Endocrine

, Volume 19, Issue 1, pp 91–102

Placental stress factors and maternal-fetal adaptive response

The corticotropin-releasing factor family
  • Pasquale Florio
  • Filiberto M. Severi
  • Pasquapina Ciarmela
  • Giovina Fiore
  • Giulia Calonaci
  • Angelica Merola
  • Claudio De Felice
  • Marco Palumbo
  • Felice Petraglia
Article

Abstract

The placenta and its accessory membranes amnion and chorion undertake the role of intermediary barriers and active messengers in the maternal-fetal dialog. They synthesize, metabolize, and serve as target to numerous hormones that regulate maternal and fetal physiology during pregnancy. Among these factors, corticotropin-releasing factor (CRF) has been one of the more investigated in the last decade. Increasing evidence indicates that in the event of acute or chronic metabolic, physical, or infectious stress, maternal or fetal physiologic and pathologic conditions may influence placental secretion of CRF. The current opinion is that the placenta actually takes part in a stress syndrome by releasing CRF, which may help to influence uterine perfusion, maternal metabolism, fluid balance, and possibly uterine contractility, thereby protecting the fetus from a hostile environment.

Key Words

Corticotropin-releasing factor urocortin syncytrotrophoblast adrenocorticotropic hormone parturition preeclampsia 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Petraglia, F., Volpe, A., Genazzani, A. R., Rivier, J., Sawchenko, P. E., and Vale, W. (1990). Front. Neuroendocrinol. 11, 6–37.Google Scholar
  2. 2.
    Petraglia, F., Florio, P., Nappi, C., and Genazzani, A. R. (1996). Endocr. Rev. 17, 156–186.PubMedCrossRefGoogle Scholar
  3. 3.
    Petraglia, F. (1996). Eur. J. Endocrinol. 135, 166, 167.PubMedGoogle Scholar
  4. 4.
    Reis, F. M., Florio, P., Cobellis, L., Luisi, S., Severi, F. M., Bocchi, C., Picciolini, E., Centini, G., and Petraglia, F. (2001). Biol. Neonate 79, 150–156.PubMedCrossRefGoogle Scholar
  5. 5.
    Petraglia, F., Sawchenko, P. E., Rivier, J., and Vale, W. (1987). Nature 328, 717–719.PubMedCrossRefGoogle Scholar
  6. 6.
    Petraglia, F., Tabanelli, S., Galassi, M. C., Garuti, G. C., Mancini, A. C., Genazzani, A. R., and Gurpide, E. (1992). J. Clin. Endocrinol. Metab. 74, 1427–1431.PubMedCrossRefGoogle Scholar
  7. 7.
    Vale, W., Rivier, C., Brown, M. R., Spiess, J., Koob, G., Swanson, L., Bilezikjian, L., Bloom, F., and Rivier, J. (1983). Recent Prog. Horm. Res. 39, 245–270.PubMedGoogle Scholar
  8. 8.
    Orth, D. N. (1992). Endocr. Rev. 13, 164–191.PubMedCrossRefGoogle Scholar
  9. 9.
    Shibasaki, T., Odagiri, E., Shizume, K., and Ling, N. (1982). J. Clin. Endocrinol. Metab. 55, 384–386.PubMedGoogle Scholar
  10. 10.
    Sasaki, A., Tempst, P., Lotta, A. S., Margioris, A. N., Hood, L. E., Kent, S. B., Sato, S., Shinkawa, O., Yoshinaga, K., and Krieger, D. T. (1988). J. Clin. Endocrinol. Metab. 67, 768–773.PubMedGoogle Scholar
  11. 11.
    Schulte, H. M. and Healy, D. L. (1987). Horm. Metab. Res. 16, 44–46.Google Scholar
  12. 12.
    Frim, D. M., Emanuel, R. L., Robinson, B. G., Smas, C. M., Adler, G. K., and Majzoub, J. A. (1988). J. Clin. Invest. 82, 287–292.PubMedGoogle Scholar
  13. 13.
    Grino, M., Chrousos, G. P., and Margioris, A. N. (1987). Biochem. Biophys. Res. Commun. 148, 1208–1214.PubMedCrossRefGoogle Scholar
  14. 14.
