A review of the mechanism for poor placentation in early-onset preeclampsia: the role of autophagy in trophoblast invasion and vascular remodeling

Aluvihare, 2004, Regulatory T cells mediate maternal tolerance to the fetus, Nat. Immunol., 5, 266, 10.1038/ni1037 Bildirici, 2012, Survival by self-destruction: a role for autophagy in the placenta?, Placenta, 33, 591, 10.1016/j.placenta.2012.04.011 Broad, 2011, Placental protection of the fetal brain during short-term food deprivation, Proc. Natl. Acad. Sci. USA, 108, 15237, 10.1073/pnas.1106022108 Burton, 2009, Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy, Placenta, 30, 473, 10.1016/j.placenta.2009.02.009 Caniggia, 1999, Inhibition of TGF-beta 3 restores the invasive capability of extravillous trophoblasts in preeclamptic pregnancies, J. Clin. Invest., 103, 1641, 10.1172/JCI6380 Caniggia, 2000, Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3), J. Clin. Invest., 105, 577, 10.1172/JCI8316 Chang, 2013, Increased autophagy in the placental territory of selective intrauterine growth-restricted monochorionic twins, Prenat. Diagn., 33, 187, 10.1002/pd.4040 Chen, 2012, Hypoxia induces autophagy in primary human trophoblasts, Endocrinology, 153, 4946, 10.1210/en.2012-1472 Curtis, 2013, Identification of autophagic vacuoles and regulators of autophagy in villous trophoblast from normal term pregnancies and in fetal growth restriction, J. Matern. Fetal. Neonatal. Med., 26, 339, 10.3109/14767058.2012.733764 Farina, 2008, Gene expression in chorionic villous samples at 11 weeks’ gestation from women destined to develop preeclampsia, Prenat. Diagn., 28, 956, 10.1002/pd.2109 Fraser, 2012, Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance, J. Pathol., 228, 322, 10.1002/path.4057 Hanna, 2006, Decidual NK cells regulate key developmental processes at the human fetal-maternal interface, Nat. Med., 12, 1065, 10.1038/nm1452 Hiby, 2004, Combinations of maternal KIR and fetal HLA-C genes influence the risk of preeclampsia and reproductive success, J. Exp. Med., 200, 957, 10.1084/jem.20041214 Hung, 2010, Differential effects of concomitant use of vitamins C and E on trophoblast apoptosis and autophagy between normoxia and hypoxia-reoxygenation, PLoS One, 5, e12202, 10.1371/journal.pone.0012202 Hung, 2012, Increased autophagy in placentas of intrauterine growth-restricted pregnancies, PLoS One, 7, e40957, 10.1371/journal.pone.0040957 Ichimura, 2011, Pathophysiological role of autophagy: lesson from autophagy-deficient mouse models, Exp. Anim., 60, 329, 10.1538/expanim.60.329 Jauniaux, 2001, Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks’ gestation, Am. J. Obstet. Gynecol., 184, 998, 10.1067/mob.2001.111935 Jauniaux, 2005, Polyol concentrations in the fluid compartments of the human conceptus during the first trimester of pregnancy: maintenance of redox potential in a low oxygen environment, J. Clin. Endocrinol. Metab., 90, 1171, 10.1210/jc.2004-1513 Jeyabalan, 2008, Circulating and placental endoglin concentrations in pregnancies complicated by intrauterine growth restriction and preeclampsia, Placenta, 29, 555, 10.1016/j.placenta.2008.03.006 Kadyrov, 2003, Pre-eclampsia and maternal anaemia display reduced apoptosis and opposite invasive phenotypes of extravillous trophoblast, Placenta, 24, 540, 10.1053/plac.2002.0946 Kalkunte, 2010, Sera from preeclampsia patients elicit symptoms of human disease in mice and provide a basis for an in vitro predictive assay, Am. J. Pathol., 177, 2387, 10.2353/ajpath.2010.100475 Kaufmann, 2003, Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia, Biol. Reprod., 69, 1, 10.1095/biolreprod.102.014977 Khong, 1986, Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants, Br. J. Obstet. Gynaecol., 93, 1049, 10.1111/j.1471-0528.1986.tb07830.x Lash, 2011, Do uterine natural killer (uNK) cells contribute to female reproductive disorders?, J. Reprod. Immunol., 88, 156, 10.1016/j.jri.2011.01.003 Lash, 2010, Regulation of extravillous trophoblast invasion by uterine natural killer cells is dependent on gestational age, Hum. Reprod., 25, 1137, 10.1093/humrep/deq050 Lee, 2013, Increased SCF/c-kit by hypoxia promotes autophagy of human placental chorionic plate-derived mesenchymal stem cells via regulating the phosphorylation of mTOR, J. Cell. Biochem., 114, 79, 10.1002/jcb.24303 Levine, 2006, Soluble endoglin and other circulating antiangiogenic factors in preeclampsia, N. Engl J. Med., 355, 992, 10.1056/NEJMoa055352 Lyall, 2001, Transforming growth factor-beta expression in human placenta and placental bed in third trimester