Decidualisation and placentation defects are a major cause of age-related reproductive decline

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Woods, Laura ^a,b   Perez Garcia, Vicente ^a,b   Kieckbusch, Jens ^c   Wang, Xiaoqiu ^d   Demayo, Francesco ^d   Colucci, Francesco ^c   Hemberger, Myriam ^a,b  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME; EMBRYONIC DEVELOPMENT; FEMALE; PREGNANCY; REPRODUCTIVE SUCCESS; RODENT;

ADULT; AGING; ANIMAL EXPERIMENT; EMBRYO DEVELOPMENT; FEMALE; HUMAN; MATERNAL AGE; MOUSE; NONHUMAN; PLACENTA DEVELOPMENT; PREGNANCY; REPRODUCTIVE SUCCESS; UTERUS; AGE; ANIMAL; C57BL MOUSE; CELL CULTURE; DECIDUA; GENE EXPRESSION PROFILING; GENETICS; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PLACENTA; PREGNANCY COMPLICATION; PROCEDURES; REPRODUCTION;

MAMMALIA; MUS;

AGE FACTORS; AGING; ANIMALS; CELLS, CULTURED; DECIDUA; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MALE; MATERNAL AGE; MICE, INBRED C57BL; PLACENTA; PLACENTATION; PREGNANCY; PREGNANCY COMPLICATIONS; REPRODUCTION; UTERUS;

EID: 85028929632     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00308-x     Document Type: Article

References (70)