    Saijonmaa, X., Laatikainen, T., and Walhstrom, T. (1988). Placenta 9, 373–385.PubMedGoogle Scholar
  15. 15.
    Riley, S. C., Walton, J. C., Herlick, J. M., and Challis, J. R. (1991). J. Clin. Endocrinol. Metab. 72, 1001–1007.PubMedGoogle Scholar
  16. 16.
    Jones, S. A., Brooks, A. N., and Challis, J. R. (1989). J. Clin. Endocrinol. Metab. 68, 825–830.PubMedGoogle Scholar
  17. 17.
    Riley, S. C. and Challis, J. R. (1991). Placenta 12, 105–119.PubMedGoogle Scholar
  18. 18.
    Robinson, B. G., Emanuel, R. L., Frim, D. M., and Majzoub, J. A. (1988). Proc. Natl. Acad. Sci. USA 85, 5244–5248.PubMedCrossRefGoogle Scholar
  19. 19.
    Warren, W. B. and Silverman, A. J. (1995). Placenta 16, 147–156.PubMedCrossRefGoogle Scholar
  20. 20.
    Di Blasio, A. M., Giraldi, F. P., Vigano, P., Petraglia, F., Vignali, M., and Cavagnini, F. (1997). J. Clin. Endocrinol. Metab. 82, 1594–1597.PubMedCrossRefGoogle Scholar
  21. 21.
    Ferrari, A., Petraglia, F., and Gurpide, E. (1995). J. Steroid Biochem. Mol. Biol. 54, 251–255.PubMedCrossRefGoogle Scholar
  22. 22.
    Petraglia, F., Florio, P., Gallo, R., Salvestroni, C., Lombardo, M., Genazzani, A. D., Di Carlo, C., Stomati, M., D’Ambrogio, G., and Artini, P. G. (1996). Horm. Res. 45, 187–191.PubMedGoogle Scholar
  23. 23.
    Potter, E., Behan, D. P., Fischer, W. H., Linton, E. A., Lowry, P. J., and Vale, W. W. (1991). Nature 349, 423–426.PubMedCrossRefGoogle Scholar
  24. 24.
    Potter, E., Behan, D. P., Linton, E. A., Lowry, P. J., Sawchenko, P. E., and Vale, W. W. (1992). Proc. Natl. Acad. Sci. USA 89, 4192–4196.PubMedCrossRefGoogle Scholar
  25. 25.
    Petraglia, F., Potter, E., Cameron, V. A., Sutton, S., Behan, D. P., Woods, R. J., Sawchenko, P. E., Lowry, P. J., and Vale, W. (1993). J. Clin. Endocrinol. Metab. 77, 919–924.PubMedCrossRefGoogle Scholar
  26. 26.
    Challis, J. R., Matthews, S. G., Meir, C. V., and Ramirez, M. M. (1995). Placenta 16, 481–502.PubMedCrossRefGoogle Scholar
  27. 27.
    Linton, E. A., Wolfe, C. D. A., Behan, D., and Lowry, P. J. (1988). Clin. Endocrinol. 28, 315–324.Google Scholar
  28. 28.
    Orth, D. N. and Mount, C. D. (1987). Biochem. Biophys. Res. Commun. 143, 411–417.PubMedCrossRefGoogle Scholar
  29. 29.
    Suda, T., Iwashita, M., Sumitomo, T., Nakano, Y., Tozawa, F., and Demura, H. (1991). Acta Endocrinol. 125, 165–169.PubMedGoogle Scholar
  30. 30.
    Vaughan, J., Donaldson, C., Bittencourt, J., Perrin, M. H., Lewis, K., Sutton, S., Chan, R., Turnbull, A. V., Lovejoy, D., Rivier, C., and Vale, W. W. (1995). Nature 378, 287–292.PubMedCrossRefGoogle Scholar
  31. 31.
    Petraglia, F., Florio, P., Gallo, R., Simoncini, T., Giuntini, A., and Genazzani, A. R. (1996). J. Clin. Endocrinol. Metab. 81, 3807–3810.PubMedCrossRefGoogle Scholar
  32. 32.
