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Circulating MMP-7 and VEGF as potential predictive biomarkers for recurrent implantation failures

Published online by Cambridge University Press:  19 March 2021

Mustapha Benkhalifa ,
Wiem Zidi ,
Hatem Bahri ,
Sami Mahjoub ,
Khaled Boudhraa ,
Haifa Sanhaji ,
Hafida Khorsi-Cauet ,
Moncef Feki ,
Moncef Benkhalifa Open the ORCID record for Moncef Benkhalifa [Opens in a new window]  and
Monia Allal-Elasmi Open the ORCID record for Monia Allal-Elasmi [Opens in a new window]
Mustapha Benkhalifa
Affiliation:
LR99ES11, Department of Biochemistry, La Rabta Hospital, Faculty of Medicine of Tunis, University of Tunis El Manar, Tunis, Tunisia Faculty of Sciences of Bizerte, University of Carthage, Tunis, Tunisia
Wiem Zidi
Affiliation:
LR99ES11, Department of Biochemistry, La Rabta Hospital, Faculty of Medicine of Tunis, University of Tunis El Manar, Tunis, Tunisia Faculty of Sciences of Bizerte, University of Carthage, Tunis, Tunisia
Hatem Bahri
Affiliation:
Alyssa Fertility Group Center, Alyssa Clinic, Les Berges du Lac, Tunis, Tunisia
Sami Mahjoub
Affiliation:
Alyssa Fertility Group Center, Alyssa Clinic, Les Berges du Lac, Tunis, Tunisia
Khaled Boudhraa
Affiliation:
Alyssa Fertility Group Center, Alyssa Clinic, Les Berges du Lac, Tunis, Tunisia
Haifa Sanhaji
Affiliation:
LR99ES11, Department of Biochemistry, La Rabta Hospital, Faculty of Medicine of Tunis, University of Tunis El Manar, Tunis, Tunisia
Hafida Khorsi-Cauet
Affiliation:
PERITOX-UMR-I 01 CURS, Picardie University Jules Verne, Amiens, France
Moncef Feki
Affiliation:
LR99ES11, Department of Biochemistry, La Rabta Hospital, Faculty of Medicine of Tunis, University of Tunis El Manar, Tunis, Tunisia
Moncef Benkhalifa
Affiliation:
PERITOX-UMR-I 01 CURS, Picardie University Jules Verne, Amiens, France Reproductive Medicine, Reproductive Biology and Genetics, University Hospital and School of Medicine Picardie University Jules Verne, Amiens, France
Monia Allal-Elasmi*
Affiliation:
LR99ES11, Department of Biochemistry, La Rabta Hospital, Faculty of Medicine of Tunis, University of Tunis El Manar, Tunis, Tunisia
*
Author for correspondence: Monia Allal-Elasmi. LR99ES11, Department of Biochemistry, Rabta Hospital, 1007 Jebbari, Tunis, Tunisia. Tel: +216 98425496. Fax: +216 71561912. E-mails: monia.elasmi@fmt.utm.tn; monia_elasmi@yahoo.fr
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Summary

Recurrent implantation failure (RIF) is considered to be one of the major limiting factors of assisted reproductive technology (ART) programme success. The current study focused on the investigation of matrix metalloproteinases (MMPs), tissue inhibitors of MMPs (TIMPs), cytokines and cell adhesion molecules in peripheral blood (PB) and follicular fluid (FF) obtained from 44 women aged between 25 and 39 years old and undergoing intracytoplasmic sperm injection (ICSI). These women were divided into two groups: 22 RIF women with embryo implantation failures after the transfer of at least four fresh or frozen–thawed good quality embryos in a minimum of three ICSI cycles, and 22 ICSI success women (controls) who achieved a clinical pregnancy at their first ICSI attempt. The PB and FF samples were obtained from each patient on the day of oocyte retrieval. MMP-1, -2, -3, -7, -9, TIMP-1, -2, vascular endothelial growth factor (VEGF), leukaemia inhibitory factor (LIF), vascular cell adhesion molecule 1 (VCAM1) and intercellular adhesion molecules 1 (ICAM1) were analyzed using enzyme-linked immunosorbent assay of PB and FF. Our results showed significant decreases in PB MMP-7 and PB VEGF in the RIF group compared with controls [281.11 (33–614) pg/ml vs 119.92 (27–441) pg/ml; P-value = 0.030] and [82.54 (25.94–210.20) pg/ml vs 30.93 (13.62–193.33) pg/ml; P-value = 0.022; respectively]. Receiver operating characteristic (ROC) curve analysis showed informative area under the curve values for PB MMP-7, as well as for PB VEGF, making them able to be proposed as biomarkers of the RIF. Therefore, circulating MMP-7 and VEGF seem to play an interesting role in embryo implantation in in vitro fertilization (IVF)/ICSI cycles and could be proposed as circulating biomarkers of the RIF. These results could be helpful for clinicians and patients to choose the best rescue strategy and treatment to minimize implantation failure in women undergoing IVF/ICSI procedures after the first attempt.

