cshperspect.a008375.

Download references

Funding

This work was supported by funding from Coordenação de Aperfeiçoamento Pessoal de Nível Superior (CAPES, finance Code 001) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, 310578/2020–5).

Author information

Authors and Affiliations

  1. Department of Morphology, N3-292, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    Lilian M. Martinelli, Victor J. H. Payano & Enrrico Bloise

  2. Department of Woman, Child, and General and Specialized Surgery, University of Campania “Luigi Vanvitelli”, Naples, Italy

    Antonio Carucci

  3. Department of Health Sciences, Carleton University, Ottawa, Canada

    Kristin L. Connor

Authors
  1. Lilian M. Martinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Antonio Carucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor J. H. Payano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kristin L. Connor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Enrrico Bloise
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Enrrico Bloise.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

All authors have stated for consent of publication.

Conflict of Interest

The authors declare no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martinelli, L.M., Carucci, A., Payano, V.J.H. et al. Translational Comparison of the Human and Mouse Yolk Sac Development and Function. Reprod. Sci. 30, 41–53 (2023). https://doi.org/10.1007/s43032-022-00872-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43032-022-00872-8

Keywords

Search

Navigation