Hypoxia is not required for human endometrial breakdown or repair in a xenograft model of menstruation.

[en] Menstrual endometrial breakdown induced by estradiol and progesterone withdrawal is regularly attributed to vasospasm of spiral arteries causing ischemia and hypoxia. We investigated whether hypoxia actually occurred in an in vivo model of menstruation. Three complementary approaches were used to look for signs of hypoxia in fragments of human functionalis xenografted to ovariectomized immunodeficient mice bearing pellets-releasing estradiol and progesterone, and then deprived of ovarian steroids. Hormone withdrawal 21 d after grafting induced menstrual breakdown and MMP expression within 4 d. Local partial oxygen pressure (pO2) was measured by electron paramagnetic resonance using implanted lithium phtalocyanine crystals. In mice with hormone maintenance until sacrifice, pO2 was low one week after grafting (14.8+/-3.4 mmHg) but increased twofold from the second week when tissue was largely revascularized. After 3 wk, pO2 was not modified by hormone withdrawal but was slightly increased on hormone reimpregnation 4 d after removal (34.7+/-6.1 mmHg) by comparison with hormone maintenance (27.1+/-8.6 mmHg). These results were confirmed using fluorescence quenching-based OxyLite measurements. In a further search for signs of hypoxia, we did not find significant HIF1-alpha immunostaining, nor pimonidazole adducts after hormone withdrawal. We conclude that hypoxia is not needed to trigger menstrual-like tissue breakdown or repair in human endometrial xenograft.-Coudyzer, P., Lemoine, P., Jordan, B. F., Gallez, B., Galant, C., Nisolle, M., Courtoy, P. J., Henriet, P., and Marbaix, E. Hypoxia is not required for human endometrial breakdown or repair in a xenograft model of menstruation.

Disciplines :

Reproductive medicine (gynecology, andrology, obstetrics)

Author, co-author :

Coudyzer, Pauline

Lemoine, Pascale

Jordan, Benedicte F.

Gallez, Bernard

Galant, Christine

Nisolle, Michelle ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique

Courtoy, Pierre J.

Henriet, Patrick

Marbaix, Etienne

Language :

English

Title :

Hypoxia is not required for human endometrial breakdown or repair in a xenograft model of menstruation.

Publication date :

2013

Journal title :

FASEB Journal

ISSN :

0892-6638

eISSN :

1530-6860

Publisher :

Federation of American Societies for Experimental Biology, United States - Maryland

Volume :

