Uterine natural killer cells severely decrease in number at gestation day 6 in Mice

Biology of Reproduction

Volumn 89, Issue 4, 2013, Pages

  Takashima, Akiko ^a   Ishikawa, Fumio ^b   Kuwabara, Taku ^b   Tanaka, Yuriko ^b   Kinoshita, Toshihiko ^a   Ito, Motohiro ^a   Kakiuchi, Terutaka ^b  

^a TOHO UNIVERSITY SAKURA MEDICAL CENTER   (Japan)

^b TOHO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Implantation; Natural killer cell; Pregnancy; Rodents (rats, mice, guinea pigs, voles); Uterus

Indexed keywords

CD11B ANTIGEN; CD27 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; GAMMA INTERFERON; INTERLEUKIN 15; INTERLEUKIN 7 RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL PROLIFERATION; CYTOKINE PRODUCTION; DECIDUALIZATION; FEMALE; LEUKOCYTE COUNT; MOUSE; NATURAL KILLER CELL; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; UTERINE NATURAL KILLER CELL;

GUINEA PIGS; IMPLANTATION; MICE; NATURAL KILLER CELL; PREGNANCY; RODENTS (RATS; UTERUS; VOLES);

ANIMALS; ANTIGENS, CD; BIOLOGICAL MARKERS; CHEMOKINE CXCL12; EMBRYO IMPLANTATION; FEMALE; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INFLAMMATION MEDIATORS; KILLER CELLS, NATURAL; LUTEAL PHASE; MICE; MICE, INBRED BALB C; PLACENTATION; PREGNANCY; PREGNANCY MAINTENANCE; RECEPTORS, CXCR4; SPECIFIC PATHOGEN-FREE ORGANISMS; UTERUS;

EID: 84896838466     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.109009     Document Type: Article

References (38)

