Knockdown of pleiotrophin increases the risk of preeclampsia following vitrified-thawed embryo transfer

Liu,Shengxian; Wang,Fang; Liu,Gelin

doi:10.3892/ijo.2018.4540

Knockdown of pleiotrophin increases the risk of preeclampsia following vitrified-thawed embryo transfer

Authors:
- Shengxian Liu
- Fang Wang
- Gelin Liu
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Affiliations: Reproductive Medicine Center, Luoyang Central Hospital Affiliated to Zhengzhou University, Luoyang, Henan 471000, P.R. China
Published online on: August 28, 2018 https://doi.org/10.3892/ijo.2018.4540
Pages: 1847-1856
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Preeclampsia (PE) in pregnancy is associated with vitrified-thawed embryo transfer. Pleiotrophin (PTN) is important in inflammation via its receptors. The aim of the present study was to determine the effect of PTN on the risk of PE following embryo transfer. An enzyme-linked immunosorbent assay was performed to determine the levels of tumor necrosis factor (TNF)-α and PTN in serum. The knockdown of PTN was conditionally induced by tamoxifen (tax) treatment. The tail-cuff method and Bradford assay were used to monitor blood pressure and the level of urine protein, respectively. The expression patterns of PTN, receptor protein tyrosine phosphatase β/ζ, (RPTPβ/ζ), syndecan-1 (SDC1), syndecan-3 (SDC3) and anaplastic lymphoma kinase (ALK) were determined by immunohistochemistry (IHC). Western blot analysis was performed to evaluate the expression level of PTN and its receptors. The risk of PE was elevated following embryo transfer in clinical and in the tax/PTN-/- group. It was found that the level of PTN increased when pregnancy progressed in normal conditions, however, the level of PTN was reduced in the PE mice. In addition, increases in TNF-α, blood pressure and urine protein were more marked in the PE mice that lacked PTN, compared with those in other PE mice. In addition, overlapping expression of PTN and its receptors in villous mesenchyme and fetal macrophages were identified using an IHC assay. However, the positive staining of PTN and its receptors was weaker or even absent in the PE mice. The protein level of RPTPβ/ζ was lower in the PE mice that lacked PTN than that in the other PE mice. The knockdown of PTN increased the risk of PE following vitrified-thawed embryo transfer, in which its receptors, particularly RPTPβ/ζ, may be involved.