Keywords

Assisted reproductive technologyMatrilysinMatrix metalloproteinasesRecurrent implantation failureVascular endothelial growth factor
Type
Research Article
Information
Zygote , Volume 29 , Issue 5 , October 2021 , pp. 365 - 371
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Aghajanova, L, Houshdaran, S, Balayan, S, Manvelyan, E, Irwin, JC, Huddleston, HG and Giudice, LC (2018). In vitro evidence that platelet-rich plasma stimulates cellular processes involved in endometrial regeneration. J Assist Reprod Genet 35, 757–70.CrossRefGoogle ScholarPubMed
Alhilali, MJS, Parham, A, Attaranzadeh, A, Amirian, M and Azizzadeh, M (2019). IL-5 in follicular fluid as a negative predictor of the intracytoplasmic sperm injection outcome. Cytokine 113, 265–71.CrossRefGoogle ScholarPubMed
Allahveisi, A, Seyedoshohadaei, F, Rezaei, M, Bazrafshan, N and Rahimi, K (2020). The effect of platelet-rich plasma on the achievement of pregnancy during frozen embryo transfer in women with a history of failed implantation. Heliyon 6, e03577.CrossRefGoogle ScholarPubMed
Bansal, R, Ford, B, Bhaskaran, S, Thum, M and Bansal, A (2017). Elevated levels of serum vascular endothelial growth factor-A are not related to NK cell parameters in recurrent IVF failure. J Reprod Infertil 18, 280–7.Google Scholar
Bashiri, A, Halper, KI and Orvieto, R (2018). Recurrent implantation failure-update overview on etiology, diagnosis, treatment and future directions. Reprod Biol Endocrinol 16, 121.CrossRefGoogle ScholarPubMed
Benkhalifa, M, Madkour, A, Louanjli, N, Bouamoud, N, Saadani, B, Kaarouch, I, Chahine, H, Sefrioui, O, Merviel, P and Copin, H (2015). From global proteome profiling to single targeted molecules of follicular fluid and oocyte: contribution to embryo development and IVF outcome. Expert Rev Proteomics 12, 407–23.CrossRefGoogle ScholarPubMed
Benkhalifa, M, Zayani, Y, Bach, V, Copin, H, Feki, M, Benkhalifa, M and Allal-Elasmi, M (2018). Does the dysregulation of matrix metalloproteinases contribute to recurrent implantation failure? Expert Rev Proteomics 15, 311–23.CrossRefGoogle ScholarPubMed
Binder, NK, Evans, J, Gardner, DK, Salamonsen, LA and Hannan, NJ (2014). Endometrial signals improve embryo outcome: functional role of vascular endothelial growth factor isoforms on embryo development and implantation in mice. Hum Reprod 10, 2278–86.CrossRefGoogle Scholar
Bodri, D, Milewski, R, Yao Serna, J, Sugimoto, T, Kato, R, Matsumoto, T and Kawachiya, S (2018). Predicting live birth by combining cleavage and blastocyst-stage time-lapse variables using a hierarchical and a data mining-based statistical model. Reprod Biol 18, 355–60.CrossRefGoogle Scholar
Bou Nemer, L, Shi, H, Carr, BR, Word, RA and Bukulmez, O (2019). Effect of single-dose ibuprofen on follicular fluid levels of interleukins in poor responders undergoing in vitro fertilization. Syst Biol Reprod Med 65, 48–53.CrossRefGoogle ScholarPubMed
Boudjenah, R, Molina-Gomes, D, Wainer, R, de Mazancourt, P, Selva, J and Vialard, F (2012). The vascular endothelial growth factor (VEGF) +405 G/C polymorphism and its relationship with recurrent implantation failure in women in an IVF programme with ICSI. J Assist Reprod Genet 29, 1415–20.CrossRefGoogle Scholar
Boudjenah, R, Molina-Gomes, D, Torre, A, Boitrelle, F, Taieb, S, Dos Santos, E, Wainer, R, de Mazancourt, P, Selva, J and Vialard, F (2014). Associations between individual and combined polymorphisms of the TNF and VEGF genes and the embryo implantation rate in patients undergoing in vitro fertilization (IVF) programs. PLoS One 9, e108287.CrossRefGoogle ScholarPubMed
