Advertisement

Angiogenesis in implantation

  • Donald S. TorryEmail author
  • Jonathan Leavenworth
  • Miao Chang
  • Vatsala Maheshwari
  • Kathleen Groesch
  • Evan R. Ball
  • Ronald J. Torry
Article

Abstract

Problem

Implantation failure and early pregnancy loss are common following natural conceptions and they are particularly important clinical hurdles to overcome following assisted reproduction attempts. The importance of adequate vascular development and maintenance during implantation has recently become a major focus of investigation.

Materials and methods

Review of current published literature was undertaken to summerize the cells and cell products that regulate tissue vascularity during implantation.

Results

Vascular development at the maternal fetal interface can be regulated by a number of different cell types; two principal candidates are trophoblast and natural killer cells. A wide range of soluble factors, some with well established angiogenic functions as well as other more novel factors, can contribute to vascular development and maintenance at the maternal–fetal interface.

Conclusions

Robust vascular development occurs during implantation and early placentation of normal pregnancies. Studies to define the extent and mechanisms by which defects in vascularity contribute to human implantation failure and early miscarriage need to be undertaken.

Keywords

Angiogenesis Growth factors Implantation Miscarriage Pregnancy Trophoblast Vasculogenesis 

Notes

Acknowledgments

Supported in part by the National Institute of Child Health and Human Development (2RO1 HD36830) (DST), the National Heart, Lung and Blood Institute (R15 HL072802) (RJT), and March of Dimes Birth Defects Foundation (DST).

