The chemokine receptor CXCR4 and its ligand CXCL12 are activated during implantation and placentation in sheep

Reproductive Biology and Endocrinology

Volumn 9, Issue , 2011, Pages

  Ashley, Ryan L ^a   Antoniazzi, Alfredo Q ^b   Anthony, Russell V ^b   Hansen, Thomas R ^b  

^a NEW MEXICO STATE UNIVERSITY   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Cxcl12; Cxcr4; Implantation; Placenta; Sheep; Trophoblast

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MESSENGER RNA; LIGAND; PLACENTA PROTEIN; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD SAMPLING; ENDOMETRIUM; ESTRUS CYCLE; FEMALE; GESTATIONAL AGE; JUGULAR VEIN; NIDATION; NONHUMAN; PREGNANCY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; SHEEP; UPREGULATION; UTERINE BLOOD VESSEL; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; BLOOD; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; LEUKOCYTE; METABOLISM; PLACENTA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; VASCULARIZATION;

OVIS ARIES;

ANIMALS; CHEMOKINE CXCL12; EMBRYO IMPLANTATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; ENDOMETRIUM; ESTROUS CYCLE; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LEUKOCYTES; LIGANDS; PLACENTA; PLACENTATION; PREGNANCY; PREGNANCY PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CXCR4; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SHEEP, DOMESTIC;

EID: 80155165247     PISSN: None     EISSN: 14777827     Source Type: Journal    
DOI: 10.1186/1477-7827-9-148     Document Type: Article

References (54)