    Florio, P., Rivest, S., Reis, F. M., Simoncini, T., Martinelli, P., Genazzani, A. R., and Petraglia, F. (1999). Prenat. Neonat. Med. 4, 296–300.Google Scholar
  33. 33.
    Chen, R., Lewis, K., Perrin, M. H., and Vale, W. (1993). Proc. Natl. Acad. Sci. USA 90, 8967–8971.PubMedCrossRefGoogle Scholar
  34. 34.
    Liaw, C. W., Lovenmerg, T. W., Barry, G., Oltersdorf, T., Grigoriadis, E., and De Souza, E. B. (1996). Endocrinology 137, 72–77.PubMedCrossRefGoogle Scholar
  35. 35.
    Valdenaire, O., Giller, T., Breu, V., Gottiwik, J., and Kilpatric, G. (1997). Biochim. Biophys. Acta 135, 129–132.Google Scholar
  36. 36.
    Karteris, E., Grammatopoulos, D., Dai, Y., Olah, K. B., Ghobara, T. B., Easton, A., and Hillhouse, E. W. (1998). J. Clin. Endocrinol. Metab. 83, 1376–1379.PubMedCrossRefGoogle Scholar
  37. 37.
    Florio, P., Franchini, A., Reis, F. M., Pezzani, I., Ottaviani, E., and Petraglia, F. (2000). Placenta 21, 32–37.PubMedCrossRefGoogle Scholar
  38. 38.
    Rodrýguez-Linares, B., Linton, E. A., and Phaneuf, S. (1998). J. Endocrinol. 156, 15–21.CrossRefGoogle Scholar
  39. 39.
    Grammatopoulos, D., Dai, Y., Chen, J., Karteris, E., Papadopoulou, N., Easton, A. J., and Hillhouse, E. W. (1998). J. Clin. Endocrinol. Metab. 83, 2539–2544.PubMedCrossRefGoogle Scholar
  40. 40.
    Petraglia, F., Florio, P., Benedetto, C., Marzio, L., Di Blasio, A. M., Ticconi, C., Piccione, E., Luisi, S., Genazzani, A. R., and Vale, W. (1999). J. Clin. Endocrinol. Metab. 84, 1420–1423.PubMedCrossRefGoogle Scholar
  41. 41.
    Margioris, A. N., Grino, M., Protos, P., Gold, P. W., and Chrousos, G. P. (1988). J. Clin. Endocrinol. Metab. 66, 922–926.PubMedGoogle Scholar
  42. 42.
    Jones, S. A. and Challis, J. R. (1989). Biochem. Biophys. Res. Commun. 159, 192–199.PubMedCrossRefGoogle Scholar
  43. 43.
    Benedetto, C., Petraglia, F., Marozio, L., Chiarolini, L., Florio, P., Genazzani, A. R., and Massobrio, M. (1994). Am. J. Obstet. Gynecol. 171, 126–131.PubMedGoogle Scholar
  44. 44.
    Petraglia, F., Benedetto, C., Florio, P., D’Ambrogio, G., Genazzani, A. D., Marozio, L., and Vale, W. (1995). J. Clin. Endocrinol. Metab. 80, 3073–3076.PubMedCrossRefGoogle Scholar
  45. 45.
    Jones, S. A. and Challis, J. R. (1990). Gynecol. Obstet. Invest. 29, 165–168.PubMedCrossRefGoogle Scholar
  46. 46.
    Florio, P., Lombardo, M., Gallo, R., Di Carlo, C., Sutton, S., Genazzani, A. R., and Petraglia, F. (1996). Placenta 17, 307–311.PubMedCrossRefGoogle Scholar
  47. 47.
    Grammatopoulos, D. K. and Hillhouse, E. W. (1999). Lancet 354, 1546–1549.PubMedCrossRefGoogle Scholar
  48. 48.
    Quartero, H. W. and Fry, C. H. (1989). Placental corticotrophin releasing factor may modulate human parturition. Placenta 10, 439–443.PubMedGoogle Scholar
  49. 49.
    Quartero, H. W., Srivatsa, G., and Gillham, B. (1992). Clin. Endocrinol. (Oxf.) 36, 141–145.Google Scholar
  50. 50.