References

  1. 1.
    Torry RJ, Rongish BJ. Angiogenesis in the uterus: potential regulation and relation to tumor angiogenesis. Am J Reprod Immunol 1992;27:171–9.PubMedGoogle Scholar
  2. 2.
    Klauber N, Rohan RM, Flynn E, D’Amato RJ. Critical components of the female reproductive pathway are suppressed by the angiogenesis inhibitor AGM-1470. Nat Med 1997;3:443–6.PubMedGoogle Scholar
  3. 3.
    Reynolds LP, Caton JS, Redmer DA, Grazul-Bilska AT, Vonnahme KA, Borowicz PP, et al. Evidence for altered placental blood flow and vascularity in compromised pregnancies. J Physiol 2006;572:51–8.PubMedGoogle Scholar
  4. 4.
    Meegdes BH, Ingenhoes R, Peeters LL, Exalto N. Early pregnancy wastage: relationship between chorionic vascularization and embryonic development. Fertil Steril 1988;49:216–20.PubMedGoogle Scholar
  5. 5.
    Vuorela P, Carpen O, Tulppala M, Halmesmaki E. VEGF, its receptors and the tie receptors in recurrent miscarriage. Mol Hum Reprod 2000;6:276–82.PubMedGoogle Scholar
  6. 6.
    Jauniaux E, Johns J, Burton GJ. The role of ultrasound imaging in diagnosing and investigating early pregnancy failure. Ultrasound Obstet Gynecol 2005;25:613–24.PubMedGoogle Scholar
  7. 7.
    Reynolds LP, Redmer DA. Growth and microvascular development of the uterus during early pregnancy in ewes. Biol Reprod 1992;47:698–708.PubMedGoogle Scholar
  8. 8.
    Plaks V, Kalchenko V, Dekel N, Neeman M. MRI analysis of angiogenesis during mouse embryo implantation. Magn Reson Med 2006;55:1013–22.PubMedGoogle Scholar
  9. 9.
    Pringle KG, Roberts CT. New Light on Early Post-Implantation Pregnancy in the Mouse: Roles for Insulin-Like Growth Factor-II (IGF-II)? Placenta 2007;28:286–97.Google Scholar
  10. 10.
    Bany BM, Cross JC. Post-implantation mouse conceptuses produce paracrine signals that regulate the uterine endometrium undergoing decidualization. Dev Biol 2006;294:445–56.PubMedGoogle Scholar
  11. 11.
    Girling JE, Rogers PA. Recent advances in endometrial angiogenesis research. Angiogenesis 2005;8:89–99.PubMedGoogle Scholar
  12. 12.
    Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 2006;27:939–58.PubMedGoogle Scholar
  13. 13.
    Cross JC, Hemberger M, Lu Y, Nozaki T, Whiteley K, Masutani M, et al. Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol Cell Endocrinol 2002;187:207–12.PubMedGoogle Scholar
  14. 14.
    Huppertz B, Peeters LL. Vascular biology in implantation and placentation. Angiogenesis 2005;8:157–67.PubMedGoogle Scholar
  15. 15.
    Geva E, Ginzinger DG, Zaloudek CJ, Moore DH, Byrne A, Jaffe RB. Human placental vascular development: vasculogenic and angiogenic (branching and nonbranching) transformation is regulated by vascular endothelial growth factor-A, angiopoietin-1, and angiopoietin-2. J Clin Endocrinol Metab 2002;87:4213–24.PubMedGoogle Scholar
  16. 16.
    Cervar M, Blaschitz A, Dohr G, Desoye G. Paracrine regulation of distinct trophoblast functions in vitro by placental macrophages. Cell Tissue Res 1999;295:297–305.PubMedGoogle Scholar
  17. 17.
    Demir R, Kayisli UA, Seval Y, Celik-Ozenci C, Korgun ET, mir-Weusten AY, et al. Sequential expression of VEGF and its receptors in human placental villi during very early pregnancy: differences between placental vasculogenesis and angiogenesis. Placenta 2004;25:560–72.PubMedGoogle Scholar
  18. 18.
    Wulff C, Weigand M, Kreienberg R, Fraser HM. Angiogenesis during primate placentation in health and disease. Reproduction 2003;126:569–77.PubMedGoogle Scholar
  19. 19.
    Cross JC, Simmons DG, Watson ED. Chorioallantoic morphogenesis and formation of the placental villous tree. Ann N Y Acad Sci 2003;995:84–93.PubMedCrossRefGoogle Scholar
  20. 20.
    Cross JC, Nakano H, Natale DR, Simmons DG, Watson ED. Branching morphogenesis during development of placental villi. Differentiation 2006;74:393–401.PubMedGoogle Scholar
  21. 21.
    Cross JC. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin Cell Dev Biol 2000;11:105–13.PubMedGoogle Scholar
  22. 22.
    Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C, et al. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol 2002;250:358–73.PubMedGoogle Scholar
  23. 23.
    Hemberger M, Nozaki T, Masutani M, Cross JC. Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion. Dev Dyn 2003;227:185–91.PubMedGoogle Scholar
  24. 24.
    Georgiades P, Watkins M, Burton GJ, Ferguson-Smith AC. Roles for genomic imprinting and the zygotic genome in placental development. Proc Natl Acad Sci U S A 2001;98:4522–7.PubMedGoogle Scholar
  25. 25.
    Constancia M, Hemberger M, Hughes J, Dean W, Ferguson-Smith A, Fundele R, et al. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 2002;417:945–8.PubMedGoogle Scholar
  26. 26.
