Leukocyte subpopulations in the uteri of leukemia inhibitory factor knockout mice during early pregnancy

Biology of Reproduction

Volumn 72, Issue 4, 2005, Pages 872-878

  Schofield, Gemma ^a,b   Kimber, Susan J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b INSTITUTE OF HUMAN GENETICS   (United Kingdom)

Author keywords

Cytokines; Immunology; Implantation; Pregnancy; Uterus

Indexed keywords

CHEMOKINE; LEUKEMIA INHIBITORY FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL COUNT; CELL MIGRATION; CONTROLLED STUDY; ENDOMETRIUM; EOSINOPHIL; FEMALE; FEMALE INFERTILITY; FIRST TRIMESTER PREGNANCY; IMMUNOCYTOCHEMISTRY; KNOCKOUT MOUSE; LEUKOCYTE; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NIDATION; NONHUMAN; PRIORITY JOURNAL; UTERUS; UTERUS CONTRACTION; UTERUS MALFORMATION;

ANIMALS; CELL MOVEMENT; EOSINOPHILS; FEMALE; GESTATIONAL AGE; INTERLEUKIN-6; KILLER CELLS, NATURAL; LEUKEMIA INHIBITORY FACTOR; LEUKOCYTES; MACROPHAGES; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; PREGNANCY; PROTEINS; STAINING AND LABELING; UTERUS;

EID: 15544377799     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.034876     Document Type: Article

References (44)

1. Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L, Stewart CL. Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 2000; 141: 4365-4372.
2. Bhatt H, Brunet LJ, Stewart CL. Uterine expression of leukemia inhibitory factor coincides with the onset of blastocyst implantation. Proc Natl Acad Sci U S A 1991; 88:11408-11412.
3. Stewart CL, Kaspar P, Brunet LJ, Bhatt H, Gadi I, Konigen F, Abbondanzo SJ. Blastocyst implantation depends on maternal expression of leukemia inhibitory factor. Nature 1992; 359:76-79.
4. Rodriguez CI, Cheng JG, Liu L, Stewart CL. Cochlin, a secreted von Willebrand factor type a domain-containing factor, is regulated by leukemia inhibitory factor in the uterus at the time of embryo implantation. Endocrinology 2004; 145:1410-1418.
5. Sherwin J, Freeman T, Stephens R, Kimber S, Smith A, Chambers I, Smith S, Sharkey A. Identification of genes regulated by Leukemia Inhibitory Factor in the mouse uterus at the time of implantation. Mol Endocrinol 2004; 18(9):2185-2195.
6. Chen B, Zhang D, Pollard JW. Progesterone regulation of the mammalian ortholog of methylcitrate dehydratase (immune response gene 1) in the uterine epithelium during implantation through the protein kinase C pathway. Mol Endocrinol 2003; 17:2340-2354.
7. Song H, Lim H, Das SK, Paria BC, Dey SK. Dysregulation of EGF family of growth factors and COX-2 in the uterus during the preattachment and attachment reactions of the blastocyst with the luminal epithelium correlates with implantation failure in LIF-deficient mice. Mol Endocrinol 2000; 14:1147-1161.
8. Daikoku T, Song H, Guo Y, Riesewijk A, Mosselman S, Das SK, Dey SK. Uterine Msx-1 and Wnt4 signaling becomes aberrant in mice with the loss of leukemia inhibitory factor or Hoxa-10: Evidence for a novel cytokine-homeobox- Wnt signaling in implantation. Mol Endocrinol 2004; 18(5):1238-1250.
9. Fouladi Nashta AA, Andreu CV, Nijjar N, Heath JK, Kimber SJ. Role of leukemia inhibitor factor (LIF) in decidualization of murine uterine stromal cells in vitro. J Endocrinol 2004; 181:477-492.
10. Giess R, Tanasescu I, Steck T, Sendtner M. Leukemia inhibitory factor gene mutations in infertile women. Mol Hum Reprod 1999; 5:581-586.
11. Vogiagis D, Marsh MM, Fry RC, Salamonsen LA. Leukemia inhibitory factor in human endometrium throughout the menstrual cycle. J Endocrinol 1996; 148:95-102.
12. Tremellen KP, Seamark RF, Robertson SA. Seminal transforming growth factor beta1 stimulates granulocyte-macrophage colony-stimulating factor production and inflammatory cell recruitment in the murine uterus. Biol Reprod 1998; 58:1217-1225.
13. Finn CA, Pope M. Control of leukocyte infiltration into the decidualized mouse uterus. J Endocrinol 1986; 110:93-96.
14. Beer AE, Billingham RE. Immunobiology of mammalian reproduction. Adv Immunol 1971; 14:1-84.
15. Hunt JS, Petroff MG, Burnett TG. Uterine leukocytes: key players in pregnancy. Semin Cell Dev Biol 2000; 11(2):127-137.
16. Pollard JW, Lin EY, Zhu L. Complexity in uterine macrophage responses to cytokines in mice. Biol Reprod 1998; 58:1469-1475.
17. Pollard JW, Hunt JS, Wiktor-Jedrzejczak W, Stanley ER. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev Biol 1991; 148:273-283.
18. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, Okamura H, Sudo T, Shultz LD. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 1990; 345:442-444.
19. Robertson SA, O'Connell AC, Hudson SN, Seamark RF. Granulocyte-macrophage colony-stimulating factor (GM-CSF) targets myeloid leukocytes in the uterus during the post-mating inflammatory response in mice. J Reprod Immunol 2000; 46:131-154.
20. Croy BA, Chantakru S, Esadeg S, Ashkar AA, Wei Q. Decidual natural killer cells: key regulators of placental development (a review). J Reprod Immunol 2002; 57:151-168.
21. Trundley A, Moffett A, Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, Masch R, Lockwood CJ, Schachter AD, Park PJ, Strominger JL, Michou VI, Kanavaros P, Athanassiou V, Chronis GB, Stabamas S, Tsilivakos V, White CA, Johansson M, Roberts CT, Ramsay AJ, Robertson SA, Ashkar AA, Black GP, Wei Q, He H, Liang L, Head JR, Croy BA, Miyazaki S, Tsuda H, Sakai M, Hori S, Sasaki Y, Futatani T, Miyawaki T, Saito S. Human uterine leukocytes and pregnancy. Tissue Antigens 2004; 63:1-12.
22. King A. Uterine leukocytes and decidualization. Hum Reprod Update 2000; 6:28-36.
23. 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.
24. 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.
25. Kruse A, Martens N, Fernekorn U, Hallmann R, Butcher EC. Alterations in the expression of homing-associated molecules at the maternal/fetal interface during the course of pregnancy. Biol Reprod 2002; 66:333-345.
26. Paffaro VA, Bizinotto MC, Joazeiro PP, Yamada AT. Subset classification of mouse uterine natural killer cells by DBA lectin reactivity. Placenta 2003; 24:479-488.
27. Stewart I, Peel S. Granulated metrial gland cells in the virgin and early pregnant mouse uterus. J Anat 1981; 133:535-541.
28. 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.
29. 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.
30. Ashkar AA, Croy BA. Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod 1999; 61:493-502.
31. Choudhury SR, Knapp LA. Human reproductive failure. I: immunological factors. Hum Reprod Update 2001; 7:113-134.
32. Quack KC, Vassiliadou N, Pudney J, Anderson DJ, Hill JA. Leukocyte activation in the decidua of chromosomally normal and abnormal fetuses from women with recurrent abortion. Hum Reprod 2001; 16: 949-955.
33. Jeziorska M, Salamonsen LA, Woolley DE. Mast cell and eosinophil distribution and activation in human endometrium throughout the menstrual cycle. Biol Reprod 1995; 53:312-320.
34. Salamonsen LA, Lathbury LJ. Endometrial leukocytes and menstruation. Hum Reprod Update 2000; 6:16-27.
35. Robertson SA, Mau VJ, Young IG, Matthaei KI. Uterine eosinophils and reproductive performance in interleukin 5-deficient mice. J Reprod Fertil 2000; 120:423-432.
36. Sferruzzi-Perri AN, Robertson SA, Dent LA. Interleukin-5 transgene expression and eosinophilia are associated with retarded mammary gland development in mice. Biol Reprod 2003; 69:224-233.
37. Sharkey AM, King A, Clark DE, Burrows TD, Jokhi PP, Charnock-Jones DS, Loke YW, Smith SK. Localization of leukemia inhibitory factor and its receptor in human placenta throughout pregnancy. Biol Reprod 1999; 60:355-364.
38. Dani C, Chambers I, Johnstone S, Robertson M, Ebrahimi B, Saito M, Taga T, Li M, Burdon T, Nichols J, Smith A. Paracrine induction of stem cell renewal by LIF-deficient cells: a new ES cell regulatory pathway. Dev Biol 1998; 203:149-162.
39. Tofaris GK, Patterson PH, Jessen KR, Mirsky R. Denervated Schwann cells attract macrophages by secretion of leukemia inhibitory factor (LIF) and monocyte chemoattractant protein-1 in a process regulated by interleukin-6 and LIF. J Neurosci 2002; 22:6696-6703.
40. Robertson SA, Roberts CT, Farr KL, Dunn AR, Seamark RF. Fertility impairment in granulocyte-macrophage colony-stimulating factor-deficient mice. Biol Reprod 1999; 60:251-261.
41. Chantakru S, Kuziel WA, Maeda N, Croy BA. A study on the density and distribution of uterine Natural Killer cells at mid pregnancy in mice genetically-ablated for CCR2, CCR 5 and the CCR5 receptor ligand, MIP-1α. J Reprod Immunol 2001; 49:33-47.
42. Wang D, Ishimura R, Walia DS, Muller H, Dai G, Hunt JS, Lee NA, Lee JJ, Soares MJ. Eosinophils are cellular targets of the novel uteroplacental heparin-binding cytokine decidual/trophoblast prolactin-related protein. J Endocrinol 2000; 167:15-28.
43. Kritikou EA, Sharkey A, Abell K, Came PJ, Anderson E, Clarkson RW, Watson CJ. A dual, non-redundant, role for LIF as a regulator of development and STAT3-mediated cell death in mammary gland. Development 2003; 130:3459-3468.
44. Lala PK, Scodras JM, Graham CH, Lysiak JJ, Parhar RS. Activation of maternal killer cells in the pregnant uterus with chronic indomethacin therapy, IL-2 therapy, or a combination therapy is associated with embryonic demise. Cell Immunol 1990; 127:368-381.