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Endocrine

, Volume 12, Issue 1, pp 1–9 | Cite as

Angiogenesis in the corpus luteum

  • Lawrence P. ReynoldsEmail author
  • Anna T. Grazul-Bilska
  • Dale A. Redmer
Review

Abstract

The ovarian corpus luteum plays a critical role in reproduction because it is the primary source of circulating progesterone. After ovulation, as the corpus luteum forms from the wall of the ruptured follicle, it grows and vascularizes extremely rapidly. In fact, the rates of tissue growth and angiogenesis in the corpus luteum rival those of even the fastest growing tumors. Thus, the corpus luteum provides an outstanding model for studying the factors that regulate the angiogenic process, which is critical for normal tissue growth, development, and function. In agreement with data from other tissues, vascular endothelial growth factors (VEGF) seem to be a major angiogenic factor responsible for vascularization of the developing corpus luteum. Recent data suggest that luteal expression of VEGF occurs primarily in specific perivascular cells, including arteriolar smooth muscle and capillary pericytes, and is regulated primarily by oxygen levels. In addition, soon after ovulation, pericytes derived from the thecal compartment appear to be the first vascular cells to invade the developing luteal parenchyma. The granulosa-derived cells produce a factor that stimulates pericyte migration. Moreover, nitric oxide (NO), which is a potent vasodilator and can stimulate VEGF production and angiogenesis, is expressed in endothelial cells of luteal arterioles and capillaries, often in association with expression of VEGF by luteal perivascular cells. Thus, we have proposed a model for the initial process of luteal vascularization in which hypoxia plays a major role. In this model, which we believe will apply to other tissues as well, a paracrine loop exists between the vascular endothelial cells, which produce NO, and the peri-endothelial cells (vascular smooth muscle and pericytes), which produce VEGF, to ensure coordinate regulation of luteal vasodilation and angiogenesis.

Key Words

Corpus luteum angiogenesis vascular endothelial growth factor (VEGF) nitric oxide (NO) pericytes 