sous presse

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 17 June 2013

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Bibliography

Gaide Chevronnay, H. P., Selvais, C., Emonard, H., Galant, C., Marbaix, E., and Henriet, P. (2012) Regulation of matrix metalloproteinases activity studied in human endometrium as a paradigm of cyclic tissue breakdown and regeneration. Biochim. Biophys. Acta 1824, 146-156
Henriet, P., Gaide Chevronnay, H. P., and Marbaix, E. (2012) The endocrine and paracrine control of menstruation. Mol. Cell. Endocrinol. 358, 197-207
Jabbour, H. N., Kelly, R. W., Fraser, H. M., and Critchley, H. O. (2006) Endocrine regulation of menstruation. Endocrine Rev. 27, 17-46
Maybin, J. A., Hirani, N., Jabbour, H. N., and Critchley, H. O. (2011) Novel roles for hypoxia and prostaglandin E2 in the regulation of IL-8 during endometrial repair. Am. J. Pathol. 178, 1245-1256
Pretto, C. M., Gaide Chevronnay, H. P., Cornet, P. B., Galant, C., Delvaux, D., Courtoy, P. J., Marbaix, E., and Henriet, P. (2008) Production of interleukin-1alpha by human endometrial stromal cells is triggered during menses and dysfunctional bleeding and is induced in culture by epithelial interleukin-1alpha released upon ovarian steroids withdrawal. J. Clin. Endocrinol. Metab. 93, 4126-4134
Gaide Chevronnay, H. P., Cornet, P. B., Delvaux, D., Lemoine, P., Courtoy, P. J., Henriet, P., and Marbaix, E. (2008) Opposite regulation of transforming growth factors-β2 and -β3 expression in the human endometrium. Endocrinology 149, 1015-1025
Fan, X., Krieg, S., Kuo, C. J., Wiegand, S. J., Rabinovitch, M., Druzin, M. L., Brenner, R. M., Giudice, L. C., and Nayak, N. R. (2008) VEGF blockade inhibits angiogenesis and reepithelialization of endometrium. FASEB J 22, 3571-3580
Markee, J. E. (1978) Menstruation in intraocular endometrial transplants in the Rhesus monkey. Am. J. Obstet. Gynecol. 131, 558-559
Critchley, H. O., Jones, R. L., Lea, R. G., Drudy, T. A., Kelly, R. W., Williams, A. R., and Baird, D. T. (1999) Role of inflammatory mediators in human endometrium during progesterone withdrawal and early pregnancy. J. Clin. Endocrinol. Metab. 84, 240-248
Gannon, B. J., Carati, C. J., and Verco, C. J. (1997) Endometrial perfusion across the normal human menstrual cycle assessed by laser Doppler fluxmetry. Human Reprod. 12, 132-139
Zhang, J., and Salamonsen, L. A. (2002) Expression of hypoxiainducible factors in human endometrium and suppression of matrix metalloproteinases under hypoxic conditions do not support a major role for hypoxia in regulating tissue breakdown at menstruation. Human Reprod. 17, 265-274
Gaide Chevronnay, H. P., Lemoine, P., Courtoy, P. J., Marbaix, E., and Henriet, P. (2010) Ovarian steroids, mitogen-activated protein kinases, and/or aspartic proteinases cooperate to control endometrial remodeling by regulating gene expression in the stroma and glands. Endocrinology 151, 4515-4526
Maybin, J. A., Hirani, N., Brown, P., Jabbour, H. N., and Critchley, H. O. (2011) The regulation of vascular endothelial growth factor by hypoxia and prostaglandin F(2)alpha during human endometrial repair. J. Clin. Endocrinol. Metab. 96, 2475- 2483
Gaide Chevronnay, H. P., Galant, C., Lemoine, P., Courtoy, P. J., Marbaix, E., and Henriet, P. (2009) Spatiotemporal coupling of focal extracellular matrix degradation and reconstruction in the menstrual human endometrium. Endocrinology 150, 5094-5105
Garry, R., Hart, R., Karthigasu, K. A., and Burke, C. (2010) Structural changes in endometrial basal glands during menstruation. BJOG 117, 1175-1185
Alvarez Gonzalez, M. L., Frankenne, F., Galant, C., Marbaix, E., Foidart, J. M., Nisolle, M., and Beliard, A. (2009) Mixed origin of neovascularization of human endometrial grafts in immunodeficient mouse models. Human Reprod. 24, 2217-2224
Bergqvist, A., Jeppsson, S., Kullander, S., and Ljungberg, O. (1985) Human uterine endometrium and endometriotic tissue transplanted into nude mice. Morphologic effects of various steroid hormones. Am. J. Pathol. 121, 337-341
Cornet, P. B., Galant, C., Eeckhout, Y., Courtoy, P. J., Marbaix, E., and Henriet, P. (2005) Regulation of matrix metalloproteinase- 9/gelatinase B expression and activation by ovarian steroids and LEFTY-A/endometrial bleeding-associated factor in the human endometrium. J. Clin. Endocrinol. Metab. 90, 1001- 1011