1. Dimitriadis E, White CA, Jones RL, Salamonsen LA. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005, 11:613-630. 10.1093/humupd/dmi023, 16006437.
2. Herrler A, von Rango U, Beier HM. Embryo-maternal signalling: how the embryo starts talking to its mother to accomplish implantation. Reprod Biomed Online 2003, 6:244-256. 10.1016/S1472-6483(10)61717-8, 12676010.
3. Higuma-Myojo S, Sasaki Y, Miyazaki S, Sakai M, Siozaki A, Miwa N, Saito S. Cytokine profile of natural killer cells in early human pregnancy. Am J Reprod Immunol 2005, 54:21-29. 10.1111/j.1600-0897.2005.00279.x, 15948769.
4. Staun-Ram E, Shalev E. Human trophoblast function during the implantation process. Reprod Biol Endocrinol 2005, 3:56. 10.1186/1477-7827-3-56, 1289292, 16236179.
5. Veenstra van Nieuwenhoven AL, Heineman MJ, Faas MM. The immunology of successful pregnancy. Hum Reprod Update 2003, 9:347-357. 10.1093/humupd/dmg026, 12926528.
6. Arici A, Seli E, Senturk LM, Gutierrez LS, Oral E, Taylor HS. Interleukin-8 in the human endometrium. J Clin Endocrinol Metab 1998, 83:1783-1787. 10.1210/jc.83.5.1783, 9589693.
7. Caballero-Campo P, Dominguez F, Coloma J, Meseguer M, Remohi J, Pellicer A, Simon C. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod 2002, 8:375-384. 10.1093/molehr/8.4.375, 11912286.
8. Robertson SA, Mayrhofer G, Seamark RF. Ovarian steroid hormones regulate granulocyte-macrophage colony-stimulating factor synthesis by uterine epithelial cells in the mouse. Biol Reprod 1996, 54:183-196. 10.1095/biolreprod54.1.183, 8838016.
9. Wood GW, Hausmann E, Choudhuri R. Relative role of CSF-1, MCP-1/JE, and RANTES in macrophage recruitment during successful pregnancy. Mol Reprod Dev 1997, 46:62-69. discussion 69-70, 10.1002/(SICI)1098-2795(199701)46:1<62::AID-MRD10>3.0.CO;2-5, 8981365.
10. Dominguez F, Galan A, Martin JJ, Remohi J, Pellicer A, Simon C. Hormonal and embryonic regulation of chemokine receptors CXCR1, CXCR4, CCR5 and CCR2B in the human endometrium and the human blastocyst. Mol Hum Reprod 2003, 9:189-198. 10.1093/molehr/gag024, 12651900.
11. Valles CS, Dominguez F. Embryo-endometrial interaction. Chang Gung Med J 2006, 29:9-14.
12. Kumar A, Kumar S, Dinda AK, Luthra K. Differential expression of CXCR4 receptor in early and term human placenta. Placenta 2004, 25:347-351. 10.1016/j.placenta.2003.10.003, 15028427.
13. Murdoch C. CXCR4: chemokine receptor extraordinaire. Immunol Rev 2000, 177:175-184. 10.1034/j.1600-065X.2000.17715.x, 11138774.
14. Huang Y, Zhu XY, Du MR, Wu X, Wang MY, Li DJ. Chemokine CXCL16, a scavenger receptor, induces proliferation and invasion of first-trimester human trophoblast cells in an autocrine manner. Hum Reprod 2006, 21:1083-1091.
15. Wu X, Jin LP, Yuan MM, Zhu Y, Wang MY, Li DJ. Human first-trimester trophoblast cells recruit CD56brightCD16- NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell-derived factor 1. J Immunol 2005, 175:61-68.
16. Wu X, Li DJ, Yuan MM, Zhu Y, Wang MY. The expression of CXCR4/CXCL12 in first-trimester human trophoblast cells. Biol Reprod 2004, 70:1877-1885. 10.1095/biolreprod.103.024729, 14973260.
17. Rosenkilde MM, Schwartz TW. The chemokine system -- a major regulator of angiogenesis in health and disease. Apmis 2004, 112:481-495. 10.1111/j.1600-0463.2004.apm11207-0808.x, 15563311.
18. Purcell SH, Cantlon JD, Wright CD, Henkes LE, Seidel GE, Anthony RV. The involvement of proline-rich 15 in early conceptus development in sheep. Biology of reproduction 2009, 81:1112-1121. 10.1095/biolreprod.109.076190, 2802235, 19605793.
19. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008, 3:1101-1108. 10.1038/nprot.2008.73, 18546601.
20. Balkwill F. Cancer and the chemokine network. Nat Rev Cancer 2004, 4:540-550. 10.1038/nrc1388, 15229479.
21. Boshier DP. A histological and histochemical examination of implantation and early placentome formation in sheep. Journal of reproduction and fertility 1969, 19:51-61. 10.1530/jrf.0.0190051, 5793914.
22. Kucia M, Jankowski K, Reca R, Wysoczynski M, Bandura L, Allendorf DJ, Zhang J, Ratajczak J, Ratajczak MZ. CXCR4-SDF-1 signalling, locomotion, chemotaxis and adhesion. Journal of molecular histology 2004, 35:233-245.
23. Grazul-Bilska AT, Borowicz PP, Johnson ML, Minten MA, Bilski JJ, Wroblewski R, Redmer DA, Reynolds LP. Placental development during early pregnancy in sheep: vascular growth and expression of angiogenic factors in maternal placenta. Reproduction 2010, 140:165-174. 10.1530/REP-09-0548, 20400519.
24. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, Fahrig M, Vandenhoeck A, Harpal K, Eberhardt C, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996, 380:435-439. 10.1038/380435a0, 8602241.
25. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996, 380:439-442. 10.1038/380439a0, 8602242.
26. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 1995, 376:66-70. 10.1038/376066a0, 7596436.
27. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995, 376:62-66. 10.1038/376062a0, 7596435.
28. Cale JM, Millican DS, Itoh H, Magness RR, Bird IM. Pregnancy induces an increase in the expression of glyceraldehyde-3-phosphate dehydrogenase in uterine artery endothelial cells. J Soc Gynecol Investig 1997, 4:284-292. 10.1016/S1071-5576(97)00067-1, 9408883.
29. Folkman J, Klagsbrun M. Angiogenic factors. Science 1987, 235:442-447. 10.1126/science.2432664, 2432664.
30. Klagsbrun M, D'Amore PA. Regulators of angiogenesis. Annu Rev Physiol 1991, 53:217-239. 10.1146/annurev.ph.53.030191.001245, 1710435.
