Role of stem cell dysfunction in the development of great obstetrical syndromes
The paper provides a systems analysis of data on functional changes in the resident uterine and placental stem cells in preeclampsia (PE) and fetal growth restriction syndrome (FGRS); in particular, it discusses a reduction in their proliferative and angiogenic potential and an increase in the production of proinflammatory factors. It considers different aspects of cell therapy, ranging from the type of stem cells and their sources to the supposed mechanisms of therapeutic action, which determine the positive effect, as applied to therapy for PE and FGRS. The analysis of the data available in the literature could lead to the conclusion that cellular technologies are promising in treating PE and FGRS. Nonetheless, for their successful introduction into clinical practice, it is necessary to conduct further investigations of the comparative characteristics of stem cells in normal and pathological pregnancy, as well as the decoding of their molecular behavior in both cases.Sukhikh G.T., Silachev D.N., Goryunov K.V., Volochaeva M.V., Shmakov R.G.
Keywords
References
1. James J.L. Stem cells and pregnancy disorders: from pathological mechanisms to therapeutic horizons. Semin. Reprod. Med. 2016; 34(1): 17-26.
2. Villar J., Carroli G., Wojdyla D., Abalos E., Giordano D., Ba’aqeel H. et al. Preeclampsia, gestational hypertension and intrauterine growth restriction, related or independent conditions? Am. J. Obstet. Gynecol. 2006; 194(4): 921-31.
3. Yu C.K., Khouri O., Onwudiwe N., Spiliopoulos Y., Nicolaides K.H. Prediction of pre-eclampsia by uterine artery Doppler imaging: relationship to gestational age at delivery and small-for-gestational age. Ultrasound Obstet. Gynecol. 2008; 31(3): 310-3.
4. James J.L., Carter A.M., Chamley L.W. Human placentation from nidation to 5 weeks of gestation. Part I: What do we know about formative placental development following implantation? Placenta. 2012; 33(5): 327-34.
5. Boyd J.D., Hamilton W.J. The human placenta. Cambridge: W.Heffer & Sons Ltd; 1970.
6. James J.L., Srinivasan S., Alexander M., Chamley L.W. Can we fix it? Evaluating the potential of placental stem cells for the treatment of pregnancy disorders. Placenta. 2014; 35(2): 77-84.
7. Gargett C.E., Masuda H. Adult stem cells in the endometrium. Mol. Hum. Reprod. 2010; 16(11): 818-34.
8. Salker M., Teklenburg G., Molokhia M., Lavery S., Trew G., Aojanepong T. et al. Natural selection of human embryos: impaired decidualization of endometrium disables embryo-maternal interactions and causes recurrent pregnancy loss. PLoS One. 2010; 5(4): e10287.
9. Murakami K., Lee Y.H., Lucas E.S., Chan Y.W., Durairaj R.P., Takeda S. et al. Decidualization induces a secretome switch in perivascular niche cells of the human endometrium. Endocrinology. 2014; 155(11): 4542-53.
10. Bose P., Kadyrov M., Goldin R., Hahn S., Backos M., Regan L. et al. Aberrations of early trophoblast differentiation predispose to pregnancy failure: lessons from the anti-phospholipid syndrome. Placenta. 2006; 27(8): 869-75.
11. Reus A.D., Stephenson M.D., van Dunne F.M., de Krijger R.R., Joosten M., Steegers E.A. et al. Chorionic villous vascularization related to phenotype and genotype in first trimester miscarriages in a recurrent pregnancy loss cohort. Hum. Reprod. 2013; 28(4): 916-23.
12. Benirschke K., Burton G.J., Baergen R. Pathology of the human placenta. Berlin, Heidelberg: Springer-Verlag; 2000.
13. Pijnenborg R., Anthony J., Davey D.A., Rees A., Tiltman A., Vercruysse L. et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br. J. Obstet. Gynaecol. 1991; 98(7): 648-55.
14. James J.L., Whitley G.S., Cartwright J.E. Pre-eclampsia: fitting together the placental, immune and cardiovascular pieces. J. Pathol. 2010; 221(4): 363-78.
15. Rolfo A., Giuffrida D., Nuzzo A.M., Pierobon D., Cardaropoli S., Piccoli E. et al. Pro-inflammatory profile of preeclamptic placental mesenchymal stromal cells: new insights into the etiopathogenesis of preeclampsia. PLoS One. 2013; 8(3): e59403.
16. Todt J.C., Yang Y., Lei J., Lauria M.R., Sorokin Y., Cotton D.B. et al. Effects of tumor necrosis factor-alpha on human trophoblast cell adhesion and motility. Am. J. Reprod. Immunol. 1996; 36(2): 65-71.
17. Xu B., Nakhla S., Makris A., Hennessy A. TNF-alpha inhibits trophoblast integration into endothelial cellular networks. Placenta. 2011; 32(3): 241-6.