Boyer, P and Boyer, M (2009). [Non invasive evaluation of the embryo: morphology of preimplantation embryos.] Gynecol Obstet Fertil 37, 908–16. (in French)CrossRefGoogle ScholarPubMed
Bruner, KL, Rodgers, WH, Gold, LI, Korc, M, Hargrove, JT, Matrisian, LM and Osteen, KG (1995). Transforming growth factor beta mediates the progesterone suppression of an epithelial metalloproteinase by adjacent stroma in the human endometrium. Proc Natl Acad Sci USA 92, 7362–66.CrossRefGoogle ScholarPubMed
Coughlan, C, Ledger, W, Wang, Q, Liu, F, Demirol, A, Gurgan, T, Cutting, R, Ong, K, Sallam, H and Li, TC (2014). Recurrent implantation failure: definition and management. Reprod Biomed Online 28, 14–38.CrossRefGoogle ScholarPubMed
European IVF-Monitoring Consortium (EIM); European Society of Human Reproduction and Embryology (ESHRE), Calhaz-Jorge, C, De Geyter, C, Kupka, MS, de Mouzon, J, Erb, K, Mocanu, E, Motrenko, T, Scaravelli, G, Wyns, C and Goossens, V (2017). Assisted reproductive technology in Europe, 2013: results generated from European registers by ESHRE. Hum Reprod 32, 1957–73.Google ScholarPubMed
Gardner, DK and Schoolcraft, WB (1999). Culture and transfer of human blastocysts. Curr Opin Obstet Gynecol 11, 307–11.CrossRefGoogle ScholarPubMed
Kaihola, H, Yaldir, FG, Bohlin, T, Samir, R, Hreinsson, J and Åkerud, H (2019). Levels of caspase-3 and histidine-rich glycoprotein in the embryo secretome as biomarkers of good-quality day-2 embryos and high-quality blastocysts. PLoS One 14, e0226419.CrossRefGoogle ScholarPubMed
Kim, H, Shin, JE, Koo, HS, Kwon, H, Choi, DH and Kim, JH (2019). Effect of autologous platelet-rich plasma treatment on refractory thin endometrium during the frozen embryo transfer cycle: a pilot study. Front Endocrinol (Lausanne) 10, 61.CrossRefGoogle ScholarPubMed
Liang, PY, Diao, LH, Huang, CY, Lian, RC, Chen, X, Li, GG, Zhao, J, Li, YY, He, XB and Zeng, Y (2015). The pro-inflammatory and anti-inflammatory cytokine profile in peripheral blood of women with recurrent implantation failure. Reprod Biomed Online 31, 823–6.CrossRefGoogle ScholarPubMed
Mackens, S, Santos-Ribeiro, S, van de Vijver, A, Racca, A, Van Landuyt, L, Tournaye, H and Blockeel, C (2017). Frozen embryo transfer: a review on the optimal endometrial preparation and timing. Hum Reprod 32, 2234–42.CrossRefGoogle Scholar
Madkour, A, Bouamoud, N, Louanjli, N, Kaarouch, I, Copin, H, Benkhalifa, M and Sefrioui, O (2016). Intrauterine insemination of cultured peripheral blood mononuclear cells prior to embryo transfer improves clinical outcome for patients with repeated implantation failures. Zygote 24, 58–69.CrossRefGoogle ScholarPubMed
Makrigiannakis, A, BenKhalifa, M, Vrekoussis, T, Mahjub, S, Kalantaridou, SN and Gurgan, T (2015). Repeated implantation failure: a new potential treatment option. Eur J Clin Invest 45, 380–84.CrossRefGoogle ScholarPubMed
Marti, HP, Lee, L, Kashgarian, M and Lovett, DH (1994). Transforming growth factor-beta 1 stimulates glomerular mesangial cell synthesis of the 72-kD type IV collagenase. Am J Pathol 144, 82–94.Google ScholarPubMed
Meinel, S, Blohberger, J, Berg, D, Berg, U, Dissen, GA, Ojeda, SR and Mayerhofer, A (2015). Pro-nerve growth factor in the ovary and human granulosa cells. Horm Mol Biol Clin Investig 24, 91–9.Google ScholarPubMed