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References

  1. 1.
    Hudlicka, O. (1984). In: Handbook of physiology, sec. 2, vol. IV, Part 1. Renkin, E. M. and Michel, C. C. (eds.) Waverly Press: Baltimore.Google Scholar
  2. 2.
    Denekamp, J. (1984). In: Progress in applied microcirculation, vol. 4. Hammersen, F. and Hudlicka, O. (eds.) Karger: Basel, Switzerland.Google Scholar
  3. 3.
    Klagsbrun, M. and D’Amore, P. A. (1991). Annu. Rev. Physiol. 53, 217–239.PubMedCrossRefGoogle Scholar
  4. 4.
    Folkman, J. and Klagsbrun M. (1987). Science 233, 442–447.CrossRefGoogle Scholar
  5. 5.
    Reynolds, L. P., Killilea, S. D., and Redmer, D. A. (1992). FASEB J. 6, 886–892.PubMedGoogle Scholar
  6. 6.
    Reynolds, L. P., Killilea, S. D., Grazul-Bilska, A. T., and Redmer, D. A. (1994). Prog. Growth Factor Res. 5, 159–175.PubMedCrossRefGoogle Scholar
  7. 7.
    Redmer, D. A. and Reynolds, L.P. (1996). Rev. Reprod. 1, 182–192.PubMedCrossRefGoogle Scholar
  8. 8.
    Reynolds, L. P. and Redmer D. A. (1998). J. Anim. Sci. 76, 1671–1681.PubMedGoogle Scholar
  9. 9.
    Baserga, R. (1985). The biology of cell reproduction. Harvard University Press: Cambridge, MA.Google Scholar
  10. 10.
    Reynolds, L. P. and Redmer, D. A. (1995). J. Anim. Sci. 73, 1839–1851.PubMedGoogle Scholar
  11. 11.
    Jablonka-Shariff, A., Grazul-Bilska, A. T., Redmer, D. A., and Reynolds, L. P. (1993). Endocrinology 133, 1871–1879.PubMedCrossRefGoogle Scholar
  12. 12.
    Nicosia, S. V., Diaz, J., Nicosia, R. F., Saunders, B. O., and Muro-Cacho, C. (1995). Ann. Clin. Lab. Sci. 25, 143–157.PubMedGoogle Scholar
  13. 13.
    Christenson, L. K. and Stouffer, R. L. (1996). Endocrinology 137, 367–374.PubMedCrossRefGoogle Scholar
  14. 14.
    Farin, C. E., Moeller, C. L., Sawyer, H. R., Gamboni, F., and Niswender, G. D. (1986). Biol. Reprod. 35, 1299–1308.PubMedCrossRefGoogle Scholar
  15. 15.
    Lei, Z. M., Chegini, N., and Rao, C. V. (1991). Biol. Reprod. 44, 1148–1156.PubMedCrossRefGoogle Scholar
  16. 16.
    Reynolds, L. P. (1986). J. Anim. Sci. 62 (Suppl. 2), 47–61.PubMedGoogle Scholar
  17. 17.
    Swann, R. T. and Bruce, N. W. (1987). J. Reprod. Fertil. 80, 599–605.PubMedCrossRefGoogle Scholar
  18. 18.
    Adair, T. H., Gay, W. J., and Montani, J.-P. (1990). Am. J. Physiol. 259, R393-R404.PubMedGoogle Scholar
  19. 19.
    Clark, J. G. (1900). Johns Hopkins Hosp. Rep. 9, 593–676.Google Scholar
  20. 20.
    Nalbandov, A. V. and James, M. F. (1949). Am. J. Anat. 85, 347–377.PubMedCrossRefGoogle Scholar
  21. 21.
    Hay, M. F., Cran, D. G., and Moor, R. M. (1976). Cell Tissue Res. 169, 515–529.PubMedCrossRefGoogle Scholar
  22. 22.
    DiZerega, G.S. and Hodgen, G. D. (1980). J. Clin. Endocrinol. Metab. 51, 903–907.PubMedGoogle Scholar
  23. 23.
    McNatty, K. P., Dobson, C., Gibb, M., Kieboom, L. E., and Thurley, D. C. (1981). J. Endocrinol. 91, 99–109.PubMedGoogle Scholar
  24. 24.
    Zeleznik, A. J., Schuler, H. M., and Reichert, L. E. (1981). Endocrinology 109, 356–361.PubMedGoogle Scholar
  25. 25.
    Moor, R. M. and Seamark, R. F. (1986). J. Dairy Sci. 69, 927–943.PubMedCrossRefGoogle Scholar
  26. 26.
    Greenwald, G. S. (1989). Biol. Reprod. 41, 175–181.PubMedCrossRefGoogle Scholar
  27. 27.
    Jablonka-Shariff, A., Fricke, P. M., Grazul-Bilska, A. T., Reynolds, L. P., and Redmer, D. A. (1994). Biol. Reprod. 51, 531–540.PubMedCrossRefGoogle Scholar
  28. 28.
    Taraska, T., Reynolds, L. P., and Redmer, D. A. (1989). In: Growth factors and the ovary. Hirshfield, A. N. (ed.) Plenum, New York.Google Scholar
  29. 29.