    Watson ED, Cross JC. Development of structures and transport functions in the mouse placenta. Physiology (Bethesda) 2005;20:180–93.Google Scholar
  27. 27.
    van den Heuvel MJ, Xie XM, Tayade C, Peralta C, Fang Y, Leonard S, et al. A review of trafficking and activation of uterine natural killer cells. Am J Reprod Immunol 2005;54:322–31.PubMedGoogle Scholar
  28. 28.
    Leonard S, Murrant C, Tayade C, van den Heuvel M, Watering R, Croy BA. Mechanisms regulating immune cell contributions to spiral artery modification—Facts and hypotheses—a review. Placenta 2006;27:S40–6.PubMedGoogle Scholar
  29. 29.
    Dosiou C, Giudice LC. Natural killer cells in pregnancy and recurrent pregnancy loss: endocrine and immunologic perspectives. Endocr Rev 2005;26:44–62.PubMedGoogle Scholar
  30. 30.
    Ledee-Bataille N, Bonnet-Chea K, Hosny G, Dubanchet S, Frydman R, Chaouat G. Role of the endometrial tripod interleukin-18, -15, and -12 in inadequate uterine receptivity in patients with a history of repeated in vitro fertilization-embryo transfer failure. Fertil Steril 2005;83:598–605.PubMedGoogle Scholar
  31. 31.
    Croy BA, van den Heuvel MJ, Borzychowski AM, Tayade C. Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 2006;214:161–85.PubMedGoogle Scholar
  32. 32.
    Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006;12:1065–74.PubMedGoogle Scholar
  33. 33.
    agaard-Tillery KM, Silver R, Dalton J. Immunology of normal pregnancy. Seminars Fetal Neonatal Med 2006;11:279–95.Google Scholar
  34. 34.
    Ruddell A, Mezquita P, Brandvold KA, Farr A, Iritani BM. B lymphocyte-specific c-Myc expression stimulates early and functional expansion of the vasculature and lymphatics during lymphomagenesis. Am J Pathol 2003;163:2233–45.PubMedGoogle Scholar
  35. 35.
    Quenby S, Bates M, Doig T, Brewster J, Lewis-Jones DI, Johnson PM, et al. Pre-implantation endometrial leukocytes in women with recurrent miscarriage. Hum Reprod 1999;14:2386–91.PubMedGoogle Scholar
  36. 36.
    Thum MY, Bhaskaran S, Bansal AS, Shehata H, Ford B, Sumar N, et al. Simple enumerations of peripheral blood natural killer (CD56+ NK) cells, B cells and T cells have no predictive value in IVF treatment outcome. Hum Reprod 2005;20:1272–6.PubMedGoogle Scholar
  37. 37.
    Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy 2005;4:3–8.PubMedGoogle Scholar
  38. 38.
    Hayashi T, Matsuoka K, Saitoh M, Takeda S, Kimura M. Influence of alpha-tumor necrosis factor and beta-interleukin-1 on production of angiogenetic factors and thymidine phosphorylase activity in immortalized human decidual fibroblasts in vitro. J Obstet Gynaecol Res 2006;32:15–22.PubMedGoogle Scholar
  39. 39.
    van Nieuwenhoven ALV, Heineman MJ, Faas MM. The immunology of successful pregnancy. Hum Reprod Updat 2003;9:347–57.Google Scholar
  40. 40.
    Chung IB, Yelian FD, Zaher FM, Gonik B, Evans MI, Diamond MP, et al. Expression and regulation of vascular endothelial growth factor in a first trimester trophoblast cell line. Placenta 2000;21:320–4.PubMedGoogle Scholar
  41. 41.
    Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy 2005;4:3–8.PubMedGoogle Scholar
  42. 42.
    Szukiewicz D, Szewczyk G, Watroba M, Kurowska E, Maslinski S. Isolated placental vessel response to vascular endothelial growth factor and placenta growth factor in normal and growth-restricted pregnancy. Gynecol Obstet Investig 2005;59:102–7.Google Scholar
  43. 43.
    Croy BA, Esadeg S, Chantakru S, van den HM, Paffaro VA, He H, et al. 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;59:175–91.PubMedGoogle Scholar
  44. 44.
    Druckmann R, Druckmann MA. Progesterone and the immunology of pregnancy. J Steroid Biochem Mol Biol 2005;97:389–96.PubMedGoogle Scholar
  45. 45.
    Naldini A, Pucci A, Bernini C, Carraro F. Regulation of angiogenesis by Th1- and Th2-type cytokines. Curr Pharm Des 2003;9:511–9.PubMedGoogle Scholar
  46. 46.
    Laird SM, Tuckerman EM, Li TC. Cytokine expression in the endometrium of women with implantation failure and recurrent miscarriage. Reprod Biomed Online 2006; 13:13-23.PubMedCrossRefGoogle Scholar
  47. 47.
    Robertson SA. Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 2005;322:43–52.PubMedGoogle Scholar
  48. 48.
    Kabawat SE, Mostoufizadeh M, Driscoll SG, Bhan AK. Implantation site in normal-pregnancy—a study with monoclonal-antibodies. Am J Pathol 1985;118:76–84.PubMedGoogle Scholar
  49. 49.
    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;148:273–83.PubMedGoogle Scholar
  50. 50.
    Cooper JC, Sharkey AM, McLaren J, Charnock-Jones DS, Smith SK. Localization of vascular endothelial growth factor and its receptor, flt, in human placenta and decidua by immunohistochemistry. J Reprod Fertil 1995;105:205–13.PubMedCrossRefGoogle Scholar