31. Zheng J, Bird IM, Melsaether AN, Magness RR. Activation of the mitogen-activated protein kinase cascade is necessary but not sufficient for basic fibroblast growth factor- and epidermal growth factor-stimulated expression of endothelial nitric oxide synthase in ovine fetoplacental artery endothelial cells. Endocrinology 1999, 140:1399-1407. 10.1210/en.140.3.1399, 10067868.
32. Reynolds LP, Redmer DA. Angiogenesis in the placenta. Biol Reprod 2001, 64:1033-1040. 10.1095/biolreprod64.4.1033, 11259247.
33. Rider V, Piva M. Role of growth factors of uterine and fetal-placental origin during pregnancy 1998, Totowa, NJ: Humana Press.
34. Zheng J, Magness RR, Redmer DA, Reynolds LP. Angiogenic activity of ovine placental tissues: immunoneutralization with FGF-2 and VEGF antisera. J Soc Gynecol Investig 1995, 2:289.
35. Zheng J, Redmer DA, Killilea SD, Reynolds LP. Characterization of heparin-binding endothelial mitogen(s) produced by the ovine endometrium during early pregnancy. Biochem Cell Biol 1998, 76:89-96. 10.1139/o98-011, 9666310.
36. Salcedo R, Oppenheim JJ. Role of chemokines in angiogenesis: CXCL12/SDF-1 and CXCR4 interaction, a key regulator of endothelial cell responses. Microcirculation 2003, 10:359-370. 10.1080/mic.10.3-4.359.370, 12851652.
37. Salcedo R, Wasserman K, Young HA, Grimm MC, Howard OM, Anver MR, Kleinman HK, Murphy WJ, Oppenheim JJ. Vascular endothelial growth factor and basic fibroblast growth factor induce expression of CXCR4 on human endothelial cells: In vivo neovascularization induced by stromal-derived factor-1alpha. Am J Pathol 1999, 154:1125-1135. 10.1016/S0002-9440(10)65365-5, 1866563, 10233851.
38. Mirshahi F, Pourtau J, Li H, Muraine M, Trochon V, Legrand E, Vannier J, Soria J, Vasse M, Soria C. SDF-1 activity on microvascular endothelial cells: consequences on angiogenesis in in vitro and in vivo models. Thromb Res 2000, 99:587-594. 10.1016/S0049-3848(00)00292-9, 10974345.
39. Salvucci O, Yao L, Villalba S, Sajewicz A, Pittaluga S, Tosato G. Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1. Blood 2002, 99:2703-2711. 10.1182/blood.V99.8.2703, 11929756.
40. Molino M, Woolkalis MJ, Prevost N, Pratico D, Barnathan ES, Taraboletti G, Haggarty BS, Hesselgesser J, Horuk R, Hoxie JA, Brass LF. CXCR4 on human endothelial cells can serve as both a mediator of biological responses and as a receptor for HIV-2. Biochim Biophys Acta 2000, 1500:227-240.
41. Tachibana K, Hirota S, Iizasa H, Yoshida H, Kawabata K, Kataoka Y, Kitamura Y, Matsushima K, Yoshida N, Nishikawa S, et al. The chemokine receptor CXCR4 is essential for vascularization of the gastrointestinal tract. Nature 1998, 393:591-594. 10.1038/31261, 9634237.
42. Grazul-Bilska AT, Johnson ML, Borowicz PP, Minten M, Bilski JJ, Wroblewski R, Velimirovich M, Coupe L, Redmer DA, Reynolds LP. Placental development during early pregnancy in sheep: Cell proliferation, global methylation and angiogenesis in the fetal placenta. Reproduction 2011,
43. Guillomot M. Cellular interactions during implantation in domestic ruminants. J Reprod Fertil Suppl 1995, 49:39-51.
44. Wimsatt WA. New histological observations on the placenta of the sheep. The American journal of anatomy 1950, 87:391-457. 10.1002/aja.1000870304, 14789741.
45. Guillomot M, Flechon JE, Wintenberger-Torres S. Conceptus attachment in the ewe: an ultrastructural study. Placenta 1981, 2:169-182. 10.1016/S0143-4004(81)80021-5, 7232339.
46. Zhou WH, Du MR, Dong L, Yu J, Li DJ. Chemokine CXCL12 promotes the cross-talk between trophoblasts and decidual stromal cells in human first-trimester pregnancy. Hum Reprod 2008, 23:2669-2679. 10.1093/humrep/den308, 18687671.
47. Shimonovitz S, Hurwitz A, Dushnik M, Anteby E, Geva-Eldar T, Yagel S. Developmental regulation of the expression of 72 and 92 kd type IV collagenases in human trophoblasts: a possible mechanism for control of trophoblast invasion. Am J Obstet Gynecol 1994, 171:832-838.
48. Staun-Ram E, Goldman S, Gabarin D, Shalev E. Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol 2004, 2:59. 10.1186/1477-7827-2-59, 516041, 15294019.
49. Jaleel MA, Tsai AC, Sarkar S, Freedman PV, Rubin LP. Stromal cell-derived factor-1 (SDF-1) signalling regulates human placental trophoblast cell survival. Mol Hum Reprod 2004, 10:901-909. 10.1093/molehr/gah118, 15475370.
50. Suzuki Y, Rahman M, Mitsuya H. Diverse transcriptional response of CD4(+) T cells to stromal cell-derived factor (SDF)-1: cell survival promotion and priming effects of SDF-1 on CD4(+) T cells. J Immunol 2001, 167:3064-3073.
51. Lin Y, Xu L, Jin H, Zhong Y, Di J, Lin QD. CXCL12 enhances exogenous CD4(+)CD25(+) T cell migration and prevents embryo loss in non-obese diabetic mice. Fertil Steril 2008,
52. Alders RG, Shelton JN. Lymphocyte subpopulations in lymph and blood draining from the uterus and ovary in sheep. Journal of reproductive immunology 1990, 17:27-40. 10.1016/0165-0378(90)90037-7, 2329547.
53. Segerson EC, Matterson PM, Gunsett FC. Endometrial T-lymphocyte subset infiltration during the ovine estrous cycle and early pregnancy. Journal of reproductive immunology 1991, 20:221-236. 10.1016/0165-0378(91)90048-U, 1720461.
54. Mansouri-Attia N, Aubert J, Reinaud P, Giraud-Delville C, Taghouti G, Galio L, Everts RE, Degrelle S, Richard C, Hue I, et al. Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation. Physiological genomics 2009, 39:14-27. 10.1152/physiolgenomics.90404.2008, 19622795.