Gallez, B., Baudelet, C., and Jordan, B. F. (2004) Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications. NMR Biomed. 17, 240-262
Vassilev, V., Pretto, C. M., Cornet, P. B., Delvaux, D., Eeckhout, Y., Courtoy, P. J., Marbaix, E., and Henriet, P. (2005) Response of matrix metalloproteinases and tissue inhibitors of metalloproteinases messenger ribonucleic acids to ovarian steroids in human endometrial explants mimics their gene- and phasespecific differential control in vivo. J. Clin. Endocrinol. Metab. 90, 5848-5857
Semenza, G. L. (2000) HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88, 1474-1480
Ljungkvist, A. S., Bussink, J., Rijken, P. F., Raleigh, J. A., Denekamp, J., and Van Der Kogel, A. J. (2000) Changes in tumor hypoxia measured with a double hypoxic marker technique. Intl. J. Radiation Oncol. Biol. Physics 48, 1529-1538
Shweiki, D., Itin, A., Soffer, D., and Keshet, E. (1992) Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359, 843-845
Battersby, S., Critchley, H. O., de Brum-Fernandes, A. J., and Jabbour, H. N. (2004) Temporal expression and signalling of prostacyclin receptor in the human endometrium across the menstrual cycle. Reproduction 127, 79-86
Nap, A. W., Griffioen, A. W., Dunselman, G. A., Bouma-Ter Steege, J. C., Thijssen, V. L., Evers, J. L., and Groothuis, P. G. (2004) Antiangiogenesis therapy for endometriosis. J. Clin. Endocrinol. Metab. 89, 1089-1095
Eggermont, J., Donnez, J., Casanas-Roux, F., Scholtes, H., and Van Langendonckt, A. (2005) Time course of pelvic endometriotic lesion revascularization in a nude mouse model. Fertil. Steril. 84, 492-499
Fraser, I. S., and Hickey, M. (2000) Endometrial vascular changes and bleeding disturbances with long-acting progestins. Steroids 65, 665-670
Brosens, I. A. (1997) Endometriosis - A disease because it is characterized by bleeding. Am. J. Obstet. Gynecol. 176, 263-267
Matsuura-Sawada, R., Murakami, T., Ozawa, Y., Nabeshima, H., Akahira, J., Sato, Y., Koyanagi, Y., Ito, M., Terada, Y., and Okamura, K. (2005) Reproduction of menstrual changes in transplanted human endometrial tissue in immunodeficient mice. Human Reprod. 20, 1477-1484
Masuda, H., Maruyama, T., Hiratsu, E., Yamane, J., Iwanami, A., Nagashima, T., Ono, M., Miyoshi, H., Okano, H. J., Ito, M., Tamaoki, N., Nomura, T., Okano, H., Matsuzaki, Y., and Yoshimura, Y. (2007) Noninvasive and real-time assessment of reconstructed functional human endometrium in NOD/SCID/ gamma c(null) immunodeficient mice. Proc. Natl. Acad. Sci. U. S. A. 104, 1925-1930
Punyadeera, C., Thijssen, V. L., Tchaikovski, S., Kamps, R., Delvoux, B., Dunselman, G. A., de Goeij, A. F., Griffioen, A. W., and Groothuis, P. G. (2006) Expression and regulation of vascular endothelial growth factor ligands and receptors during menstruation and post-menstrual repair of human endometrium. Mol. Human Reprod. 12, 367-375
Critchley, H. O., Osei, J., Henderson, T. A., Boswell, L., Sales, K. J., Jabbour, H. N., and Hirani, N. (2006) Hypoxia-inducible factor-1alpha expression in human endometrium and its regulation by prostaglandin E-series prostanoid receptor 2 (EP2). Endocrinology 147, 744-753
Charnock-Jones, D. S., Sharkey, A. M., Rajput-Williams, J., Burch, D., Schofield, J. P., Fountain, S. A., Boocock, C. A., and Smith, S. K. (1993) Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol. Reprod. 48, 1120-1128
Graubert, M. D., Ortega, M. A., Kessel, B., Mortola, J. F., and Iruela-Arispe, M. L. (2001) Vascular repair after menstruation involves regulation of vascular endothelial growth factor-receptor phosphorylation by sFLT-1. Am. J. Pathol. 158, 1399-1410
Popovici, R. M., Irwin, J. C., Giaccia, A. J., and Giudice, L. C. (1999) Hypoxia and cAMP stimulate vascular endothelial growth factor (VEGF) in human endometrial stromal cells: potential relevance to menstruation and endometrial regeneration. J. Clin. Endocrinol. Metab. 84, 2245-2248
Sharkey, A. M., Day, K., McPherson, A., Malik, S., Licence, D., Smith, S. K., and Charnock-Jones, D. S. (2000) Vascular endothelial growth factor expression in human endometrium is regulated by hypoxia. J. Clin. Endocrinol. Metab. 85, 402-409
Smith, S. K. (2001) Regulation of angiogenesis in the endometrium. Trends Endocrinol. Metab. 12, 147-151
Du, H., Naqvi, H., and Taylor, H. S. (2012) Ischemia/reperfusion injury promotes and granulocyte-colony stimulating factor inhibits migration of bone marrow-derived stem cells to endometrium. Stem Cells Dev. 21, 3324-3331