18. Takao T., Asanoma K., Kato K., Fukushima K., Tsunematsu R., Hirakawa T. et al. Isolation and characterization of human trophoblast side-population (SP) cells in primary villous cytotrophoblasts and HTR-8/SVneo cell line. PLoS One. 2011; 6(7): e21990.
19. Nuzzo A.M., Giuffrida D., Masturzo B., Mele P., Piccoli E., Eva C. et al. Altered expression of G1/S phase cell cycle regulators in placental mesenchymal stromal cells derived from preeclamptic pregnancies with fetal-placental compromise. Cell Cycle. 2017; 16(2): 200-12.
20. Burton G.J., Woods A.W., Jauniaux E., Kingdom J.C. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta. 2009; 30(6): 473-82.
21. Zhao G., Zhou X., Chen S., Miao H., Fan H., Wang Z. et al. Differential expression of microRNAs in decidua-derived mesenchymal stem cells from patients with pre-eclampsia. J. Biomed. Sci. 2014; 21: 81.
22. Hwang J.H., Lee M.J., Seok O.S., Paek Y.C., Cho G.J., Seol H.J. et al. Cytokine expression in placenta-derived mesenchymal stem cells in patients with pre-eclampsia and normal pregnancies. Cytokine. 2010; 49(1): 95-101.
23. Bills V.L., Hamdollah-Zadeh M., Soothill P.W., Harper S.J., Bates D.O. The role of VEGF-A165b in trophoblast survival. BMC Pregnancy Childbirth. 2014; 14: 278.
24. Ji L., Zhang L., Li Y., Guo L., Cao N., Bai Z. et al. MiR-136 contributes to pre-eclampsia through its effects on apoptosis and angiogenesis of mesenchymal stem cells. Placenta. 2017; 50: 102-9.
25. Clausson B., Gardosi J., Francis A., Cnattingius S. Perinatal outcome in SGA births defined by customised versus population-based birthweight standards. BJOG. 2001; 108(8): 830-4.
26. Eskenazi B., Fenster L., Sidney S., Elkin E.P. Fetal growth retardation in infants of multiparous and nulliparous women with preeclampsia. Am. J. Obstet. Gynecol. 1993; 169(5): 1112-8.
27. Sibley C.P. Understanding placental nutrient transfer-why bother? New biomarkers of fetal growth. J. Physiol. 2009; 587(Pt 14): 3431-40.
28. Langheinrich A.C., Vorman S., Seidenstucker J., Kampschulte M., Bohle R.M., Wienhard J. et al. Quantitative 3D micro-CT imaging of the human feto-placental vasculature in intrauterine growth restriction. Placenta. 2008; 29(11): 937-41.
29. Macara L., Kingdom J.C., Kaufmann P., Kohnen G., Hair J., More I.A. et al. Structural analysis of placental terminal villi from growth-restricted pregnancies with abnormal umbilical artery Doppler waveforms. Placenta. 1996; 17(1): 37-48.
30. Mando C., Razini P., Novielli C., Anelli G.M., Belicchi M., Erratico S. et al. Impaired angiogenic potential of human placental mesenchymal stromal cells in intrauterine growth restriction. Stem Cells Transl. Med. 2016; 5(4): 451-63.
31. Sipos P.I., Bourque S.L., Hubel C.A., Baker P.N., Sibley C.P., Davidge S.T. et al. Endothelial colony-forming cells derived from pregnancies complicated by intrauterine growth restriction are fewer and have reduced vasculogenic capacity. J. Clin. Endocrinol. Metab. 2013; 98(12): 4953-60.
32. Ligi I., Simoncini S., Tellier E., Vassallo P.F., Sabatier F., Guillet B. et al. A switch toward angiostatic gene expression impairs the angiogenic properties of endothelial progenitor cells in low birth weight preterm infants. Blood. 2011; 118(6): 1699-709.
33. Barker D.J., Eriksson J.G., Forsen T., Osmond C. Fetal origins of adult disease: strength of effects and biological basis. Int. J. Epidemiol. 2002; 31(6): 1235-9.
34. Сухих Г.Т., Чернуха Г.Е., Табеева Г.И., Горюнов К.В., Силачев Д.Н. Современные возможности клеточной терапии синдрома Ашермана. Акушерство и гинекология. 2018; 5: 20-9.
35. Nagori C.B., Panchal S.Y., Patel H. Endometrial regeneration using autologous adult stem cells followed by conception by in vitro fertilization in a patient of severe Asherman’s syndrome. J. Hum. Reprod. Sci. 2011; 4(1): 43-8.
36. Meraviglia V., Vecellio M., Grasselli A., Baccarin M., Farsetti A., Capogrossi M.C. et al. Human chorionic villus mesenchymal stromal cells reveal strong endothelial conversion properties. Differentiation. 2012; 83(5): 260-70.
37. Kong P., Xie X., Li F., Liu Y., Lu Y. Placenta mesenchymal stem cell accelerates wound healing by enhancing angiogenesis in diabetic Goto-Kakizaki (GK) rats. Biochem. Biophys. Res. Commun. 2013; 438(2): 410-9.