    Redmer, D. A., Kirsch, J. D., and Reynolds, L. P. (1991). J. Anim. Sci. 69, 237–245.PubMedGoogle Scholar
  30. 30.
    Dharmarajan, A. M., Bruce, N. W., and Meyer, G. T. (1985). Am. J. Anat. 172, 87–99.PubMedCrossRefGoogle Scholar
  31. 31.
    Niswender, G. D. and Nett, T. M. (1988). In: The physiology of reproduction. Knobil, E. and Neill, J.D. et al., eds. Raven: New York.Google Scholar
  32. 32.
    Garverick, H. A. and Smith, M. F. (1986). J. Anim. Sci. 62 (Suppl. 2), 92–105.PubMedGoogle Scholar
  33. 33.
    Keisler, D. H. and Keisler, L. W. (1989). J. Reprod. Fertil. 87, 265–273.PubMedCrossRefGoogle Scholar
  34. 34.
    Hunter, M. G. (1991). J. Reprod. Fertil. Suppl. 43, 91–99.Google Scholar
  35. 35.
    Garverick, H. A., Zollers, W. G., Jr., and Smith, M. F. (1992). Anim. Reprod. Sci. 28, 111–124.CrossRefGoogle Scholar
  36. 36.
    Foley, G. L. (1996). Theriogenology 45, 1413–1428.PubMedCrossRefGoogle Scholar
  37. 37.
    Smith, G. D., Sawyer, H. R., Mirando, M. A., Griswold, M. D., Sadhu, A., and Reeves, J. J. (1996). Biol. Reprod. 55, 902–909.PubMedCrossRefGoogle Scholar
  38. 38.
    Jones, G. S., Maffezzoli, R. D., Strott, C. A., Ross, G. T., and Kaplan, G. (1970). Am. J. Obstetr. Gynecol. 108, 847–867.Google Scholar
  39. 39.
    Soules, M. R., Wiebe, R. H., Askel, S., and Hammond, C. B. (1977). Fertil. Steril. 29, 1033–1037.Google Scholar
  40. 40.
    Andrews, W. C. (1979). Fertil. Steril. 32, 501–509.PubMedGoogle Scholar
  41. 41.
    Smith, S. K., Lenton, E. A., Landren, B. M., and Cooke, I. D. (1985). Ann. NY Acad. Sci. 442, 387–390.PubMedCrossRefGoogle Scholar
  42. 42.
    Redmer, D. A., Rone, J. D., and Goodman, A. L. (1985). Proc. Soc. Exp. Biol. Med. 179, 136–140.PubMedGoogle Scholar
  43. 43.
    Redmer, D. A., Grazul, A. T., Kirsch, J. D., and Reynolds, L. P. (1988). J. Reprod. Fertil. 82, 627–634.PubMedCrossRefGoogle Scholar
  44. 44.
    Goede, V., Schmidt, T., Kimmina, S., Kozian, D., and Augustin, H. G. (1998). Lab. Invest. 78, 1385–1394.PubMedGoogle Scholar
  45. 45.
    Hazzard, T.M., Christenson, L.K., and Stouffer, R.L. (1999). Biol. Reprod. 60(Suppl. 1), 279.Google Scholar
  46. 46.
    Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999). FASEB J. 13, 9–22.PubMedGoogle Scholar
  47. 47.
    Ferrara, N. and Davis-Smyth, T. (1997). Endocrine Rev. 18, 4–25.CrossRefGoogle Scholar
  48. 48.
    Grazul-Bilska, A. T., Redmer, D. A., Killilea, S. D., Zheng, J., and Reynolds, L. P. (1993). Biochem. Cell Biol. 71, 270–277.PubMedGoogle Scholar
  49. 49.
    Grazul-Bilska, A. T., Redmer, D. A., Zheng, J., Killilea, S. D., and Reynolds, L. P. (1995). Growth Factors 12, 131–144.PubMedGoogle Scholar
  50. 50.
    Grazul-Bilska, A. T., Redmer, D. A., Killilea, S. D., Kraft, K. C., and Reynolds, L. P. (1992). Endocrinology 130, 3625–3632.PubMedCrossRefGoogle Scholar
  51. 51.
    Zheng, J., Redmer, D. A., and Reynolds, L. P. (1993). Biol. Reprod. 49, 1177–1189.PubMedCrossRefGoogle Scholar
  52. 52.
    Schams, D., Amselgruber, W., Einspanier, R., Sinowatz, F., and Gospodarowicz, D. (1994). Endocrine 2, 907–912.Google Scholar
  53. 53.
    Jablonka-Shariff, A., Grazul-Bilska, A. T., Redmer, D. A., and Reynolds, L. P. (1997). Growth Factors 14, 15–23.PubMedCrossRefGoogle Scholar
  54. 54.
    Grazul-Bilska, A. T., Redmer, D. A., Jablonka-Shariff, A., Biondini, M. E., and Reynolds, L. P. (1995). Can. J. Physiol. Pharmacol. 73, 491–500.PubMedGoogle Scholar
  55. 55.