Nobijari, FF, Arefi, SS, Moini, A, Taheripanah, R, Fazeli, E, Kharazi, H, Hosseini, SZ, Hosseini, A, Valojerdi, MR, Copin, H and Benkhalifa, M (2019). Endometrium immunomodulation by intrauterine insemination administration of treated peripheral blood mononuclear cell prior frozen/thawed embryos in patients with repeated implantation failure. Zygote 27, 214–18.CrossRefGoogle ScholarPubMed
Osteen, KG, Rodgers, WH, Gaire, M, Hargrove, JT, Gorstein, F and Matrisian, LM (1994). Stromal–epithelial interaction mediates steroidal regulation of metalloproteinase expression in human endometrium. Proc Natl Acad Sci USA 91, 10129–33.CrossRefGoogle ScholarPubMed
Osteen, KG, Sierra-Rivera, E, Keller, NR and Fox, DB (1997). Interleukin-1α opposes progesterone-mediated suppression of MMP-7: a possible role of this cytokine during human implantation. Ann NY Acad Sci 828, 137–45.CrossRefGoogle Scholar
Palermo, GD, O’Neill, CL, Chow, S, Cheung, S, Parrella, A, Pereira, N and Rosenwaks, Z (2017). Intracytoplasmic sperm injection: state of the art in humans. Reproduction 154, F93–110.CrossRefGoogle ScholarPubMed
Papanikolaou, E, Chartomatsidou, T, Timotheou, E, Tatsi, P, Katsoula, E, Vlachou, C, Asouchidou, I, Zafeiratis, O and Najdecki, R (2019). In freeze-all strategy, cumulative live birth rate (CLBR) is increasing according to the number of blastocysts formed in women <40 undergoing intracytoplasmic sperm injection (ICSI). Front Endocrinol (Lausanne) 10, 427.CrossRefGoogle Scholar
Rodgers, WH, Osteen, KG, Matrisian, LM, Navre, M, Giudice, LC and Gorstein, F (1993). Expression and localization of matrilysin, a matrix metalloproteinase, in human endometrium during the reproductive cycle. Am J Obstet Gynecol 168, 253–60.CrossRefGoogle ScholarPubMed
Shim, SH, Kim, JO, Jeon, YJ, An, HJ, Lee, HA, Kim, JH, Ahn, EH, Lee, WS and Kim, NK (2018). Association between vascular endothelial growth factor promoter polymorphisms and the risk of recurrent implantation failure. Exp Ther Med 15, 2109–19.Google ScholarPubMed
Sohn, SH, Penzias, AS, Emmi, AM, Dubey, AK, Layman, LC, Reindollar, RH and DeCherney, AH (1999). Administration of progesterone before oocyte retrieval negatively affects the implantation rate. Fertil Steril 71, 11–14.CrossRefGoogle ScholarPubMed
Thompson, JG, Brown, HM and Sutton-McDowall, ML (2016). Measuring embryo metabolism to predict embryo quality. Reprod Fertil Dev 28, 41–50.CrossRefGoogle ScholarPubMed
Vagnini, LD, Nascimento, AM, Canas Mdo, C, Renzi, A, Oliveira-Pelegrin, GR, Petersen, CG, Mauri, AL, Oliveira, JB, Baruffi, RL, Cavagna, M and Franco, JG Jr (2015). The relationship between vascular endothelial growth factor 1154G/A polymorphism and recurrent implantation failure. Med Princ Pract 24, 533–37.CrossRefGoogle ScholarPubMed
Valdes, CT, Schutt, A and Simon, C (2017). Implantation failure of endometrial origin: It is not pathology, but our failure to synchronize the developing embryo with a receptive endometrium. Fertil Steril 108, 15–18.CrossRefGoogle Scholar
Wu, PI, Diaz, R and Borg-Stein, J (2016). Platelet-rich plasma. Phys Med Rehabil Clin 27, 825–53.CrossRefGoogle ScholarPubMed
Yanushpolsky, EH (2015). Luteal phase support in in vitro fertilization. Semin Reprod Med 33, 118–27.Google ScholarPubMed
Yu, N, Yang, J, Guo, Y, Fang, J, Yin, T, Luo, J, Li, X, Li, W, Zhao, Q, Zou, Y and Xu, W (2014). Intrauterine administration of peripheral blood mononuclear cells (PBMCs) improves endometrial receptivity in mice with embryonic implantation dysfunction. Am J Reprod Immunol 71, 24–33.CrossRefGoogle ScholarPubMed