Autophagy regulation of physiological and pathological processes in the female reproductive tract

American Journal of Reproductive Immunology

Volumn 77, Issue 5, 2017, Pages

  Cao, Bin ^a   Camden, Alison J ^a   Parnell, Lindsay A ^a   Mysorekar, Indira U ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atg16l1; ovary; placenta; preterm birth; syncytiotrophoblast

Indexed keywords

AUTOPHAGY; BIRTH; CONFERENCE PAPER; FEMALE; FEMALE GENITAL SYSTEM; HUMAN; LABOR; OOCYTE; OOCYTE DEVELOPMENT; PLACENTA; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; UTERUS; PHYSIOLOGY; PLACENTA DEVELOPMENT;

AUTOPHAGY; FEMALE; GENITALIA, FEMALE; HUMANS; PARTURITION; PLACENTATION; PREGNANCY;

EID: 85012911430     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12650     Document Type: Conference Paper

References (58)

1. Bauckman KA, Owusu-Boaitey N, Mysorekar IU. Selective autophagy: xenophagy. Methods 2015;75:120–127.
2. Kroemer G, Galluzzi L, Vandenabeele P, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16:3–11.
3. Campisi J, Robert L. Cell senescence: role in aging and age-related diseases. Interdiscip Top Gerontol. 2014;39:3945–3961.
4. Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
5. Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004;432:1032–1036.
6. Mizushima N. Autophagy: process and function. Genes Dev. 2007;21:2861–2873.
7. Levine B, Mizushima N, Virgin HW. Autophagy in immunity and inflammation. Nature. 2011;469:323–335.
8. Song ZH, Yu HY, Wang P, et al. Germ cell-specific Atg7 knockout results in primary ovarian insufficiency in female mice. Cell Death Dis 2015;6:e1589.
9. Choi J, Jo M, Lee E, Choi D. Induction of apoptotic cell death via accumulation of autophagosomes in rat granulosa cells. Fertil Steril. 2011;95:1482–1486.
10. Duerrschmidt N, Zabirnyk O, Nowicki M, et al. Lectin-like oxidized low-density lipoprotein receptor-1-mediated autophagy in human granulosa cells as an alternative of programmed cell death. Endocrinology. 2006;147:3851–3860.
11. Adastra KL, Chi MM, Riley JK, Moley KH. A differential autophagic response to hyperglycemia in the developing murine embryo. Reproduction. 2011;141:607–615.
12. El-Shershaby AM, Hinchliffe JR. Epithelial autolysis during implantation of the mouse blastocyst: an ultrastructural study. J Embryol Exp Morphol. 1975;33:1067–1080.
13. Hou X, Tan Y, Li M, Dey SK, Das SK. Canonical Wnt signaling is critical to estrogen-mediated uterine growth. Mol Endocrinol. 2004;18:3035–3049.
14. Das A, Mantena SR, Kannan A, Evans DB, Bagchi MK, Bagchi IC. De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc Natl Acad Sci USA. 2009;106:12542–12547.
15. Choi S, Shin H, Song H, Lim HJ. Suppression of autophagic activation in the mouse uterus by estrogen and progesterone. J Endocrinol. 2014;221:39–50.
16. Lee JE, Oh HA, Song H, et al. Autophagy regulates embryonic survival during delayed implantation. Endocrinology. 2011;152:2067–2075.
17. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA. 2003;100:15077–15082.
18. Fimia GM, Stoykova A, Romagnoli A, et al. Ambra1 regulates autophagy and development of the nervous system. Nature. 2007;447:1121–1125.
19. Tsukamoto S, Kuma A, Murakami M, Kishi C, Yamamoto A, Mizushima N. Autophagy is essential for preimplantation development of mouse embryos. Science. 2008;321:117–120.
20. Schier AF. The maternal-zygotic transition: death and birth of RNAs. Science. 2007;316:406–407.
21. Luo SM, Ge ZJ, Wang ZW, et al. Unique insights into maternal mitochondrial inheritance in mice. Proc Natl Acad Sci USA. 2013;110:13038–13043.
22. Hung TH, Hsieh TT, Chen SF, Li MJ, Yeh YL. Autophagy in the human placenta throughout gestation. PLoS ONE. 2013;8:e83475.
23. Shen ZY, Li EM, Lu SQ, et al. Autophagic and apoptotic cell death in amniotic epithelial cells. Placenta. 2008;29:956–961.
24. Shen ZY, Xu LY, Li EM, et al. Autophagy and endocytosis in the amnion. J Struct Biol. 2008;162:197–204.
25. Hiyama M, Kusakabe KT, Takeshita A, et al. Nutrient starvation affects expression of LC3 family at the feto-maternal interface during murine placentation. J Vet Med Sci. 2015;77:305–311.
26. Cao B, Macones C, Mysorekar IU. ATG16L1 governs placental infection risk and preterm birth in mice and women. JCI Insight. 2016;1:e86654.
