Altered Gene Expression of Caspase-10, Death Receptor-3 and IGFBP-3 in Preeclamptic Placentas

  • Han, Jae Yoon (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Kim, Yoon Sook (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Cho, Gyeong Jae (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Roh, Gu Seob (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Kim, Hyun Joon (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Choi, Won Jun (Department of Obstetrics and Gynecology, School of Medicine, Gyeongsang National University) ;
  • Paik, Won Young (Department of Obstetrics and Gynecology, School of Medicine, Gyeongsang National University) ;
  • Rho, Gyu Jin (Department of Obstetrics and Theriogenology, College of Veterinary Medicine, Gyeongsang National University) ;
  • Kang, Sang Soo (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University) ;
  • Choi, Wan Sung (Department of Anatomy and Neurobiology, Institute of Health Science, Gyeongsang National University)
  • Received : 2006.04.27
  • Accepted : 2006.07.14
  • Published : 2006.10.31

Abstract

Enhanced apoptosis has been observed in the placentas of women with preeclampsia, but few studies have examined changes at the molecular level. This study was designed to detect genes specifically expressed in full-term preeclamptic placentas. Tissue samples were collected immediately after cesarean delivery from 11 normal and 8 preeclamptic placentas at 35-40 weeks of gestation. Total RNAs were extracted and hybridized to a cDNA microarray. Results were confirmed by reverse-transcription polymerase chain reaction (RT-PCR), Western blotting and immunohistochemistry. Hematoxylin and eosin and TUNEL staining were also performed to confirm apoptosis in preeclamptic placentas. Among 205 genes, three were up- or downregulated in preeclamptic placentas. The expression of caspase-10 and death receptor 3 (DR-3) was significantly increased, whereas insulin-like growth factor binding protein-3 (IGFBP-3) was strongly downregulated. RT-PCR analysis and Western blotting confirmed these effects. Immunohistochemical analysis showed that the DR-3, caspase-10 and IGFBP-3 proteins were localized in the syncytial membrane. Apoptosis in the trophoblast was also increased in term placentas from women with pregnancies complicated by preeclampsia. These results suggest that caspase-10, DR-3 and IGFBP-3 are involved in apoptosis in the preeclamptic placenta.

Keywords

Acknowledgement

Supported by : Korea Science and Engineering Foundation, Rural Development Administration