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1	Sharma A, Singh AK and Singh SK: Increasing prevalence of male infertility and stress factors: An overview. Int J Clin Cases Invest. 3:17–24. 2011.
2	Araoye MO: Epidemiology of infertility: Social problems of the infertile couples. West Afr J Med. 22:190–196. 2003.PubMed/NCBI
3	Kol S: Assisted Reproductive Technology (ART). Encyclopedia of Endocrine Diseases. Academic Press; New York, NY: pp. 269–277. 2004, View Article : Google Scholar
4	Sunderam S, Kissin DM, Crawford SB, Folger SG, Jamieson DJ, Warner L and Barfield WD: Assisted Reproductive Technology Surveillance - United States, 2013. MMWR Surveill Summ. 64:1–25. 2015. View Article : Google Scholar : PubMed/NCBI
5	Saragusty J: Arav A Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction. 141:1–19. 2011. View Article : Google Scholar
6	Veeck LL: Does the developmental stage at freeze impact on clinical results post-thaw? Reprod Biomed Online. 6:367–374. 2003. View Article : Google Scholar : PubMed/NCBI
7	Anderson AR, Wilkinson SS, Price S and Crain JL: Reduction of high order multiples in frozen embryo transfers. Reprod Biomed Online. 10:402–405. 2005. View Article : Google Scholar : PubMed/NCBI
8	Desai N, Blackmon H, Szeptycki J and Goldfarb J: Cryoloop vitrification of human day 3 cleavage-stage embryos: Post- vitrification development, pregnancy outcomes and live births. Reprod Biomed Online. 14:208–213. 2007. View Article : Google Scholar : PubMed/NCBI
9	Vajta G and Nagy ZP: Are programmable freezers still needed in the embryo laboratory? Review on vitrification. Reprod Biomed Online. 12:779–796. 2006. View Article : Google Scholar : PubMed/NCBI
10	Kuleshova LL and Lopata A: Vitrification can be more favorable than slow cooling. Fertil Steril. 78:449–454. 2002. View Article : Google Scholar : PubMed/NCBI
11	Liebermann J and Tucker MJ: Effect of carrier system on the yield of human oocytes and embryos as assessed by survival and developmental potential after vitrification. Reproduction. 124:483–489. 2002. View Article : Google Scholar : PubMed/NCBI
12	Vajta G and Kuwayama M: Improving cryopreservation systems. Theriogenology. 65:236–244. 2006. View Article : Google Scholar
13	Doody KJ: Cryopreservation and delayed embryo transfer-assisted reproductive technology registry and reporting implications. Fertil Steril. 102:27–31. 2014. View Article : Google Scholar : PubMed/NCBI
14	Pastore LM and Williams CD: Perinatal outcomes in singletons following in vitro fertilization: A meta-analysis. Obstet Gynecol. 104:4122004. View Article : Google Scholar
15	Opdahl S, Henningsen AA, Tiitinen A, Bergh C, Pinborg A, Romundstad PR, Wennerholm UB, Gissler M, Skjærven R and Romundstad LB: Risk of hypertensive disorders in pregnancies following assisted reproductive technology: A cohort study from the CoNARTaS group. Hum Reprod. 30:1724–1731. 2015. View Article : Google Scholar : PubMed/NCBI
16	Roberts JM: Preeclampsia: New approaches but the same old problems. Am J Obstet Gynecol. 199:443–444. 2008. View Article : Google Scholar : PubMed/NCBI
17	Roberts JM, Pearson GD, Cutler JA, Lindheimer MD and National Heart Lung; Blood Institute: Summary of the NHLBI Working Group on Research on Hypertension During Pregnancy. Hypertens Pregnancy. 22:109–127. 2003. View Article : Google Scholar : PubMed/NCBI
18	Myklestad K, Vatten LJ, Salvesen KA, Davey Smith G and Romundstad PR: Hypertensive disorders in pregnancy and paternal cardiovascular risk: A population-based study. Ann Epidemiol. 21:407–412. 2011. View Article : Google Scholar : PubMed/NCBI
19	Redman CW and Sargent IL: Latest advances in understanding preeclampsia. Science. 308:1592–1594. 2005. View Article : Google Scholar : PubMed/NCBI
20	Sircar M, Thadhani R and Karumanchi SA: Pathogenesis of preeclampsia. Curr Opin Nephrol Hypertens. 24:131–138. 2015. View Article : Google Scholar : PubMed/NCBI
21	Zhang Y, Hua Z, Zhang K, Meng K and Hu Y: Therapeutic effects of anticoagulant agents on preeclampsia in a murine model induced by phosphatidylserine/phosphatidylcholine microvesicles. Placenta. 30:1065–1070. 2009. View Article : Google Scholar : PubMed/NCBI
22	American College of Obstetricians and Gynecologists; Task Force on Hypertension in Pregnancy: Hypertension in pregnancy. Report of the American College of Obstetricians and Gynecologists’ Task Force on Hypertension in Pregnancy. Obstet Gynecol. 122:1122–1131. 2013.
23	Redman CW and Sargent IL: Placental stress and pre-eclampsia: a revised view. Placenta. 30(Suppl A): pp. S38–S42. 2009, View Article : Google Scholar : PubMed/NCBI
24	Mohaupt M: Molecular aspects of preeclampsia. Mol Aspects Med. 28:169–191. 2007. View Article : Google Scholar : PubMed/NCBI
25	Das UN: Cytokines, angiogenic, and antiangiogenic factors and bioactive lipids in preeclampsia. Nutrition. 31:1083–1095. 2015. View Article : Google Scholar : PubMed/NCBI