normal pregnancy preeclampsia, and fetal growth restriction, Am. J. Pathol., 159, 1827, 10.1016/S0002-9440(10)63029-5 Meekins, 1994, Endothelial cell activation by tumour necrosis factor-alpha (TNF-alpha) and the development of pre-eclampsia, Clin. Exp. Immunol., 98, 110, 10.1111/j.1365-2249.1994.tb06615.x Mizushima, 2010, Methods in mammalian autophagy research, Cell, 140, 313, 10.1016/j.cell.2010.01.028 Mizushima, 2011, The role of Atg proteins in autophagosome formation, Annu. Rev. Cell. Dev. Biol., 27, 107, 10.1146/annurev-cellbio-092910-154005 Mulla, 2011, Uric acid induces trophoblast IL-1β production via the inflammasome: implications for the pathogenesis of preeclampsia, Am. J. Reprod. Immunol., 65, 542, 10.1111/j.1600-0897.2010.00960.x Nakashima, 2013, Impaired autophagy by soluble endoglin under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia, Autophagy, 9, 303, 10.4161/auto.22927 Naruse, 2009, The urokinase plasminogen activator (uPA) system in uterine natural killer cells in the placental bed during early pregnancy, Placenta, 30, 398, 10.1016/j.placenta.2009.02.002 Naruse, 2009, Localization of matrix metalloproteinase (MMP)-2 MMP-9 and tissue inhibitors for MMPs (TIMPs) in uterine natural killer cells in early human pregnancy, Hum. Reprod., 24, 553, 10.1093/humrep/den408 Oh, 2008, Autophagy-related proteins, LC3 and Beclin-1 in placentas from pregnancies complicated by preeclampsia, Reprod. Sci., 15, 912, 10.1177/1933719108319159 Pijnenborg, 1980, Trophoblastic invasion of human decidua from 8 to 18 weeks of pregnancy, Placenta, 1, 3, 10.1016/S0143-4004(80)80012-9 Pursiheimo, 2009, Hypoxia-activated autophagy accelerates degradation of SQSTM1/p62, Oncogene, 28, 334, 10.1038/onc.2008.392 Redman, 2010, Immunology of pre-eclampsia, Am. J. Reprod. Immunol., 63, 534, 10.1111/j.1600-0897.2010.00831.x Redman, 1999, Preeclampsia: an excessive maternal inflammatory response to pregnancy, Am. J. Obstet. Gynecol., 180, 499, 10.1016/S0002-9378(99)70239-5 Saito, 2013, The role of autophagy in extravillous trophoblast function under hypoxia, Placenta, 27, S79, 10.1016/j.placenta.2012.11.026 Saito, 1999, Increased T-helper-1-type immunity and decreased T-helper-2-type immunity in patients with preeclampsia, Am. J. Reprod. Immunol., 41, 297, 10.1111/j.1600-0897.1999.tb00442.x Saito, 2007, Inadequate tolerance induction may induce pre-eclampsia, J. Reprod. Immunol., 76, 30, 10.1016/j.jri.2007.08.002 Saitoh, 2008, Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production, Nature, 456, 264, 10.1038/nature07383 Samstein, 2012, Extrathymic generation of regulatory T cells in placental mammals mitigates maternal-fetal conflict, Cell, 150, 29, 10.1016/j.cell.2012.05.031 Sasaki, 2004, Decidual and peripheral blood CD4+CD25+regulatory T cells in early pregnancy subjects and spontaneous abortion cases, Mol. Hum. Reprod., 10, 347, 10.1093/molehr/gah044 Sasaki, 2007, Proportion of peripheral blood and decidual CD4(+) CD25(bright) regulatory T cells in pre-eclampsia, Clin. Exp. Immunol., 149, 139, 10.1111/j.1365-2249.2007.03397.x Shen, 2008, Autophagic and apoptotic cell death in amniotic epithelial cells, Placenta, 29, 956, 10.1016/j.placenta.2008.09.001 Signorelli, 2011, Autophagy in term normal human placentas, Placenta, 32, 482, 10.1016/j.placenta.2011.03.005 Smith, 2009, Evidence for immune cell involvement in decidual spiral arteriole remodeling in early human pregnancy, Am. J. Pathol., 174, 1959, 10.2353/ajpath.2009.080995 Stark, 1993, Pre-eclampsia and cytokine induced oxidative stress, Br. J. Obstet. Gynaecol., 100, 105, 10.1111/j.1471-0528.1993.tb15203.x Steegers, 2010, Pre-eclampsia, Lancet, 376, 631, 10.1016/S0140-6736(10)60279-6 Stepan, 2007, Maternal plasma concentrations of soluble endoglin in pregnancies with intrauterine growth restriction, J. Clin. Endocrinol. Metab., 92, 2831, 10.1210/jc.2006-2774 Tuuli, 2011, Review: oxygen and trophoblast biology—a source of controversy, Placenta, 32, S109, 10.1016/j.placenta.2010.12.013 Venkatesha, 2006, Soluble endoglin contributes to the pathogenesis of preeclampsia, Nat. Med., 12, 642, 10.1038/nm1429 Yang, 2004, Persistent Toll-like receptor signals are required for reversal of regulatory T cell-mediated CD8 tolerance, Nat. Immunol., 5, 508, 10.1038/ni1059 Yoshizaki, 2012, Autophagy regulates inflammation in adipocytes, Biochem. Biophys. Res. Commun., 417, 352, 10.1016/j.bbrc.2011.11.114 Zhou, 1993, Preeclampsia is associated with abnormal expression of adhesion molecules by invasive cytotrophoblasts, J. Clin. Invest., 91, 950, 10.1172/JCI116316