  51. 51.
    Pongcharoen S, Somran J, Sritippayawan S, Niumsup P, Chanchan P, Butkhamchot P, et al. Interleukin-17 expression in the human placenta. Placenta 2007;28:59–63.PubMedGoogle Scholar
  52. 52.
    Guilbert L, Robertson SA, Wegmann TG. The trophoblast as an integral component of a macrophage cytokine network. Immunol Cell Biol 1993;71:49–57.PubMedGoogle Scholar
  53. 53.
    Girardi G, Yarilin D, Thurman JM, Holers VM, Salmon JE. Complement activation induces dysregulation of angiogenic factors and causes fetal rejection and growth restriction. J Exp Med 2006;203:2165–75.PubMedGoogle Scholar
  54. 54.
    Vessella RL, Corey E. Targeting factors involved in bone remodeling as treatment strategies in prostate cancer bone metastasis. Clin Cancer Res 2006;12:6285s–90s.PubMedGoogle Scholar
  55. 55.
    Lipinski MJ, Frias JC, Fayad ZA. Advances in detection and characterization of atherosclerosis using contrast agents targeting the macrophage. J Nucl Cardiol 2006;13:699–709.PubMedGoogle Scholar
  56. 56.
    Siristatidis C, Nissotakis C, Chrelias C, Iacovidou H, Salamalekis E. Immunological factors and their role in the genesis and development of endometriosis. J Obstet Gynaecol Res 2006;32:162–70.PubMedGoogle Scholar
  57. 57.
    Lewis CE, Pollard JW. Distinct role of macrophages in different tumor microenvironments. Cancer Res 2006;66:605–12.PubMedGoogle Scholar
  58. 58.
    Takahashi H, Shibuya M. The vascular endothelial growth factor (VEGF)/VEGF receptor system and its role under physiological and pathological conditions. Clin Sci (Lond) 2005;109:227–41.CrossRefGoogle Scholar
  59. 59.
    Tammela T, Enholm B, Alitalo K, Paavonen K. The biology of vascular endothelial growth factors. Cardiovasc Res 2005;65:550–63.PubMedGoogle Scholar
  60. 60.
    Halder JB, Zhao X, Soker S, Paria BC, Klagsbrun M, Das SK, et al. Differential expression of VEGF isoforms and VEGF(164)-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF(164) in vascular permeability and angiogenesis during implantation. Genesis 2000;26:213–24.PubMedGoogle Scholar
  61. 61.
    Gluzman-Poltorak Z, Cohen T, Herzog Y, Neufeld G. Neuropilin-2 and neuropilin-1 are receptors for the 165-amino acid form of vascular endothelial growth factor (VEGF) and of placenta growth factor-2, but only neuropilin-2 functions as a receptor for the 145- amino acid form of VEGF. J Biol Chem 2000;275:18040–5.PubMedGoogle Scholar
  62. 62.
    Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Gertsenstein M, et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996;380:435–9.PubMedGoogle Scholar
  63. 63.
    Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996;380:439–42.PubMedGoogle Scholar
  64. 64.
    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.PubMedGoogle Scholar
  65. 65.
    Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 1995;376:62–6.PubMedGoogle Scholar
  66. 66.
    Takashima S, Kitakaze M, Asakura M, Asanuma H, Sanada S, Tashiro F, et al. Targeting of both mouse neuropilin-1 and neuropilin-2 genes severely impairs developmental yolk sac and embryonic angiogenesis. Proc Natl Acad Sci U S A 2002;99:3657–62.PubMedGoogle Scholar
  67. 67.
    Chakraborty I, Das SK, Dey SK. Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 1995;147:339–52.PubMedCrossRefGoogle Scholar
  68. 68.
    Das SK, Chakraborty I, Wang J, Dey SK, Hoffman LH. Expression of vascular endothelial growth factor (VEGF) and VEGF-receptor messenger ribonucleic acids in the peri-implantation rabbit uterus. Biol Reprod 1997;56:1390–9.PubMedGoogle Scholar
  69. 69.
    Kapiteijn K, Koolwijk P, van der Weiden RM, van Nieuw AG, Plaisier M, van HV, et al. Human embryo-conditioned medium stimulates in vitro endometrial angiogenesis. Fertil Steril 2006;85(Suppl 1):1232–9.PubMedGoogle Scholar
  70. 70.
    Kingdom JC, Kaufmann P. Oxygen and placental vascular development. Adv Exp Med Biol 1999;474:259–75.PubMedGoogle Scholar
  71. 71.
    Shore VH, Wang TH, Wang CL, Torry RJ, Caudle MR, Torry DS. Vascular endothelial growth factor, placenta growth factor and their receptors in isolated human trophoblast. Placenta 1997;18:657–65.PubMedGoogle Scholar
  72. 72.
    Ahmed A, Dunk C, Ahmad S, Khaliq A. Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen—a review. Placenta 2000;21(Suppl A):S16–24.PubMedGoogle Scholar
  73. 73.
    Nagamatsu T, Fujii T, Kusumi M, Zou L, Yamashita T, Osuga Y, et al. Cytotrophoblasts up-regulate soluble fms-like tyrosine kinase-1 expression under reduced oxygen: an implication for the placental vascular development and the pathophysiology of preeclampsia. Endocrinology 2004;145:4838–45.PubMedGoogle Scholar
  74. 74.