1. Santoni A, Carlino C, Gismondi A. Uterine NK cell development, migration and function. Reprod Biomed Online 2008; 16:202-210.
2. Reeves RK, Gillis J, Wong FE, Yu Y, Connole M, Johnson RP. CD16-natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 2010; 115: 4439-4446.
3. Sun JC, Beilke JN, Lanier LL. Adaptive immune features of natural killer cells. Nature 2009; 457:557-561.
4. Moffett A, Loke C. Immunology of placentation in eutherian mammals. Nat Rev Immunol 2006; 6:584-594.
5. Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 2006; 214:161-185.
6. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol 2002; 2:656-663.
7. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12: 1065-1074.
8. Guimond MJ, Luross JA, Wang B, Terhorst C, Danial S, Croy BA. Absence of natural killer cells during murine pregnancy is associated with reproductive compromise in TgE26 mice. Biol Reprod 1997; 56:169-179.
9. Guimond MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 1998; 187:217-223.
10. Greenwood JD, Minhas K, di Santo JP, Makita M, Kiso Y, Croy BA. Ultrastructural studies of implantation sites from mice deficient in uterine natural killer cells. Placenta 2000; 21:693-702.
11. Ashkar AA, Croy BA. Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod 1999; 61:493-502.
12. Paffaro VA Jr, Bizinotto MC, Joazeiro PP, Yamada AT. Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 2003; 24:479-488.
13. Ashkar AA, Di Santo JP, Croy BA. Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J Exp Med 2000; 192:259-270.
14. Manaster I, Mandelboim O. The unique properties of human NK cells in the uterine mucosa. Placenta 2008; 29(Suppl A):S60-S66.
15. Croy BA, Esadeg S, Chantakru S, van den Heuvel M, Paffaro VA, He H, Black GP, Ashkar AA, Kiso Y, Zhang J. Update on pathways regulating the activation of uterine natural killer cells, their interactions with decidual spiral arteries and homing of their precursors to the uterus. J Reprod Immunol 2003; 59:175-191.
16. Delgado SR, McBey BA, Yamashiro S, Fujita J, Kiso Y, Croy BA. Accounting for the peripartum loss of granulated metrial gland cells, a natural killer cell population, from the pregnant mouse uterus. J Leukoc Biol 1996; 59:262-269.
17. Chantakru S, Miller C, Roach LE, Kuziel WA, Maeda N, Wang WC, Evans SS, Croy BA. Contributions from self-renewal and trafficking to the uterine NK cell population of early pregnancy. J Immunol 2002; 168: 22-28.
18. Aritomi K, Kuwabara T, Tanaka Y, Nakano H, Yasuda T, Ishikawa F, Kurosawa H, Kakiuchi T. Altered antibody production and helper T cell function in mice lacking chemokines CCL19 and CCL21-Ser. Microbiol Immunol 2010; 54:691-701.
19. Kuwabara T, Ishikawa F, Yasuda T, Aritomi K, Nakano H, Tanaka Y, Okada Y, Lipp M, Kakiuchi T. CCR7 ligands are required for development of experimental autoimmune encephalomyelitis through generating IL-23-dependent Th17 cells. J Immunol 2009; 183:2513-2521.
20. Chiossone L, Chaix J, Fuseri N, Roth C, Vivier E, Walzer T. Maturation of mouse NK cells is a 4-stage developmental program. Blood 2009; 113: 5488-5496.
21. Karimi K, Solano ME, Ashkar AA, Ho H, Steidle EM, McVey Neufeld KA, Hecher K, Bienenstock J, Arck PC. Regulation of pregnancy maintenance and fetal survival in mice by CD27(low) mature NK cells. J Mol Med (Berl) 2012; 90:1047-1057.
22. Zhang J, Chen Z, Fritz JH, Rochman Y, Leonard WJ, Gommerman JL, Plumb AW, Abraham N, Croy BA. Unusual timing of CD127 expression by mouse uterine natural killer cells. J Leukoc Biol 2012; 91:417-426.
23. Mallidi TV, Craig LE, Schloemann SR, Riley JK. Murine endometrial and decidual NK1.1ρ natural killer cells display a B220ρCD11cρ cell surface phenotype. Biol Reprod 2009; 81:310-318.
24. Boyman O, Krieg C, Homann D, Sprent J. Homeostatic maintenance of T cells and natural killer cells. Cell Mol Life Sci 2012; 69:1597-1608.
25. Bernardini G, Sciume G, Bosisio D, Morrone S, Sozzani S, Santoni A. CCL3 and CXCL12 regulate trafficking of mouse bone marrow NK cell subsets. Blood 2008; 111:3626-3634.
26. Noda M, Omatsu Y, Sugiyama T, Oishi S, Fujii N, Nagasawa T. CXCL12-CXCR4 chemokine signaling is essential for NK-cell development in adult mice. Blood 2011; 117:451-458.
27. Bianco J, Stephenson K, Yamada AT, Croy BA. Time-course analyses addressing the acquisition of DBA lectin reactivity in mouse lymphoid organs and uterus during the first week of pregnancy. Placenta 2008; 29: 1009-1015.
28. Yadi H, Burke S, Madeja Z, Hemberger M, Moffett A, Colucci F. Unique receptor repertoire in mouse uterine NK cells. J Immunol 2008; 181: 6140-6147.
29. Peel S. Granulated metrial gland cells. Adv Anat Embryol Cell Biol 1989; 115:1-112.
30. Prlic M, Blazar BR, Farrar MA, Jameson SC. In vivo survival and homeostatic proliferation of natural killer cells. J Exp Med 2003; 197: 967-976.
31. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, Matsuki N, Charrier K, Sedger L, Willis CR, Brasel K, Morrissey PJ, et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000; 191:771-780.
32. Fehniger TA, Suzuki K, Ponnappan A, VanDeusen JB, Cooper MA, Florea SM, Freud AG, Robinson ML, Durbin J, Caligiuri MA. Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8ρ T cells. J Exp Med 2001; 193: 219-231.
33. Kusakabe K, Otsuki Y, Kiso Y. Involvement of the fas ligand and fas system in apoptosis induction of mouse uterine natural killer cells. J Reprod Dev 2005; 51:333-340.
34. Kalkunte S, Chichester CO, Gotsch F, Sentman CL, Romero R, Sharma S. Evolution of non-cytotoxic uterine natural killer cells. Am J Reprod Immunol 2008; 59:425-432.
35. Zhang J, Chen Z, Smith GN, Croy BA. Natural killer cell-triggered vascular transformation: maternal care before birth?. Cell Mol Immunol 2011; 8:1-11.
36. Lin Y, Wang H, Wang W, Zeng S, Zhong Y, Li DJ. Prevention of embryo loss in non-obese diabetic mice using adoptive ITGA2(ρ)ISG20(ρ) natural killer-cell transfer. Reproduction 2009; 137:943-955.
37. Blasius AL, Barchet W, Cella M, Colonna M. Development and function of murine B220ρCD11cρNK1.1ρ cells identify them as a subset of NK cells. J Exp Med 2007; 204:2561-2568.
38. van den Heuvel MJ, Xie X, Tayade C, Peralta C, Fang Y, Leonard S, Paffaro VA Jr, Sheikhi AK, Murrant C, Croy BA. A review of trafficking and activation of uterine natural killer cells. Am J Reprod Immunol 2005; 54:322-331.