    Stirling, D. T., Waterman, M. F., and Simpson, E. R. (1991). J. Reprod. Fertil. 91, 1–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Redmer, D. A., Kirsch, J. D., and Grazul, A. T. (1987). In: Regulation of ovarian and testicular function, Adv. Exp. Med. Biol. vol. 219. Mahesh, V. B., Dhindsa, D. S., Anderson, E., and Kalra, S. P. (eds.) Plenum, New York.Google Scholar
  57. 57.
    Grazul-Bilska, A. T., Reynolds, L. P., Slanger, W. D., and Redmer, D. A. (1992). J. Anim. Sci. 70, 254–262.PubMedGoogle Scholar
  58. 58.
    Ricke, W. A., Redmer, D. A., and Reynolds, L. P. (1995). Biol. Reprod. 52 (Suppl. 1), 112.Google Scholar
  59. 59.
    Ricke, W. A., Redmer, D. A., and Reynolds, L. P. (1999). J. Reprod. Fertil. 117, 369–377.PubMedCrossRefGoogle Scholar
  60. 60.
    Doraiswamy, V., Knutson, D. L., Grazul-Bilska, A. T., Redmer, D. A., and Reynolds, L. P. (1998). Growth Factors 125–135.Google Scholar
  61. 61.
    Miyamoto, A., Okuda, K., Schweigert, F. J., and Schams, D. (1992). J. Endocrinol. 135, 497–502.CrossRefGoogle Scholar
  62. 62.
    Liebermann, J., Schams, D., and Miyamoto, A. (1996). Reprod. Fertil. Dev. 8, 1003–1011.PubMedCrossRefGoogle Scholar
  63. 63.
    Tilly, J. L., Billig, H., Kowalski, K. I., and Hsueh, A. J. W. (1992). Mol. Endocrinol. 6, 1942–1950.PubMedCrossRefGoogle Scholar
  64. 64.
    Yasuda, T., Grinspan, J., Stern, J., Franceschini, B., Bannerman, P., and Pleasure, D. (1995). J. Neurosci. Res. 40, 306–317.PubMedCrossRefGoogle Scholar
  65. 65.
    Hanahan, D. (1997). Science 277, 48–50.PubMedCrossRefGoogle Scholar
  66. 66.
    Ferrara, N., Chen, H., Davis-Smyth, T., Gerber, H. P., Nguyen, T. N., Peers, D., Chisolm, V., Hillan, K. J., and Schwall, R. H. (1998). Nature Med. 4, 336–340.PubMedCrossRefGoogle Scholar
  67. 67.
    Redmer, D. A., Dai, Y., Li, J., Charnock-Jones, D. S., Smith, S. K., Reynolds, L. P., and Moor, R. M. (1996). J. Reprod. Fertil. 108, 157–165.PubMedCrossRefGoogle Scholar
  68. 68.
    Doraiswamy, V., Grazul-Bilska, A. T., Ricke, W. A., Redmer, D. A., and Reynolds, L. P. (1995). Biol. Reprod. 52 (Suppl. 1), 112.Google Scholar
  69. 69.
    Ravindranath, N., Little-Ihrig, L., Phillips, H. S., Ferrara, N., and Zeleznik, A. J. (1992). Endocrinology 131, 254–260.PubMedCrossRefGoogle Scholar
  70. 70.
    Phillips, H. S., Hains, J., Leung, D. W., and Ferrara, N. (1990). Endocrinology 127, 956–967.CrossRefGoogle Scholar
  71. 71.
    Yan, Z., Weich, H. A., Bernart, W., Breckwoldt, M., and Neulen, J. (1993). J. Clin. Endocrinol. Metab. 77, 1723–1725.PubMedCrossRefGoogle Scholar
  72. 72.
    Kamat, B. R., Brown, L. F., Manseau, E. J., Senger, D. R., and Dvorak, H. F. (1995). Am. J. Pathol. 146, 157–165.PubMedGoogle Scholar
  73. 73.
    Toutges, M. J., Grazul-Bilska, A. T., Kirsch, J. D., Reynolds, L. P., and Redmer, D. A. (1999). Biol. Reprod. 60(Suppl. 1), 280.Google Scholar
  74. 74.
    Garrido, C., Saule, S., and Gospodarowicz, D. (1993). Growth Factors 8, 109–117.PubMedGoogle Scholar
  75. 75.
    Koos, R. D. (1995). Biol. Reprod. 52, 1426–1435.PubMedCrossRefGoogle Scholar
  76. 76.
    Silvester, L. M. and Luck, M. R. (1999). J. Reprod. Fertil. 116, 187–198.PubMedCrossRefGoogle Scholar
  77. 77.
    Doraiswamy, V. D. (1998). PhD Thesis. North Dakota State University, Fargo.Google Scholar
  78. 78.
    Neeman, M., Abramovitch, R., Schiffenbauer, Y. S., and Tempel, C. (1997). Int. J. Exp. Pathol. 78, 57–70.PubMedCrossRefGoogle Scholar
  79. 79.
    Yamagishi, S.-I., Yonekura, H., Yamamoto, Y., Fujimori, H., Sakurai, S., Tanake, N., and Yamamoto, H. (1999). Lab. Invest. 79, 501–509.PubMedGoogle Scholar
  80. 80.
    Antonelli-Orlidge, A., Smith, S. R., and D’Amore, P. A. (1989). Am. Rev. Respir. Dis. 140, 1129–1131.PubMedGoogle Scholar