    Simpkin, J. C., Kermani, F., Palmer, A. M., Campa, J. S., Tribe, R. M., Linton, E. A., and Poston, L. (1999). Br. J. Obstet. Gynaecol. 106, 439–445.PubMedGoogle Scholar
  51. 51.
    Hillhouse, E. W. and Grammatopoulos, D. K. (2000). Stress 4, 235–246.CrossRefGoogle Scholar
  52. 52.
    Grammatopoulos, D. K., Randeva, H. S., Levine, M. A., Katsanou, E. S., and Hillhouse, E. W. (2000). Mol. Endocrinol. 14, 2076–2091.PubMedCrossRefGoogle Scholar
  53. 53.
    MacCannell, K. L., Hamilton, P. L., Lederis, K., Newton, C. A., and Rivier, J. (1984). Gastroenterology 87, 94–102.PubMedGoogle Scholar
  54. 54.
    Hermus, A. R., Pieters, G. F., Willemsen, J. J., Ross, H. A., Smals, A. G., Benraad, T. J., and Kloppenborg, P. W. (1987). Eur. J. Clin. Pharmacol. 31, 531–534.PubMedCrossRefGoogle Scholar
  55. 55.
    Kiang, J. G. and Wei, E. T. (1987). J. Pharmacol. Exp. Ther. 243, 517–520.PubMedGoogle Scholar
  56. 56.
    Corder, R., Turnill, D., Ling, N., and Gaillard, R. C. (1992). Peptides 13, 1–6.PubMedCrossRefGoogle Scholar
  57. 57.
    Lei, S., Richter, R., Bienert, M., and Mulvany, M. J. (1993). Br. J. Pharmacol. 108, 941–947.PubMedGoogle Scholar
  58. 58.
    Challis, J. R. G., Matthews, S. G., Gibb, W., and Lye, S. J. (2000). Endocr. Rev. 21, 514–550.PubMedCrossRefGoogle Scholar
  59. 59.
    Clifton, V. L., Read, M. A., Leitch, I. M., Boura, A. L., Robinson, P. J., and Smith, R. (1994). J. Clin. Endocrinol. Metab. 79, 666–669.PubMedCrossRefGoogle Scholar
  60. 60.
    Simoncini, T., Apa, R., Reis, F. M., Miceli, F., Stomati, M., Driul, L., Lanzone, A., Genazzani, A. R., and Petraglia, F. (1999). J. Clin. Endocrinol. Metab. 84, 2802–2806.PubMedCrossRefGoogle Scholar
  61. 61.
    Clifton, V. L., Read, M. A., Leitch, I. M., Giles, W. B., Boura, A. L., Robinson, P. J., and Smith, R. (1995). J. Clin. Endocrinol. Metab. 80, 2888–2893.PubMedCrossRefGoogle Scholar
  62. 62.
    Torpy, D. J., Webster, E. L., Zachman, E. K., Aguilera, G., and Chrousos, G. P. (1999). Neuroimmunomodulation 6, 182–186.PubMedCrossRefGoogle Scholar
  63. 63.
    Leitch, I. M., Boura, A. L., Botti, C., Read, M. A., Walters, W. A., and Smith, R. (1998). J. Clin. Endocrinol. Metab. 83, 4510–4513.PubMedCrossRefGoogle Scholar
  64. 64.
    Boura, A. L., Walters, W. A., Read, M. A., and Leitch, I. M. (1994). Clin. Exp. Pharmacol. Physiol. 21, 737–748.PubMedCrossRefGoogle Scholar
  65. 65.
    Reis, F. M., Fadalti, M., Florio, P., and Petraglia, F. (1999). J. Soc. Gynecol. Invest. 6, 109–119.CrossRefGoogle Scholar
  66. 66.
    Clifton, V. L., Read, M. A., Boura, A. L., Robinson, P. J., and Smith, R. (1996). J. Clin. Endocrinol. Metab. 81, 1406–1410.PubMedCrossRefGoogle Scholar
  67. 67.
    Furchgott, R. F. (1993). J. Cardiovasc. Pharmacol. 22, S1-S2.PubMedGoogle Scholar
  68. 68.
    Brayden, J. E. and Nelson, M. T. (1992). Science 256, 532–535.PubMedCrossRefGoogle Scholar
  69. 69.