    Kendall RL, Wang G, Thomas KA. Identification of a natural soluble form of the vascular endothelial growth factor receptor, FLT-1, and its heterodimerization with KDR. Biochem Biophys Res Commun 1996;226:324–8.PubMedGoogle Scholar
  75. 75.
    Evans PW, Wheeler T, Anthony FW, Osmond C. A longitudinal study of maternal serum vascular endothelial growth factor in early pregnancy. Hum Reprod 1998;13:1057–62.PubMedGoogle Scholar
  76. 76.
    Licht P, Russu V, Wildt L. On the role of human chorionic gonadotropin (hCG) in the embryo-endometrial microenvironment: implications for differentiation and implantation. Semin Reprod Med 2001;19:37–47.PubMedGoogle Scholar
  77. 77.
    Papazoglou D, Galazios G, Papatheodorou K, Liberis V, Papanas N, Maltezos E, et al. Vascular endothelial growth factor gene polymorphisms and idiopathic recurrent pregnancy loss. Fertil Steril 2005;83:959–63.PubMedGoogle Scholar
  78. 78.
    Yamazaki Y, Morita T. Molecular and functional diversity of vascular endothelial growth factors. Mol Divers 2006.Google Scholar
  79. 79.
    Torry DS, Mukherjea D, Arroyo J, Torry RJ. Expression and function of placenta growth factor: implications for abnormal placentation. J Soc Gynecol Investig 2003;10:178–88.PubMedGoogle Scholar
  80. 80.
    Torry DS, Hinrichs M, Torry RJ. Determinants of placental vascularity. Am J Reprod Immunol 2004;51:257–68.PubMedGoogle Scholar
  81. 81.
    Ikai T, Miwa H, Shikami M, Hiramatsu A, Tajima E, Yamamoto H, et al. Placenta growth factor stimulates the growth of Philadelphia chromosome positive acute lymphoblastic leukemia cells by both autocrine and paracrine pathways. Eur J Haematol 2005;75:273–9.PubMedGoogle Scholar
  82. 82.
    Autiero M, Luttun A, Tjwa M, Carmeliet P. Placental growth factor and its receptor, vascular endothelial growth factor receptor-1: novel targets for stimulation of ischemic tissue revascularization and inhibition of angiogenic and inflammatory disorders. J Thromb Haemost 2003;1:1356–70.PubMedGoogle Scholar
  83. 83.
    Carmeliet P, Moons L, Luttun A, Vincenti V, Compernolle V, De Mol M, et al. Synergism between vascular endothelial growth factor and placental growth factor contributes to angiogenesis and plasma extravasation in pathological conditions. Nat Med 2001;7:575–83.PubMedGoogle Scholar
  84. 84.
    Lijnen HR, Christiaens V, Scroyen I, Voros G, Tjwa M, Carmeliet P, et al. Impaired adipose tissue development in mice with inactivation of placental growth factor function. Diabetes 2006;55:2698–704.PubMedGoogle Scholar
  85. 85.
    Ziche M, Maglione D, Ribatti D, Morbidelli L, Lago CT, Battisti M, et al. Placenta growth factor-1 is chemotactic, mitogenic, and angiogenic. Lab Invest 1997;76:517–31.PubMedGoogle Scholar
  86. 86.
    Welch PC, Amankwah KS, Miller P, McAsey ME, Torry DS. Correlations of placental perfusion and PlGF protein expression in early human pregnancy. Am J Obstet Gynecol 2006;194:1625–9.PubMedGoogle Scholar
  87. 87.
    Demir R, Kayisli UA, Cayli S, Huppertz B. Sequential steps during vasculogenesis and angiogenesis in the very early human placenta. Placenta 2006;27:535–9.PubMedGoogle Scholar
  88. 88.
    Ghosh D, Sharkey AM, Charnock-Jones DS, Dhawan L, Dhara S, Smith SK, et al. Expression of vascular endothelial growth factor (VEGF) and placental growth factor (PlGF) in conceptus and endometrium during implantation in the rhesus monkey. Mol Hum Reprod 2000;6:935–41.PubMedGoogle Scholar
  89. 89.
    Levine RJ, Thadhani R, Qian C, Lam C, Lim KH, Yu KF, et al. Urinary placental growth factor and risk of preeclampsia. JAMA 2005;293:77–85.PubMedGoogle Scholar
  90. 90.
    Tidwell SC, Ho HN, Chiu WH, Torry RJ, Torry DS. Low maternal serum levels of placenta growth factor as an antecedent of clinical preeclampsia. Am J Obstet Gynecol 2001;184:1267–72.PubMedGoogle Scholar
  91. 91.
    Taylor RN, Grimwood J, Taylor RS, McMaster MT, Fisher SJ, North RA. Longitudinal serum concentrations of placental growth factor: evidence for abnormal placental angiogenesis in pathologic pregnancies. Am J Obstet Gynecol 2003;188:177–82.PubMedGoogle Scholar
  92. 92.
    Ornitz DM, Itoh N. Fibroblast growth factors. Genome Biol 2001;2.Google Scholar
  93. 93.
    Rossant J, Cross JC. Placental development: lessons from mouse mutants. Nat Rev Genet 2001;2:538–48.PubMedGoogle Scholar
  94. 94.
    Moscatelli D, Joseph-Silverstein J, Presta M, Rifkin DB. Multiple forms of an angiogenesis factor: basic fibroblast growth factor. Biochimie 1988;70.Google Scholar
  95. 95.
    Hamai Y, Fujii T, Yamashita T, Kozuma S, Okai T, Taketani Y. Evidence for basic fibroblast growth factor as a crucial angiogenic growth factor, released from human trophoblasts during early gestation. Placenta 1998;19.Google Scholar
  96. 96.