1. Martin, J. A., Hamilton, B. E., Osterman, M. J., Curtin, S. C. & Matthews, T. J. Births: final data for 2013. Natl. Vital Stat. Rep. 64, 1-65 (2015)
2. Johnson, J. A. & Tough, S., Society of Obstetricians and Gynaecologists of Canada. Delayed child-bearing. J. Obstet. Gynaecol. Can. 34, 80-93 (2012)
3. Abel, E. L., Kruger, M. & Burd, L. Effects of maternal and paternal age on Caucasian and Native American preterm births and birth weights. Am. J. Perinatol. 19, 49-54 (2002)
4. Jolly, M., Sebire, N., Harris, J., Robinson, S. & Regan, L. The risks associated with pregnancy in women aged 35 years or older. Hum. Reprod. 15, 2433-2437 (2000)
5. Delbaere, I. et al. Pregnancy outcome in primiparae of advanced maternal age. Eur. J. Obstet. Gynecol. Reprod. Biol. 135, 41-46 (2007)
6. Hansen, J. P. Older maternal age and pregnancy outcome: a review of the literature. Obstet. Gynecol. Surv. 41, 726-742 (1986)
7. Salihu, H. M., Wilson, R. E., Alio, A. P. & Kirby, R. S. Advanced maternal age and risk of antepartum and intrapartum stillbirth. J. Obstet. Gynaecol. Res. 34, 843-850 (2008)
8. Astolfi, P. & Zonta, L. A. Risks of preterm delivery and association with maternal age, birth order, and fetal gender. Hum. Reprod. 14, 2891-2894 (1999)
9. Lamminpaa, R., Vehvilainen-Julkunen, K., Gissler, M. & Heinonen, S. Preeclampsia complicated by advanced maternal age: a registry-based study on primiparous women in Finland 1997-2008. BMC Pregnancy Childbirth 12, 47 (2012)
10. Jacobsson, B., Ladfors, L. & Milsom, I. Advanced maternal age and adverse perinatal outcome. Obstet. Gynecol. 104, 727-733 (2004)
11. Reefhuis, J. & Honein, M. A. Maternal age and non-chromosomal birth defects, Atlanta-1968-2000: teenager or thirty-something, who is at risk Birth Defects Res 70, 572-579 (2004)
12. Hollier, L. M., Leveno, K. J., Kelly, M. A., DD, M. C. & Cunningham, F. G. Maternal age and malformations in singleton births. Obstet. Gynecol. 96, 701-706 (2000)
13. Schulkey, C. E. et al. The maternal-age-associated risk of congenital heart disease is modifiable. Nature. 520, 230-233 (2015)
14. Norwitz, E. R. Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod. Biomed. Online 13, 591-599 (2006)
15. Hemberger, M. & Cross, J. C. Genes governing placental development. Trends. Endocrinol. Metab. 12, 162-168 (2001)
16. Holinka, C. F., Tseng, Y. C. & Finch, C. E. Reproductive aging in C57BL/6J mice: plasma progesterone, viable embryos and resorption frequency throughout pregnancy. Biol. Reprod. 20, 1201-1211 (1979)
17. Lopes, F. L. et al. Reproductive and epigenetic outcomes associated with aging mouse oocytes. Hum. Mol. Genet. 18, 2032-2044 (2009)
18. Biggers, J. D., Finn, C. A. & Mc, L. A. Long-term reproductive performance of female mice. II. Variation of litter size with parity. J. Reprod. Fertil. 3, 313-330 (1962)
19. Copp, A. J. Death before birth: clues from gene knockouts and mutations. Trends Genet. 11, 87-93 (1995)
20. Watson, E. D. & Cross, J. C. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 20, 180-193 (2005)
21. Weissbein, U., Schachter, M., Egli, D. & Benvenisty, N. Analysis of chromosomal aberrations and recombination by allelic bias in RNA-Seq. Nat. Commun. 7, 12144 (2016)
22. Ramathal, C. Y., Bagchi, I. C., Taylor, R. N. & Bagchi, M. K. Endometrial decidualization: of mice and men. Semin. Reprod. Med. 28, 17-26 (2010)
23. Lee, K. Y. et al. Bmp2 is critical for the murine uterine decidual response. Mol. Cell Biol. 27, 5468-5478 (2007)
24. Paria, B. C. et al. Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc. Natl Acad. Sci. USA 98, 1047-1052 (2001)
25. Rahman, M. A. et al. Hoxa-10 deficiency alters region-specific gene expression and perturbs differentiation of natural killer cells during decidualization. Dev. Biol. 290, 105-117 (2006)
26. Kapur, S., Tamada, H., Dey, S. K. & Andrews, G. K. Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol. Reprod. 46, 208-219 (1992)
27. Inoue, A., Takeuchi, S. & Takahashi, S. Insulin-like growth factor-I stimulated DNA replication in mouse endometrial stromal cells. J. Reprod. Dev. 51, 305-313 (2005)
28. Barber, E. M. & Pollard, J. W. The uterine NK cell population requires IL-15 but these cells are not required for pregnancy nor the resolution of a Listeria monocytogenes infection. J. Immunol. 171, 37-46 (2003)
29. Ashkar, A. A. et al. Assessment of requirements for IL-15 and IFN regulatory factors in uterine NK cell differentiation and function during pregnancy. J. Immunol. 171, 2937-2944 (2003)
30. Henemyre, C. & Markoff, E. Decidualization and expression of insulin-like growth factor-I and insulin-like growth factor binding protein-4 in the periimplantation mouse uterus. Biol. Reprod. 58, 801-806 (1998)
31. Murphy, L. J. & Ghahary, A. Uterine insulin-like growth factor-1: regulation of expression and its role in estrogen-induced uterine proliferation. Endocr. Rev. 11, 443-453 (1990)
32. Wang, Q. et al. Wnt6 is essential for stromal cell proliferation during decidualization in mice. Biol. Reprod. 88, 5 (2013)
33. Finn, C. A. Reproductive capacity and litter size in mice: effect of age and environment. J. Reprod. Fertil. 6, 205-214 (1963)
34. Shehata, H. M., Hoebe, K. & Chougnet, C. A. The aged nonhematopoietic environment impairs natural killer cell maturation and function. Aging Cell 14, 191-199 (2015)
35. Moffett, A. & Colucci, F. Uterine NK cells: active regulators at the maternal-fetal interface. J. Clin. Invest. 124, 1872-1879 (2014)