    Jain, V., Shi, S. Q., Vedernikov, Y. P., Saade, G. R., Chwalisz, K., and Garfield, R. E. (1998). Am. J. Obstet. Gynecol. 178, 186–191.PubMedCrossRefGoogle Scholar
  70. 70.
    Jain, V., Vedernikov, Y. P., Saade, G. R., Chwalisz, K., and Garfield, R. E. (1999). J. Pharmacol. Exp. Ther. 288, 407–413.PubMedGoogle Scholar
  71. 71.
    Sue-Tang, A., Bocking, A. D., Brooks, A. N., Hooper, S., White, S. E., Jacobs, R. A., Fraher, L. J., and Challis, J. R. (1992). Can. J. Physiol. Pharmacol. 70, 1396–1402.Google Scholar
  72. 72.
    Gagnon, R., Murotsuki, J., Challis, J. R., Fraher, L., and Richardson, B. S. (1997). Am. J. Physiol. 272, E817-E823.PubMedGoogle Scholar
  73. 73.
    Goland, R. S., Jozak, S., and Conwell, I. (1994). Am. J. Obstet. Gynecol. 171, 1287–1291.PubMedGoogle Scholar
  74. 74.
    Laatikainen, T., Virtanen, T., Raisanen, I., and Salminen, K. (1987). Neuropeptides 10, 343–353.PubMedCrossRefGoogle Scholar
  75. 75.
    Allolio, B., Hoffmann, J., Linton, E. A., Winkelmann, W., Kusche, M., and Schulte, H. M. (1990). Clin. Endocrinol. (Oxf.) 33, 279–289.Google Scholar
  76. 76.
    Barbieri, R. L. (1994). In: Maternal-fetal endocrinology, 2nd ed. Tulchinsky, D. and Little, A. B. (eds.). W.B. Saunders: Philadelphia, pp. 751–784.Google Scholar
  77. 77.
    Sasaki, A., Shinkawa, O., and Yoshinaga, K. (1989). J. Clin. Invest. 84, 1997–1901.PubMedGoogle Scholar
  78. 78.
    Schulte, H. M., Weisner, D., and Allolio, B. (1990). Clin. Endocrinol. 33, 99–106.Google Scholar
  79. 79.
    Marinoni, E., Korebrits, C., Di Iorio, R., Cosmi, E. V., and Challis, J. R. (1998). Am. J. Obstet. Gynecol. 178, 770–778.PubMedCrossRefGoogle Scholar
  80. 80.
    Tropper, P. J., Goland, R. S., Wardlaw, S. L., Fox, H. E., and Frantz, A. G. (1987). J. Perinat. Med. 15, 221–225.PubMedCrossRefGoogle Scholar
  81. 81.
    Ohrlander, S. A., Gennser, G. M., and Grennert, L. (1975). Am. J. Obstet. Gynecol. 123, 228–236.PubMedGoogle Scholar
  82. 82.
    Chan, E. C., Smith, R., Lewin, T., Brinsmead, M. W., Zhang, H. P., Cubis, J., Thornton, K., and Hurt, D. (1993). Acta Endocrinol. 128, 339–344.PubMedGoogle Scholar
  83. 83.
    Petraglia, F., Genazzani, A. D., Aguzzoli, L., Gallinelli, A., de Vita, D., Caruso, A., and Genazzani, A. R. (1994). Acta Obstet. Gynecol. Scand. 73, 284–289.PubMedGoogle Scholar
  84. 84.
    Stalla, G. K., Bost, H., and Stalla, J. (1989). Gynecol. Endocrinol. 3, 1–10.PubMedGoogle Scholar
  85. 85.
    Blumenfeld, Z. and Jaffe, R. G. (1986). J. Clin. Invest. 38, 288–294.Google Scholar
  86. 86.
    Smith, R., Mesiano, S., Chan, E. C., Brown, S., and Jaffe, R. B. (1998). J. Clin. Endocrinol. Metab. 83, 2916–2920.PubMedCrossRefGoogle Scholar
  87. 87.
    Petraglia, F., Lim, A. T., and Vale, W. (1987). J. Clin. Endocrinol. Metab. 65, 1020–1025.PubMedGoogle Scholar
  88. 88.