    Hyder SM, Stancel GM. Regulation of angiogenic growth factors in the female reproductive tract by estrogens and progestins. Mol Endocrinol 1999;13.Google Scholar
  97. 97.
    Wei P, Chen XL, Song XX, Han CS, Liu YX. VEGF, bFGF, and their receptors in the endometrium of rhesus monkey during menstrual cycle and early pregnancy. Mol Reprod Dev 2004;68.Google Scholar
  98. 98.
    Wei P, Yu FQ, Chen XL, Tao SX, Han CS, Liu YX. VEGF, bFGF and their receptors at the fetal-maternal interface of the rhesus monkey. Placenta 2004;25.Google Scholar
  99. 99.
    Srivastava RK, Gu Y, Ayloo S, Zilberstein M, Gibori G. Developmental expression and regulation of basic fibroblast growth factor and vascular endothelial growth factor in rat decidua and in a decidual cell line. J Mol Endocrinol 1998;21.Google Scholar
  100. 100.
    Wordinger RJ, Smith KJ, Bell C, Chang IF. The immunolocalization of basic fibroblast growth factor in the mouse uterus during the initial stages of embryo implantation. Growth Factors 1994;11.Google Scholar
  101. 101.
    Shams M, Ahmed A. Localization of mRNA for basic fibroblast growth factor in human placenta. Growth Factors 1994;11:105–11.PubMedGoogle Scholar
  102. 102.
    Wollenhaupt K, Welter H, Einspanier R, Manabe N, Brussow KP. Expression of epidermal growth factor receptor (EGF-R), vascular endothelial growth factor receptor (VEGF-R) and fibroblast growth factor receptor (FGF-R) systems in porcine oviduct and endometrium during the time of implantation. J Reprod Dev 2004;50.Google Scholar
  103. 103.
    Buscaglia ML, Ong M, Fuller J, Gonzalez AM, Baird A. Inhibition of pregnancy in the passively and actively immunized mammals rabbit, rat, and mouse. Ann N Y Acad Sci 1991;638.Google Scholar
  104. 104.
    Sangha RK, Li XF, Shams M, Ahmed A. Fibroblast growth factor receptor-1 is a critical component for endometrial remodeling: localization and expression of basic fibroblast growth factor and FGF-R1 in human endometrium during the menstrual cycle and decreased FGF-R1 expression in menorrhagia. Lab Invest 1997;77.Google Scholar
  105. 105.
    Anteby EY, Greenfield C, Natanson-Yaron S, Goldman-Wohl D, Hamani Y, Khudyak V, et al. Vascular endothelial growth factor, epidermal growth factor and fibroblast growth factor-4 and -10 stimulate trophoblast plasminogen activator system and metalloproteinase-9. Mol Hum Reprod 2004;10.Google Scholar
  106. 106.
    Wollenhaupt K, Welter H, Brussow KP, Einspanier R. Regulation of endometrial fibroblast growth factor 7 (FGF-7) and its receptor FGFR2IIIb in gilts after sex steroid replacements, and during the estrous cycle and early gestation. J Reprod Dev 2005;51.Google Scholar
  107. 107.
    Massabbal E, Parveen S, Weisoly DL, Nelson DM, Smith SD, Fant M. PLAC1 expression increases during trophoblast differentiation: evidence for regulatory interactions with the fibroblast growth factor-7 (FGF-7) axis. Mol Reprod Dev 2005;71.Google Scholar
  108. 108.
    Tsai SJ, Wu MH, Chen HM, Chuang PC, Wing LY. Fibroblast growth factor-9 is an endometrial stromal growth factor. Endocrinology 2002;143.Google Scholar
  109. 109.
    Wing LY, Chuang PC, Wu MH, Chen HM, Tsai SJ. Expression and mitogenic effect of fibroblast growth factor-9 in human endometriotic implant is regulated by aberrant production of estrogen. J Clin Endocrinol Metab 2003;88.Google Scholar
  110. 110.
    Fujimoto J, Hori M, Ichigo S, Hirose R, Tamaya T. Ability of ovarian steroids to regulate the expression of the fibroblast growth factor family in fibroblasts derived from uterine endometrium. J Biomed Sci 1996;3.Google Scholar
  111. 111.
    Presta M. Sex hormones modulate the synthesis of basic fibroblast growth factor in human endometrial adenocarcinoma cells: implications for the neovascularization of normal and neoplastic endometrium. J Cell Physiol 1988;137.Google Scholar
  112. 112.
    Rider V, Carlone DL, Foster RT. Oestrogen and progesterone control basic fibroblast growth factor mRNA in the rat uterus. J Endocrinol 1997;154.Google Scholar
  113. 113.
    Matsui H, Taga M, Kurogi K, Minaguchi H. Gene expressions of keratinocyte growth factor and its receptor in the human endometrium/decidua and chorionic villi. Endocr J 1997;44.Google Scholar
  114. 114.
    Eklund L, Olsen BR. Tie receptors and their angiopoietin ligands are context-dependent regulators of vascular remodeling. Exp Cell Res 2006;312:630–41.PubMedGoogle Scholar
  115. 115.
    Lee HJ, Cho CH, Hwang SJ, Choi HH, Kim KT, Ahn SY, et al. Biological characterization of angiopoietin-3 and angiopoietin-4. FASEB J 2004;18:1200–8.PubMedGoogle Scholar
  116. 116.
    Saharinen P, Kerkela K, Ekman N, Marron M, Brindle N, Lee GM, et al. Multiple angiopoietin recombinant proteins activate the Tie1 receptor tyrosine kinase and promote its interaction with Tie23. J Cell Biol 2005;169:239–43.PubMedGoogle Scholar