References

  1. Allaire, A. D., Ballenger, K. A., Wells, S. R., McMahon, M. J., and Lessey, B. A. (2000) Placental apoptosis in preeclampsia. Obstet. Gynecol. 96, 271−276
  2. Ashkenazi, A. and Dixit, V. M. (1999) Apoptosis control by death and decoy receptors. Curr. Opin. Cell Biol. 11, 255− 260 https://doi.org/10.1016/S0955-0674(99)80034-9
  3. Chee, M., Yang, R., Hubbell, E., Berno, A., Huang, X. C., et al. (1996) Accessing genetic information with high-density DNA arrays. Science 274, 610−614 https://doi.org/10.1126/science.274.5287.610
  4. Chinnaiyan, A. M., O'Rourke, K., Tewari, M., and Dixit, V. M. (1995) FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81, 505−512 https://doi.org/10.1016/0092-8674(95)90071-3
  5. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenolchloroform extraction. Anal. Biochem. 162, 156−159
  6. Clemmons, D. R. (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev. 8, 45−62 https://doi.org/10.1016/S1359-6101(96)00053-6
  7. Correia-da-Silva, G., Bell, S. C., Pringle, J. H., and Teixeira, N. (1999) Expression of mRNA encoding insulin-like growth factors I and II by uterine tissues and placenta during pregnancy in the rat. Mol. Reprod. Dev. 53, 294−305 https://doi.org/10.1002/(SICI)1098-2795(199907)53:3<294::AID-MRD5>3.0.CO;2-0
  8. Dupont, J., Fernandez, A. M., Glackin, C. A., Helman, L., and LeRoith, D. (2001) Insulin-like growth factor 1 (IGF-1)- induced twist expression is involved in the anti-apoptotic effects of the IGF-1 receptor. J. Biol. Chem. 276, 26699−26707 https://doi.org/10.1074/jbc.M102664200
  9. Granger, J. P., Alexander, B. T., Bennett, W. A., and Khalil, R. A. (2001) Pathophysiology of pregnancy-induced hypertension. Am. J. Hypertens. 14, 178−185
  10. Hossenlopp, P., Segovia, B., Lassarre, C., Roghani, M., Bredon, M., et al. (1990) Evidence of enzymatic degradation of insulin- like growth factor-binding proteins in the 150K complex during pregnancy. J. Clin. Endocrinol. Metab. 71, 797−805 https://doi.org/10.1210/jcem-71-4-797
  11. Hu, R., Zhou, S., and Li, X. (2006) Altered Bcl-2 and Bax expression is associated with cultured first trimester human cytotrophoblasts apoptosis induced by hypoxia. Life Sci. 79, 351−355 https://doi.org/10.1016/j.lfs.2006.01.011
  12. Hung, T. H., Charnock-Jones, D. S., Skepper, J. N., and Burton, G. J. (2004) Secretion of tumor necrosis factor-alpha from human placental tissues induced by hypoxia-reoxygenation causes endothelial cell activation in vitro: a potential mediator of the inflammatory response in preeclampsia. Am. J. Pathol. 164, 1049−1061 https://doi.org/10.1016/S0002-9440(10)63192-6
  13. Huppertz, B., Kadyrov, M., and Kingdom, J. C. (2006) Apoptosis and its role in the trophoblast. Am. J. Obstet. Gynecol. 195, 29−39 https://doi.org/10.1016/j.ajog.2005.07.039
  14. Ishihara, N., Matsuo, H., Murakoshi, H., Laoag-Fernandez, J. B., Samoto, T., et al. (2002) Increased apoptosis in the syncytiotrophoblast in human term placentas complicated by either preeclampsia or intrauterine growth retardation. Am. J. Obstet. Gynecol. 186, 158−166 https://doi.org/10.1067/mob.2002.119176
  15. Jin, Y., Norquay, L. D., Yang, X., Gregoire, S., and Cattini, P. A. (2004) Binding of AP-2 and ETS-domain family members is associated with enhancer activity in the hypersensitive site III region of the human growth hormone/chorionic somatomammotropin locus. Mol. Endocrinol. 18, 574−587
  16. Kadyrov, M., Kingdom, J. C., and Huppertz. B. (2006) Divergent trophoblast invasion and apoptosis in placental bed spiral arteries from pregnancies complicated by maternal anemia and early-onset preeclampsia/intrauterine growth restriction. Am. J. Obstet. Gynecol. 194, 557−563 https://doi.org/10.1016/j.ajog.2005.07.035
  17. Kaufmann, P. and Stegner, H. E. (1972) Functional differentiation of the human placental syncytiotrophoblast. Z. Zellforsch. Mikrosk. Anat. 135, 361−382
  18. Kim, Y. and Seol, D. W. (2003) TRAIL, a mighty apoptosis inducer. Mol. Cells 15, 283−293