    Petraglia, F., Sutton, S., and Vale, W. (1989). Am. J. Obstet. Gynecol. 160, 247–251.PubMedGoogle Scholar
  89. 89.
    Sastry, B. V. (1997). Biochem. Pharmacol. 53, 1577–1586.PubMedCrossRefGoogle Scholar
  90. 90.
    Rivier, C. L. and Plotsky, P. M. (1986). Annu. Rev. Physiol. 48, 475–494.PubMedCrossRefGoogle Scholar
  91. 91.
    Plotsky, P. M., Cunningham, E. T. Jr., and Widmaier, E. P. (1989). Endocr. Rev. 10, 437–458.PubMedGoogle Scholar
  92. 92.
    Suh, B. Y., Liu, J. H., Rasmussenm, D. D., Gibbs, D. M., Steinberg, J., and Yen, S. S. (1986). Neuroendocrinology 44, 309–313.PubMedGoogle Scholar
  93. 93.
    Plotsky, P. M., Thrivikraman, K. V., and Meaney, M. J. (1993). Ciba Found. Symp. 172, 59–75PubMedGoogle Scholar
  94. 94.
    Plotsky, P. M. (1988). Adv. Exp. Med. Biol. 245, 65–81.PubMedGoogle Scholar
  95. 95.
    Campbell, E. A., Linton, E. A., Wolfe, C. D. A., Scraggs, P. R., Jones, M. T., and Lowry, P. J. (1987). J. Clin. Endocrinol. Metab. 63, 1054–1059.CrossRefGoogle Scholar
  96. 96.
    McLean, M., Bisit, A., Davies, J. J., Woods, R. J., Lowry, P. J., and Smith, R. (1995). Nat. Med. 1, 460–463.PubMedCrossRefGoogle Scholar
  97. 97.
    Sorem, K. A., Smikle, C. B., Spencer, D. K., Yoder, B. A., Graveson, M. A., and Siler-Khodr, T. M. (1996). Am. J. Obstet. Gynecol. 175, 912–916.PubMedCrossRefGoogle Scholar
  98. 98.
    Berkowitz, G. S., Lapinski, R. H., Lockwood, C. J., Florio, P., Blackmore Prince, C., and Petraglia, F. (1996). Am. J. Obstet. Gynecol. 174, 1477–1483.PubMedCrossRefGoogle Scholar
  99. 99.
    Petraglia, F., Florio, P., Benedetto, C., Gallo, C., Woods, R. J., Genazzani, A. R., and Lowry, P. J. (1996). J. Clin. Endocrinol. Metab. 81, 852–856.PubMedCrossRefGoogle Scholar
  100. 100.
    Economides, D., Linton, E., Nicolaides, K., Rodeck, C. H., Lowry, P. J., and Chard, T. (1987). J. Endocrinol. 114, 497–501.PubMedCrossRefGoogle Scholar
  101. 101.
    Goland, R. S., Wardlaw, S. L., Blum, M., Tropper, P. J., and Stark, R. I. (1988). Am. J. Obstet. Gynecol. 159, 884–890.PubMedGoogle Scholar
  102. 102.
    Laatikainen, T. J., Raisanen, I. J., and Salminen, K. R. (1988). Am. J. Obstet. Gynecol. 159, 891–895.PubMedGoogle Scholar
  103. 103.
    Sasaki, A., Shinkawa, O., and Yoshinaga, K. (1990). Am. J. Obstet. Gynecol. 162, 194–198.PubMedGoogle Scholar
  104. 104.
    Linton, E. A., Perkins, A. V., Woods, R. J., Eben, F., Wolfe, C. D., Behan, D. P., Potter, E., Vale, W. W., and Lowry, P. J. (1993). J. Clin. Endocrinol. Metab. 76, 260–262.PubMedCrossRefGoogle Scholar
  105. 105.
    Perkins, A. V., Eben, F., Wolfe, C. D., Schulte, H. M., and Linton, E. A. (1993). J. Endocrinol. 138, 149–157.PubMedGoogle Scholar
  106. 106.
    Petraglia, F., Florio, P., Simoncini, T., Woods, R. J., Giuntini, A., Gremigni, R., Serra, G. B., Genazzani, A. R., and Lowry, P. J. (1997). Placenta 18, 115–119.PubMedCrossRefGoogle Scholar
  107. 107.