  81. 81.
    Hoover, G. A., McCormick, S., and Kalant, N. (1989). Arteriosclerosis 9, 76–83.PubMedGoogle Scholar
  82. 82.
    Folkman, J. and D’Amore, P. A. (1996). Cell 87, 1153–1155.PubMedCrossRefGoogle Scholar
  83. 83.
    Hirschi, K. K. and D’Amore, P. A. (1996). Pericytes in the microvasculature. Cardiovasc. Res. 32, 687–696.PubMedCrossRefGoogle Scholar
  84. 84.
    Shifren, J. L., Doldi, N., Ferrara, N., Mesiano, S., and Jaffe, R. B. (1994). J. Clin. Endocrinol. Metab. 79, 316–322.PubMedCrossRefGoogle Scholar
  85. 85.
    Aiello, L. P., Northrup, J. M., Keyt, B. A., Takagi, H., and Iwamoto, M. A. (1995). Arch. Opthalmol. 113, 1538–1544.Google Scholar
  86. 86.
    Nomura, M., Yamagishi, S., Harada, S., Hayashi, Y., Yamashima, T., Yamashita, J., and Yamamoto, H. (1995), J. Biol. Chem. 270, 28,316–28,324.Google Scholar
  87. 87.
    Stavri, G. T., Zachary, I. C., Baskerville, P. A., Martin, J. F., and Erusalimsky, J. D. (1995). Circulation 92, 11–14.PubMedGoogle Scholar
  88. 88.
    Neufeld, G., Ferrara, N., Schweigerer, L., Mitchell, R., and Gospodarowicz, D. (1987). Endocrinology 121, 597–603.PubMedCrossRefGoogle Scholar
  89. 89.
    Wordinger, R. J., Brun-Zinkernagel, A.-M., and Chang, I.-F. C. (1993). Growth Factors 9, 279–289.PubMedCrossRefGoogle Scholar
  90. 90.
    Redmer, D. A., MacDonald, H. E., Klemin, P. L., Kirsch, J. D., Kraft, K. C., Johnson, M. L., Reynolds, L. P., and Grazul-Bilska, A. T. (1999). Biol. Reprod. 60(Suppl. 1), 172.Google Scholar
  91. 91.
    Chin, K., Kurashima, Y., Ogura, T., Tajiri, H., Yoshida, S., and Esumi, H. (1997). Oncogene 15, 437–442.PubMedCrossRefGoogle Scholar
  92. 92.
    Frank, S., Stallmeyer, B., Kampfer, H., Schaffner, C., and Pfeilschifter, J. (1999). Biochem. J. 338, 367–374.PubMedCrossRefGoogle Scholar
  93. 93.
    Van der Zee, R., Murohara, T., Luo, Z., Zollmann, F., Passeri, J., Lekutat, C., and Isner, J. M. (1997). Circulation 95, 1030–1037.PubMedGoogle Scholar
  94. 94.
    Hood, J. D., Meininger, C. J., Ziche, M., and Granger, H. J. (1998). Am. J. Physiol. 274, H1054-H1058.PubMedGoogle Scholar
  95. 95.
    Kroll, J. and Waltenberger, J. (1998). Biochem. Biophys. Res. Commun. 252, 743–746.PubMedCrossRefGoogle Scholar
  96. 96.
    Bouloumie, A., Schini-Kerth, V. B., and Busse, R. (1999). Cardiovasc. Res. 41, 773–780.PubMedCrossRefGoogle Scholar
  97. 97.
    Anthony, F. W., Gornall, R. J., Lincoln, J., Richardson, M. C., Hitchcock, A., and Stones, R. W. (1997). J. Reprod. Fertil. Abstr. Ser. 19, 63.Google Scholar
  98. 98.
    Lamming, G. E., Darwash, A. O., and Back, H. L. (1989). J. Reprod. Fertil. Suppl. 37, 245–252.Google Scholar
  99. 99.
    Short, R. E., Bellows, R. A., Staigmiller, R. B., Berardinelli, J. G., and Custer, E. E. (1990). J. Anim. Sci. 68, 799–816.PubMedGoogle Scholar
  100. 100.
    Darland, N. W. (1985). J. Obstet. Gynecol. Neonatal Nurs. 14, 212–217.PubMedCrossRefGoogle Scholar
  101. 101.
    Karamardian, L. M. and Grimes, D. A. (1992). Am. J. Obstet. Gynecol. 167, 1391–1398.PubMedGoogle Scholar
  102. 102.
    Dickson, S. E. and Fraser, H. M. (1999). Biol. Reprod. 60 (Suppl. 1), 279–280.Google Scholar
  103. 103.
    Barinaga, M. (1997). Science 275, 482–484.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc 2000

Authors and Affiliations

  • Lawrence P. Reynolds
    • 1
    Email author
  • Anna T. Grazul-Bilska
    • 1
  • Dale A. Redmer
    • 1
  1. 1.Department of Animal and Range Sciences, and Cell Biology Center, Biotechnology InstituteNorth Dakota State UniversityFargo

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