26	Ball M, Carmody M, Wynne F, Dockery P, Aigner A, Cameron I, Higgins J, Smith SD, Aplin JD and Moore T: Expression of pleiotrophin and its receptors in human placenta suggests roles in trophoblast life cycle and angiogenesis. Placenta. 30:649–653. 2009. View Article : Google Scholar : PubMed/NCBI
27	Achour A, M’bika JP, Baudouin F, Caruelle D and Courty J: Pleiotrophin induces expression of inflammatory cytokines in peripheral blood mononuclear cells. Biochimie. 90:1791–1795. 2008. View Article : Google Scholar : PubMed/NCBI
28	Amet LE, Lauri SE, Hienola A, Croll SD, Lu Y, Levorse JM, Prabhakaran B, Taira T, Rauvala H and Vogt TF: Enhanced hippocampal long-term potentiation in mice lacking heparin- binding growth-associated molecule. Mol Cell Neurosci. 17:1014–1024. 2001. View Article : Google Scholar : PubMed/NCBI
29	del Olmo N, Gramage E, Alguacil LF, Pérez-Pinera P, Deuel TF and Herradón G: Pleiotrophin inhibits hippocampal long-term potentiation: A role of pleiotrophin in learning and memory. Growth Factors. 27:189–194. 2009. View Article : Google Scholar : PubMed/NCBI
30	Gramage E, Herradón G, Martín YB, Vicente-Rodríguez M, Rojo L, Gnekow H, Barbero A and Pérez-García C: Differential phosphoproteome of the striatum from pleiotrophin knockout and midkine knockout mice treated with amphetamine: Correlations with amphetamine-induced neurotoxicity. Toxicology. 306:147–156. 2013. View Article : Google Scholar : PubMed/NCBI
31	Hayashi S and McMahon AP: Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: A tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol. 244:305–318. 2002. View Article : Google Scholar : PubMed/NCBI
32	Aigner A, Brachmann P, Beyer J, Jäger R, Raulais D, Vigny M, Neubauer A, Heidenreich A, Weinknecht S, Czubayko F, et al: Marked increase of the growth factors pleiotrophin and fibroblast growth factor-2 in serum of testicular cancer patients. Ann Oncol. 14:1525–1529. 2003. View Article : Google Scholar : PubMed/NCBI
33	Krege JH, Hodgin JB, Hagaman JR and Smithies O: A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension. 25:1111–1115. 1995. View Article : Google Scholar : PubMed/NCBI
34	Monahan E and Yamazaki K: An improved urine collection technique for laboratory mice: The bladder massage method. Lab Animal. 22:38–39. 1993.
35	Martin AS, Monsour M, Kawwass JF, Boulet SL, Kissin DM and Jamieson DJ: Risk of preeclampsia in pregnancies after assisted reproductive technology and ovarian stimulation. Matern Child Health J. 20:pp. 2050–2056. 2016, View Article : Google Scholar : PubMed/NCBI
36	Kadomatsu K: The midkine family in cancer, inflammation and neural development. Nagoya J Med Sci. 67:71–82. 2005.
37	Wester-Rosenlöf L, Casslé V, Axelsson J, Edström-Hägerwall A, Gram M, Holmqvist M, Johansson ME, Larsson I, Ley D, Marsal K, et al: A1M/α1-microglobulin protects from heme- induced placental and renal damage in a pregnant sheep model of preeclampsia. PLoS One. 9:pp. e863532014, View Article : Google Scholar
38	Wang YA, Chughtai AA, Farquhar CM, Pollock W, Lui K and Sullivan EA: Increased incidence of gestational hypertension and preeclampsia after assisted reproductive technology treatment. Fertil Steril. 105:920–926.e2. 2016. View Article : Google Scholar
39	Högberg U: The World Health Report 2005: ‘Make every mother and child count’ - including Africans. Scand J Public Health. 33:409–411. 2005. View Article : Google Scholar
40	Al-Jameil N, Aziz Khan F, Fareed Khan M and Tabassum H: A brief overview of preeclampsia. J Clin Med Res. 6:1–7. 2014.PubMed/NCBI
41	Shaw J, Tang Z, Schneider H, Saljé K, Hansson SR and Guller S: Inflammatory processes are specifically enhanced in endothelial cells by placental-derived TNF-α: Implications in preeclampsia (PE). Placenta. 43:1–8. 2016. View Article : Google Scholar : PubMed/NCBI
42	Xu C, Zhu S, Wu M, Han W and Yu Y: Functional receptors and intracellular signal pathways of midkine (MK) and pleiotrophin (PTN). Biol Pharm Bull. 37:511–520. 2014. View Article : Google Scholar
43	Gandley RE, Althouse A, Jeyabalan A, Bregand-White JM, McGonigal S, Myerski AC, Gallaher M, Powers RW and Hubel CA: Low soluble syndecan-1 precedes preeclampsia. PLoS One. 11:pp. e01576082016, View Article : Google Scholar : PubMed/NCBI
44	Palmieri D, Mura M, Mambrini S and Palombo D: Effects of Pleiotrophin on endothelial and inflammatory cells: Pro-angiogenic and anti-inflammatory properties and potential role for vascular bio-prosthesis endothelialization. Adv Med Sci. 60:287–293. 2015. View Article : Google Scholar : PubMed/NCBI
45	Anjum N, Baker PN, Robinson NJ and Aplin JD: Maternal celiac disease autoantibodies bind directly to syncytiotrophoblast and inhibit placental tissue transglutaminase activity. Reprod Biol Endocrinol. 7:162009. View Article : Google Scholar : PubMed/NCBI
46	Hung JH: Oxidative stress and antioxidants in preeclampsia. J Chin Med Assoc. 70:430–432. 2007. View Article : Google Scholar : PubMed/NCBI