    Florio, P., Woods, R. J., Genazzani, A. R., Lowry, P. J., and Petraglia, F. (1997). J. Clin. Endocrinol. Metab. 82, 835–838.PubMedCrossRefGoogle Scholar
  108. 108.
    Glynn, B. P., Wolton, A., Rodriguez-Linares, B., Phaneuf, S., and Linton, E. A. (1998). Am. J. Obstet. Gynecol. 179, 533–539.PubMedCrossRefGoogle Scholar
  109. 109.
    Watanabe, F., Oki, Y., Ozawa, M., Masuzawa, M., Iwabuchi, M., Yoshimi, T., Nishiguchi, T., Iino, K., and Sasano, H. (1999). Peptides 20, 205–209.PubMedCrossRefGoogle Scholar
  110. 110.
    Clifton, V. L., Qing, G., Murphy, V. E., Schwartz, J., Madsen, G., and Smith, R. (2000). Placenta 21, 782–788.PubMedCrossRefGoogle Scholar
  111. 111.
    Goland, R. S., Wardlaw, S. L., Stark, R. I., Brown, L. S. Jr., and Frantz, A. G. (1986). J. Clin. Endocrinol. Metab. 63, 1199–1203.PubMedGoogle Scholar
  112. 112.
    Petraglia, F., Giardino, L., Coukos, G., Calza, L., Vale, W., and Genazzani, A. R. (1990). Obstet. Gynecol. 75, 784–790.PubMedGoogle Scholar
  113. 113.
    Florio, P., Cobellis, L., Woodman, J., Severi, F. M., Linton, E. A., and Petraglia, F. (2002). J. Soc. Gynecol. Invest. 9, 233–237.CrossRefGoogle Scholar
  114. 114.
    Petraglia, F., Santuz, M., Florio, P., Simoncini, T., Luisi, S., Plaino, L., Genazzani, A. R., Genazzani, A. D., and Volpe, A. (1998). J. Reprod. Immunol. 39, 221–233.PubMedCrossRefGoogle Scholar
  115. 115.
    Jaffe, R. B. (2001). Front. Horm. Res. 27, 75–85.PubMedGoogle Scholar
  116. 116.
    Korebrits, C., Ramirez, M. M., Watson, L., Brinkman, E., Bocking, A. D., and Challis, J. R. (1998). J. Clin. Endocrinol. Metab. 83, 1585–1591.PubMedCrossRefGoogle Scholar
  117. 117.
    Kurki, T., Laatikainen, T., Lappalainen, K. S., and Ylikorkala, O. (1991). Br. J. Obstet. Gynaecol. 98, 685–691.PubMedGoogle Scholar
  118. 118.
    Lockwood, C. J. (1995). Clin. Obstet. Gynecol. 38, 675–687.PubMedGoogle Scholar
  119. 119.
    Erickson, K., Thorsen, P., Chrousos, G., Grigoriadis, D. E., Khongsaly, O., McGregor, J., and Schulkin, J. (2001). J. Clin. Endocrinol. Metab. 86, 2544–2552.PubMedCrossRefGoogle Scholar
  120. 120.
    Reis, F. M., D’Antona, D., and Petraglia, F. (2002). Endocr. Rev. 23, 230–257.PubMedCrossRefGoogle Scholar
  121. 121.
    Chrousos, G. P. (1998). Endocrinology 139, 437–440.PubMedCrossRefGoogle Scholar
  122. 122.
    Chrousos, G. P. and Gold, P. W. (1992). JAMA 267, 1252.CrossRefGoogle Scholar
  123. 123.
    Hoffman, S. and Hatch, M. (1996). Paediatr. Perinat. Epidemiol. 10, 380–385.PubMedCrossRefGoogle Scholar
  124. 124.
    Hobel, C. J., Dunkel-Schetter, C., Roesch, S. C., Castro, L. C., and Arora, C. P. (1999). Am. J. Obstet. Gynecol. 180, S257-S263.PubMedCrossRefGoogle Scholar
  125. 125.