  19. Kischkel, F. C., Lawrence, D. A., Tinel, A., LeBlanc, H., Virmani, A., et al. (2001) Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J. Biol. Chem. 276, 46639−46646 https://doi.org/10.1074/jbc.M105102200
  20. Leung, D. N., Smith, S. C., To, K. F., Sahota, D. S., and Baker, P. N. (2001) Increased placental apoptosis in pregnancies complicated by preeclampsia. Am. J. Obstet. Gynecol. 184, 1249−1250
  21. Levy, R., Smith, S. D., Chandler, K., Sadovsky, Y., and Nelson, D. M. (2000) Apoptosis in human cultured trophoblasts is enhanced by hypoxia and diminished by epidermal growth factor. Am. J. Physiol. Cell Physiol. 278, C982−988
  22. Lipton, S. A. (1997) Janus faces of NF-kappa B: neurodestruction versus neuroprotection. Nat. Med. 3, 20−22 https://doi.org/10.1038/nm0197-20
  23. Manousos, O., Souglakos, J., Bosetti, C., Tzonou, A., Chatzidakis, V., et al. (1999) IGF-I and IGF-II in relation to colorectal cancer. Int. J. Cancer 83, 15−17 https://doi.org/10.1002/(SICI)1097-0215(19990924)83:1<15::AID-IJC4>3.0.CO;2-Y
  24. Marsters, S. A., Sheridan, J. P., Pitti, R. M., Brush, J., Goddard, A., et al. (1998) Identification of a ligand for the deathdomain- containing receptor Apo3. Curr. Biol. 8, 525−528 https://doi.org/10.1016/S0960-9822(98)70204-0
  25. Martin, D. C., Fowlkes, J. L., Babic, B., and Khokha, R. (1999) Insulin-like growth factor II signaling in neoplastic proliferation is blocked by transgenic expression of the metalloproteinase inhibitor TIMP-7. J. Cell Biol. 146, 881−892 https://doi.org/10.1083/jcb.146.4.881
  26. Michell, N. P., Langman, M. J., and Eggo, M. C. (1997) Insulinlike growth factors and their binding proteins in human colonocytes: preferential degradation of insulin-like growth factor binding protein 2 in colonic cancers. Br. J. Cancer 76, 60–66
  27. National Heart, Lung, and Blood Institute National High Blood Pressure Education Program. (2000) Report of the National High Blood Pressure Education Program Working Group on High Blood Pressure in Pregnancy. Am. J. Obstet. Gynecol. 183, S1−S22 https://doi.org/10.1067/mob.2000.107928
  28. Parrizas, M., Saltiel, A. R., and LeRoith, D. (1997) Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinositol 3′-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272, 154−161 https://doi.org/10.1074/jbc.272.1.154
  29. Peruzzi, F., Prisco, M., Morrione, A., Valentinis, B., and Baserga, R. (2001) Anti-apoptotic signaling of the insulin-like growth factor-I receptor through mitochondrial translocation of c- Raf and Nedd4. J. Biol. Chem. 276, 25990−25996 https://doi.org/10.1074/jbc.M103188200
  30. Ramaswamy, M., Efimova, E. V., Martinez, O., Mulherkar, N. U., Singh, S. P., et al. (2004) IG20 (MADD splice variant-5), a proapoptotic protein, interacts with DR4/DR5 and enhances TRAIL-induced apoptosis by increasing recruitment of FADD and caspase-8 to the DISC. Oncogene 23, 6083−6094 https://doi.org/10.1038/sj.onc.1207804
  31. Ravelich, S. R., Breier, B. H., Reddy, S., Keelan, J. A., Wells, D. N., et al. (2004) Insulin-like growth factor-I and binding proteins 1, 2, and 3 in bovine nuclear transfer pregnancies. Biol. Reprod. 70, 430−438 https://doi.org/10.1095/biolreprod.103.021139
  32. Sprick, M. R., Rieser, E., Stahl, H., Grosse-Wilde, A., Weigand, M. A., et al. (2002) Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signalling complexes in a FADD-dependent manner but can not functionally substitute caspase-8. EMBO J. 21, 4520−4530 https://doi.org/10.1093/emboj/cdf441
  33. Srivastava, R. K., Gu, Y., Ayloo, S., Zilberstein, M., and Gibori, G. (1998) 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. 21, 355−362
  34. Tartaglia, L. A. and Goeddel, D. V. (1992) Two TNF receptors. Immunol. Today 13, 151−153
  35. Umezawa, K. and Chaicharoenpong, C. (2002) Molecular design and biological activities of NF-kappaB inhibitors. Mol. Cells 14, 163−167
  36. Weber, C. H. and Vincenz, C. (2001) A docking model of key components of the DISC complex: death domain superfamily interactions redefined. FEBS Lett. 492, 171−176