36. Madeja, Z. et al. Paternal MHC expression on mouse trophoblast affects uterine vascularization and fetal growth. Proc. Natl Acad. Sci. USA 108, 4012-4017 (2011)
37. Kieckbusch, J., Gaynor, L. M., Moffett, A. & Colucci, F. MHC-dependent inhibition of uterine NK cells impedes fetal growth and decidual vascular remodelling. Nat. Commun. 5, 3359 (2014)
38. Tagliani, E. et al. Coordinate regulation of tissue macrophage and dendritic cell population dynamics by CSF-1. J. Exp. Med. 208, 1901-1916 (2011)
39. Guo, Z., Tilburgs, T., Wong, B. & Strominger, J. L. Dysfunction of dendritic cells in aged C57BL/6 mice leads to failure of natural killer cell activation and of tumor eradication. Proc. Natl Acad. Sci. USA 111, 14199-14204 (2014)
40. Nelson, A. C., Mould, A. W., Bikoff, E. K. & Robertson, E. J. Single-cell RNA-seq reveals cell type-specific transcriptional signatures at the maternal-foetal interface during pregnancy. Nat. Commun. 7, 11414 (2016)
41. Benson, G. V. et al. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 122, 2687-2696 (1996)
42. Gendron, R. L. et al. Abnormal uterine stromal and glandular function associated with maternal reproductive defects in Hoxa-11 null mice. Biol. Reprod. 56, 1097-1105 (1997)
43. Franco, H. L. et al. WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J. 25, 1176-1187 (2011)
44. Tan, Y. et al. HB-EGF directs stromal cell polyploidy and decidualization via cyclin D3 during implantation. Dev. Biol. 265, 181-195 (2004)
45. Large, M. J. et al. The epidermal growth factor receptor critically regulates endometrial function during early pregnancy. PLoS Genet. 10, e1004451 (2014)
46. Jeong, J. W. et al. Foxa2 is essential for mouse endometrial gland development and fertility. Biol. Reprod. 83, 396-403 (2010)
47. Hantak, A. M., Bagchi, I. C. & Bagchi, M. K. Role of uterine stromal-epithelial crosstalk in embryo implantation. Int. J. Dev. Biol. 58, 139-146 (2014)
48. Pawar, S. et al. STAT3 regulates uterine epithelial remodeling and epithelial-stromal crosstalk during implantation. Mol. Endocrinol. 27, 1996-2012 (2013)
49. Finn, C. A. & Martin, L. Patterns of cell division in the mouse uterus during early pregnancy. J. Endocrinol. 39, 593-597 (1967)
50. Wang, H. & Dey, S. K. Roadmap to embryo implantation: clues from mouse models. Nat. Rev. Genet. 7, 185-199 (2006)
51. Rubel, C. A. et al. Research resource: genome-wide profiling of progesterone receptor binding in the mouse uterus. Mol. Endocrinol. 26, 1428-1442 (2012)
52. Gertz, J. et al. Distinct properties of cell-type-specific and shared transcription factor binding sites. Mol. Cell 52, 25-36 (2013)
53. Hewitt, S. C. et al. Research resource: whole-genome estrogen receptor alpha binding in mouse uterine tissue revealed by ChIP-seq. Mol. Endocrinol. 26, 887-898 (2012)
54. Mulac-Jericevic, B., Mullinax, R. A., DeMayo, F. J., Lydon, J. P. & Conneely, O. M. Subgroup of reproductive functions of progesterone mediated by progesterone receptor-B isoform. Science 289, 1751-1754 (2000)
55. Liu, T. & Ogle, T. F. Signal transducer and activator of transcription 3 is expressed in the decidualized mesometrium of pregnancy and associates with the progesterone receptor through protein-protein interactions. Biol. Reprod. 67, 114-118 (2002)
56. Lee, J. H. et al. Signal transducer and activator of transcription-3 (Stat3) plays a critical role in implantation via progesterone receptor in uterus. FASEB J. 27, 2553-2563 (2013)
57. Sun, X., Bartos, A., Whitsett, J. A. & Dey, S. K. Uterine deletion of Gp130 or Stat3 shows implantation failure with increased estrogenic responses. Mol. Endocrinol. 27, 1492-1501 (2013)
58. Talbert, G. B. & Krohn, P. L. Effect of maternal age on viability of ova and uterine support of pregnancy in mice. J. Reprod. Fertil. 11, 399-406 (1966)
59. Biggers, J. D., Finn, C. A. & Mc, L. A. Long-term reproductive performance of female mice. I. Effect of removing one ovary. J. Reprod. Fertil. 3, 303-312 (1962)
60. Tagliani, E. & Erlebacher, A. Dendritic cell function at the maternal-fetal interface. Expert Rev. Clin. Immunol. 7, 593-602 (2011)
61. Krey, G. et al. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J. Mol. Med. 86, 999-1011 (2008)
62. Plaks, V. et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J. Clin. Invest. 118, 3954-3965 (2008)
63. Finn, C. A. The initiation of the decidual cell reaction in the uterus of the aged mouse. J. Reprod. Fertil. 11, 423-428 (1966)
64. Mukherjee, A. et al. Steroid receptor coactivator 2 is critical for progesterone-dependent uterine function and mammary morphogenesis in the mouse. Mol. Cell Biol. 26, 6571-6583 (2006)
65. Robker, R. L. et al. Identification of sites of STAT3 action in the female reproductive tract through conditional gene deletion. PLoS ONE 9, e101182 (2014)
66. Chong, H. P. et al. Age-related changes in murine myometrial transcript profile are mediated by exposure to the female sex hormones. Aging Cell 15, 177-180 (2016)
67. Kong, S. et al. Determinants of uterine aging: lessons from rodent models. Sci. China Life Sci. 55, 687-693 (2012)
68. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009)
69. Eden, E., Navon, R., Steinfeld, I., Lipson, D. & Yakhini, Z. GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists. BMC Bioinform. 10, 48 (2009)
70. Afonso, S., Tovar, C., Romagnano, L. & Babiarz, B. Control and expression of cystatin C by mouse decidual cultures. Mol. Reprod. Dev. 61, 155-163 (2002).