    Petraglia, F., Hatch, M. C., Lapinski, R., Stomati, M., Reis, F. M., Cobellis, L., and Berkowitz, G. S. (2001). J. Soc. Gynecol. Invest. 8, 83–88.CrossRefGoogle Scholar
  126. 126.
    Nakamura, H., Seto, T., Nagase, H., Yoshida, M., Dan, S., and Ogino, K. (1997). J. Neuroimmunol. 75, 1–8.PubMedCrossRefGoogle Scholar
  127. 127.
    Goldenberg, R. L., Hauth, J. C., and Andrews, W. W. (2000). N. Engl. J. Med. 342, 1500–1507.PubMedCrossRefGoogle Scholar
  128. 128.
    Angioni, S., Petraglia, F., Gallinelli, A., Cossarizza, A., Franceschi, C., Muscettola, M., Genazzani, A. D., Surico, N., and Genazzani, A. R. (1993). Life Sci. 53, 1735–1742.PubMedCrossRefGoogle Scholar
  129. 129.
    Petraglia, F., Garuti, G. C., De Ramundo, B., Angioni, S., Genazzani, A. R., and Bilezikjian, L. M. (1990). Am. J. Obstet. Gynecol. 163, 1307–1312.PubMedGoogle Scholar
  130. 130.
    De Felice, C., Toti, P., Taurini, R. N., Stumpo, M., Picciolini, E., Todros, T., Tanganelli, P., Buonocore, G., and Bracci, R. (2001). J. Pediatr. 138, 101–104.PubMedCrossRefGoogle Scholar
  131. 131.
    Petraglia, F., Aguzzoli, L., Florio, P., Baumann, P., Genazzani, A. D., Di Carlo, C., and Romero, R. (1995). Placenta 16, 157–164.PubMedCrossRefGoogle Scholar
  132. 132.
    Roberts, J. M. and Cooper, D. W. (2001). Lancet 357, 53–56.PubMedCrossRefGoogle Scholar
  133. 133.
    Laatikainen, T., Virtanen, T., Kaaja, R., and Salminen-Lappalainen, K. (1991). Eur. J. Obstet. Gynecol. Reprod. Biol. 39, 19–24.PubMedCrossRefGoogle Scholar
  134. 134.
    Perkins, A. V., Linton, E. A., Eben, F., Simpson, J., Wolfe, C. D., and Redman, C. W. (1995). Br. J. Obstet. Gynaecol. 102, 118–122.PubMedGoogle Scholar
  135. 135.
    Goland, R. S., Tropper, P. J., Warren, W. B., Stark, R. I., Jozak, S. M., and Conwell, I. M. (1995). Reprod. Fertil. Dev. 7, 1227–1230.PubMedCrossRefGoogle Scholar
  136. 136.
    Goland, R. S., Jozak, S., Warren, W. B., Conwell, I. M., Stark, R. I., and Tropper, P. J. (1993). J. Clin. Endocrinol. Metab. 77, 1174–1179.PubMedCrossRefGoogle Scholar
  137. 137.
    Giles, W. B., McLean, M., Davies, J. J., and Smith, R. (1996). Obstet. Gynecol. 87, 107–111.PubMedCrossRefGoogle Scholar
  138. 138.
    Thompson, R. S., Trudinger, B. J., and Cook, C. M. (1988). Br. J. Obstet. Gynaecol. 85, 581–588.Google Scholar
  139. 139.
    Wallace, E. M. and Baker, L. S. (1999). Lancet 353, 1404–1407.PubMedCrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 2002

Authors and Affiliations

  • Pasquale Florio
    • 1
  • Filiberto M. Severi
    • 1
  • Pasquapina Ciarmela
    • 1
  • Giovina Fiore
    • 1
  • Giulia Calonaci
    • 1
  • Angelica Merola
    • 1
  • Claudio De Felice
    • 3
  • Marco Palumbo
    • 2
  • Felice Petraglia
    • 1
  1. 1.Chair of Obstetrics and GynecologyUniversity of SienaSienaItaly
  2. 2.Department of Microbiological and Gynecological ScienceUniversity of CataniaSiena and CataniaItaly
  3. 3.Department of Pediatrics, Obstetrics and Reproductive MedicineUniversity of Siena, Policlinico “Le Scotte”SienaItaly

Personalised recommendations