  117. 117.
    Wakui S, Yokoo K, Muto T, Suzuki Y, Takahashi H, Furusato M, et al. Localization of Ang-1, -2, Tie-2, and VEGF expression at endothelial-pericyte interdigitation in rat angiogenesis1. Lab Invest 2006;86:1172–84.PubMedGoogle Scholar
  118. 118.
    Sato TN, Tozawa Y, Deutsch U, Wolburg-Buchholz K, Fujiwara Y, Gendron-Maguire M, et al. Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation2. Nature 1995;376:70–4.PubMedGoogle Scholar
  119. 119.
    Hirchenhain J, Huse I, Hess A, Bielfeld P, De BF, Krussel JS. Differential expression of angiopoietins 1 and 2 and their receptor Tie-2 in human endometrium1. Mol Hum Reprod 2003;9:663–9.PubMedGoogle Scholar
  120. 120.
    Puri MC, Rossant J, Alitalo K, Bernstein A, Partanen J. The receptor tyrosine kinase TIE is required for integrity and survival of vascular endothelial cells4. EMBO J 1995;14:5884–91.PubMedGoogle Scholar
  121. 121.
    Roviezzo F, Tsigkos S, Kotanidou A, Bucci M, Brancaleone V, Cirino G, et al. Angiopoietin-2 causes inflammation in vivo by promoting vascular leakage1. J Pharmacol Exp Ther 2005;314:738–44.PubMedGoogle Scholar
  122. 122.
    Tait CR, Jones PF. Angiopoietins in tumours: the angiogenic switch. J Pathol 2004;204:1–10.PubMedGoogle Scholar
  123. 123.
    Matsumoto H, Ma WG, Daikoku T, Zhao X, Paria BC, Das SK, et al. Cyclooxygenase-2 differentially directs uterine angiogenesis during implantation in mice3. J Biol Chem 2002;277:29260–7.PubMedGoogle Scholar
  124. 124.
    Rowe AJ, Wulff C, Fraser HM. Localization of mRNA for vascular endothelial growth factor (VEGF), angiopoietins and their receptors during the peri-implantation period and early pregnancy in marmosets (Callithrix jacchus). Reproduction 2003;126:227–38.PubMedGoogle Scholar
  125. 125.
    Nayak NR, Kuo CJ, Desai TA, Wiegand SJ, Lasley BL, Giudice LC, et al. Expression, localization and hormonal control of angiopoietin-1 in the rhesus macaque endometrium: potential role in spiral artery growth1. Mol Hum Reprod 2005;11:791–9.PubMedGoogle Scholar
  126. 126.
    Wulff C, Wilson H, Largue P, Duncan WC, Armstrong DG, Fraser HM. Angiogenesis in the human corpus luteum: localization and changes in angiopoietins, tie-2, and vascular endothelial growth factor messenger ribonucleic acid. J Clin Endocrinol Metab 2000;85:4302–9.PubMedGoogle Scholar
  127. 127.
    Zhou Y, Bellingard V, Feng KT, McMaster M, Fisher SJ. Human cytotrophoblasts promote endothelial survival and vascular remodeling through secretion of Ang-2, PlGF, and VEGF-C9. Dev Biol 2003;263:114–25.PubMedGoogle Scholar
  128. 128.
    Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K, et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001;86:1823–34.PubMedGoogle Scholar
  129. 129.
    Kayisli UA, Cayli S, Seval Y, Tertemiz F, Huppertz B, Demir R. Spatial and temporal distribution of Tie-1 and Tie-2 during very early development of the human placenta. Placenta 2006;27:648–59.PubMedGoogle Scholar
  130. 130.
    Vuorela P, Carpen O, Tulppala M, Halmesmaki E. VEGF, its receptors and the tie receptors in recurrent miscarriage. Mol Hum Reprod 2000;6:276–82.PubMedGoogle Scholar
  131. 131.
    Pietrowski D, Tempfer C, Bettendorf H, Burkle B, Nagele F, Unfried G, et al. Angiopoietin-2 polymorphism in women with idiopathic recurrent miscarriage. Fertil Steril 2003;80:1026–9.PubMedGoogle Scholar
  132. 132.
    Ingman WV, Robertson SA. Defining the actions of transforming growth factor beta in reproduction. Bioessays 2002;24:904–14.PubMedGoogle Scholar
  133. 133.
    Pardali K, Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2006.Google Scholar
  134. 134.
    Relf M, LeJeune S, Scott PAE, Fox S, Smith K, Leek R, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res 1997;57:963–9.PubMedGoogle Scholar
  135. 135.
    Lilli C, Marinucci L, Bellocchio S, Ribatti D, Balducci C, Baroni T, et al. Effects of transforming growth factor-beta1 and tumour necrosis factor-alpha on cultured fibroblasts from skin fibroma as modulated by toremifene. Int J Cancer 2002;98:824–32.PubMedGoogle Scholar
  136. 136.
    Jadlowiec J, Dongell D, Smith J, Conover C, Campbell P. Pregnancy-associated plasma protein-a is involved in matrix mineralization of human adult mesenchymal stem cells and angiogenesis in the chick chorioallontoic membrane. Endocrinology 2005;146:3765–72.PubMedGoogle Scholar
  137. 137.
    Qian D, Lin HY, Wang HM, Zhang X, Liu DL, Li QL, et al. Involvement of ERK1/2 pathway in TGF-beta1-induced VEGF secretion in normal human cytotrophoblast cells. Mol Reprod Dev 2004;68:198–204.PubMedGoogle Scholar
  138. 138.
    Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, et al. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci U S A 1993;90:770–4.PubMedGoogle Scholar