38. Tran T.C., Kimura K., Nagano M., Yamashita T., Ohneda K., Sugimori H. et al. Identification of human placenta-derived mesenchymal stem cells involved in re-endothelialization. J. Cell. Physiol. 2011; 226(1): 224-35.
39. Gnecchi M., Zhang Z., Ni A., Dzau V.J. Paracrine mechanisms in adult stem cell signaling and therapy. Circ. Res. 2008; 103(11): 1204-19.
40. Mirotsou M., Zhang Z., Deb A., Zhang L., Gnecchi M., Noiseux N. et al. Secreted frizzled related protein 2 (Sfrp2) is the key Akt-mesenchymal stem cell-released paracrine factor mediating myocardial survival and repair. Proc. Natl. Acad. Sci. USA. 2007; 104(5): 1643-8.
41. von Bahr L., Batsis I., Moll G., Hagg M., Szakos A., Sundberg B. et al. Analysis of tissues following mesenchymal stromal cell therapy in humans indicates limited long-term engraftment and no ectopic tissue formation. Stem Cells. 2012; 30(7): 1575-8.
42. Redline R.W. Villitis of unknown etiology: noninfectious chronic villitis in the placenta. Hum. Pathol. 2007; 38(10): 1439-46.
43. Rubtsov Y., Goryunov К., Romanov А., Suzdaltseva Y., Sharonov G., Tkachuk V. Molecular Mechanisms of immunomodulation properties of mesenchymal stromal cells: a new insight into the Role of ICAM-1. Stem Cells Int. 2017; 2017: 6516854.
44. Aggarwal S., Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005; 105(4): 1815-22.
45. Spaggiari G.M., Capobianco A., Abdelrazik H., Becchetti F., Mingari M.C., Moretta L. Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: role of indoleamine 2,3-dioxygenase and prostaglandin E2. Blood. 2008; 111(3): 1327-33.
46. Abumaree M.H., Al Jumah M.A., Kalionis B., Jawdat D., Al Khaldi A., Abomaray F.M. et al. Human placental mesenchymal stem cells (pMSCs) play a role as immune suppressive cells by shifting macrophage differentiation from inflammatory M1 to anti-inflammatory M2 macrophages. Stem Cell Rev. 2013; 9(5): 620-41.
47. Rubtsov Y.P., Suzdaltseva Y.G., Goryunov K.V., Kalinina N.I., Sysoeva V.Y., Tkachuk V.A. Regulation of immunity via multipotent mesenchymal stromal cells. Acta Naturae. 2012; 4(1): 23-31.
48. Chatterjee P., Chiasson V.L., Pinzur L., Raveh S., Abraham E., Jones K.A. et al. Human placenta-derived stromal cells decrease inflammation, placental injury and blood pressure in hypertensive pregnant mice. Clin. Sci. (Lond.). 2016; 130(7): 513-23.
Received 28.09.2017
Accepted 27.10.2017
About the Authors
Gennady T. Sukhikh, PhD, Professor, Academician of RAS, Director of National Medical Research Center of Obstetrics, Gynecology and Perinatology namedafter Academician V.I. Kulakov. 117997, Russia, Moscow, Ac. Oparina str. 4. Tel.: +74954381800. E-mail: g_sukhikh@oparina4.ru
Roman G. Shmakov, Doctor of Medical Science, Medical director, National Medical Research Center of Obstetrics, Gynecology and Perinatology named after Academician V.I. Kulakov. 117997, Russia, Moscow, Ac. Oparina str. 4. Tel.: +74954387200. E-mail: r_shmakov@oparina4.ru
Kirill V. Goryunov, Junior Research Scientist, laboratory of cell technologies, National Medical Research Center of Obstetrics, Gynecology and Perinatology named
after Academician V.I. Kulakov. 117997, Russia, Moscow, Ac. Oparina str. 4. Tel.: +79164108844. E-mail: k_gorunov@oparina4.ru
Maria V. Volochaeva, PhD, medical sciences, Obstetrician-gynaecologist, physiological and obstetric department, National Medical Research Center of Obstetrics,
Gynecology and Perinatology named after Academician V.I. Kulakov. 117997, Russia, Moscow, Ac. Oparina str. 4. Tel.: +79199687298. E-mail: m_volochaeva@oparina4.ru
Denis N. Silachev, PhD. Senior Research Scientist, Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University.
119992, Russia, Moscow, Leninskye gory, 1, bld. 40. Tel.: +79057921301. E-mail: silachevdn@genebee.msu.ru
For citations: Sukhikh G.T., Silachev D.N., Goryunov K.V., Volochaeva M.V., Shmakov R.G. Role of stem cell dysfunction in the development of great obstetrical syndromes. Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2018; (7): 5-11. (in Russian)
https://dx.doi.org/10.18565/aig.2018.7.5-11