  139. 139.
    Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, et al. Targeted disruption of the mouse transforming growth factor-beta 1 gene results in multifocal inflammatory disease. Nature 1992;359:693–9.PubMedGoogle Scholar
  140. 140.
    Kallapur S, Ormsby I, Doetschman T. Strain dependency of TGFbeta1 function during embryogenesis. Mol Reprod Dev 1999;52:341–9.PubMedGoogle Scholar
  141. 141.
    Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 1995;121:1845–54.PubMedGoogle Scholar
  142. 142.
    Larsson J, Goumans MJ, Sjostrand LJ, van Rooijen MA, Ward D, Leveen P, et al. Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice. EMBO J 2001;20:1663–73.PubMedGoogle Scholar
  143. 143.
    Giudice LC. Growth-factors and growth modulators in human uterine endometrium - their potential relevance to reproductive medicine. Fertil Steril 1994;61:1–17.PubMedGoogle Scholar
  144. 144.
    Ogasawara MS, Aoki K, Aoyama T, Katano K, Iinuma Y, Ozaki Y, et al. Elevation of transforming growth factor-beta1 is associated with recurrent miscarriage. J Clin Immunol 2000;20:453–7.PubMedGoogle Scholar
  145. 145.
    Lea RG, Underwood J, Flanders KC, Hirte H, Banwatt D, Finotto S, et al. A subset of patients with recurrent spontaneous abortion is deficient in transforming growth factor beta-2-producing “suppressor cells” in uterine tissue near the placental attachment site. Am J Reprod Immunol 1995;34:52–64.PubMedGoogle Scholar
  146. 146.
    Hossein H, Mahroo M, Abbas A, Firouzeh A, Nadia H. Cytokine production by peripheral blood mononuclear cells in recurrent miscarriage. Cytokine 2004;28:83–6.PubMedGoogle Scholar
  147. 147.
    Amani D, Dehaghani AS, Zolghadri J, Ravangard F, Niikawa N, Yoshiura K, et al. Lack of association between the TGF-beta1 gene polymorphisms and recurrent spontaneous abortion. J Reprod Immunol 2005;68:91–103.PubMedGoogle Scholar
  148. 148.
    Filicori M, Fazleabas AT, Huhtaniemi I, Licht P, Rao C, Tesarik J, et al. Novel concepts of human chorionic gonadotropin: reproductive system interactions and potential in the management of infertility. Fertil Steril 2005;84:275–84.PubMedGoogle Scholar
  149. 149.
    Berndt S, d'Hauterive SP, Blacher S, Pequeux C, Lorquet S, Munaut C, et al. Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium. FASEB J 2006.Google Scholar
  150. 150.
    Zygmunt M, Herr F, Keller-Schoenwetter S, Kunzi-Rapp K, Munstedt K, Rao CV, et al. Characterization of human chorionic gonadotropin as a novel angiogenic factor. J Clin Endocrinol Metab 2002;87:5290–6.PubMedGoogle Scholar
  151. 151.
    Toth P, Li X, Rao CV, Lincoln SR, Sanfilippo JS, Spinnato JA, et al. Expression of functional human chorionic gonadotropin/human luteinizing hormone receptor gene in human uterine arteries. J Clin Endocrinol Metab 1994;79:307–15.PubMedGoogle Scholar
  152. 152.
    Islami D, Bischof P, Chardonnens D. Modulation of placental vascular endothelial growth factor by leptin and hCG. Mol Hum Reprod 2003;9:395–8.PubMedGoogle Scholar
  153. 153.
    Herr F, Liang OD, Herrero J, Lang U, Preissner KT, Han VK, et al. Possible angiogenic roles of insulin-like growth factor II and its receptors in uterine vascular adaptation to pregnancy. J Clin Endocrinol Metab 2003;88:4811–7.PubMedGoogle Scholar
  154. 154.
    Volpert O, Jackson D, Bouck N, Linzer DI. The insulin-like growth factor II/mannose 6-phosphate receptor is required for proliferin-induced angiogenesis. Endocrinology 1996;137:3871–6.PubMedGoogle Scholar
  155. 155.
    Kwon YW, Kwon KS, Moon HE, Park JA, Choi KS, Kim YS, et al. Insulin-like growth factor-II regulates the expression of vascular endothelial growth factor by the human keratinocyte cell line HaCaT. J Invest Dermatol 2004;123:152–8.PubMedGoogle Scholar
  156. 156.
    Licht P, Russu V, Lehmeyer S, Moll J, Siebzehnrubl E, Wildt L. Intrauterine microdialysis reveals cycle-dependent regulation of endometrial insulin-like growth factor binding protein-1 secretion by human chorionic gonadotropin. Fertil Steril 2002;78:252–8.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Donald S. Torry
    • 1
    • 2
    Email author
  • Jonathan Leavenworth
    • 1
    • 2
  • Miao Chang
    • 1
    • 2
  • Vatsala Maheshwari
    • 1
    • 2
  • Kathleen Groesch
    • 1
    • 2
  • Evan R. Ball
    • 3
  • Ronald J. Torry
    • 3
  1. 1.Department of Medical Microbiology, Immunology and Cell BiologySouthern Illinois University School of MedicineSpringfieldUSA
  2. 2.Department of Obstetrics and GynecologySouthern Illinois University School of MedicineSpringfieldUSA
  3. 3.College of Pharmacy and Health SciencesDrake UniversityDes MoinesUSA

Personalised recommendations