27. Pringle KG, Kind KL, Sferruzzi-Perri AN, Thompson JG, Roberts CT. Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy. Hum Reprod Update. 2010;16:415–431.
28. Chen B, Longtine MS, Nelson DM. Hypoxia induces autophagy in primary human trophoblasts. Endocrinology. 2012;153:4946–4954.
29. Choi JH, Lee HJ, Yang TH, Kim GJ. Effects of hypoxia inducible factors-1alpha on autophagy and invasion of trophoblasts. Clin Exp Reprod Med. 2012;39:73–80.
30. Yamanaka-Tatematsu M, Nakashima A, Fujita N, Shima T, Yoshimori T, Saito S. Autophagy induced by HIF1alpha overexpression supports trophoblast invasion by supplying cellular energy. PLoS ONE. 2013;8:e76605.
31. Muralimanoharan S, Gao X, Weintraub S, Myatt L, Maloyan A. Sexual dimorphism in activation of placental autophagy in obese women with evidence for fetal programming from a placenta-specific mouse model. Autophagy. 2016;12:752–769.
32. Avagliano L, Danti L, Doi P, et al. Autophagy in placentas from acidotic newborns: an immunohistochemical study of LC3 expression. Placenta 2013;34:1091–1094.
33. Avagliano L, Massa V, Zullino S, et al. Inflammation modulates LC3 expression in human preterm delivery. J Matern Fetal Neonatal Med. 2017;30:698–704.
34. Avagliano L, Virgili E, Garo C, et al. Autophagy and human parturition: evaluation of LC3 expression in placenta from spontaneous or medically induced onset of labor. Biomed Res Int. 2013;2013:689768.
35. Paavola LG. The corpus luteum of the guinea pig: cytochemistry of luteal cell regression. J Cell Biol 1978;79:59–73.
36. Kyathanahalli C, Marks J, Nye K, et al. Cross-species withdrawal of MCL1 facilitates postpartum uterine involution in both the mouse and baboon. Endocrinology. 2013;154:4873–4884.
37. Oh SY, Choi SJ, Kim KH, Cho EY, Kim JH, Roh CR. Autophagy-related proteins, LC3 and Beclin-1, in placentas from pregnancies complicated by preeclampsia. Reprod Sci. 2008;15:912–920.
38. Hung TH, Chen SF, Lo LM, Li MJ, Yeh YL, Hsieh TT. Increased autophagy in placentas of intrauterine growth-restricted pregnancies. PLoS ONE. 2012;7:e40957.
39. Akaishi R, Yamada T, Nakabayashi K, et al. Autophagy in the placenta of women with hypertensive disorders in pregnancy. Placenta. 2014;35:974–980.
40. Gao L, Qi HB, Kamana KC, Zhang XM, Zhang H, Baker PN. Excessive autophagy induces the failure of trophoblast invasion and vasculature: possible relevance to the pathogenesis of preeclampsia. J Hypertens. 2015;33:106–117.
41. Goldman-Wohl D, Cesla T, Smith Y, et al. Expression profiling of autophagy associated genes in placentas of preeclampsia. Placenta. 2013;34:959–962.
42. Nakashima A, Yamanaka-Tatematsu M, Fujita N, et al. Impaired autophagy by soluble endoglin, under physiological hypoxia in early pregnant period, is involved in poor placentation in preeclampsia. Autophagy. 2013;9:303–316.
43. Kanninen TT, Jayaram A, Jaffe Lifshitz S, Witkin SS. Altered autophagy induction by sera from pregnant women with pre-eclampsia: a case-control study. BJOG. 2014;121:958–964.
44. Curtis S, Jones CJ, Garrod A, Hulme CH, Heazell AE. 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. 2013;26:339–346.
45. Chang YL, Wang TH, Chang SD, Chao AS, Hsieh PC, Wang CN. Increased autophagy in the placental territory of selective intrauterine growth-restricted monochorionic twins. Prenat Diagn. 2013;33:187–190.
46. Sisti G, Kanninen TT, Di TM, Witkin SS, Spandorfer SD. Autophagy induction by sera from women undergoing an in vitro fertilization cycle varies with subsequent outcome. J Reprod Immunol 2016;117:1–3.
47. Kanninen TT, Sisti G, Witkin SS. Induction of the 70 kDa heat shock protein stress response inhibits autophagy: possible consequences for pregnancy outcome. J Matern Fetal Neonatal Med. 2016;29:159–162.
48. Kanninen TT, de Andrade Ramos BR, Witkin SS. The role of autophagy in reproduction from gametogenesis to parturition. Eur J Obstet Gynecol Reprod Biol 2013;171:3–8.
49. de Andrade Ramos BR, Witkin SS. The influence of oxidative stress and autophagy cross regulation on pregnancy outcome. Cell Stress Chaperones. 2016;21:755–762.
50. Hirota Y, Cha J, Yoshie M, Daikoku T, Dey SK. Heightened uterine mammalian target of rapamycin complex 1 (mTORC1) signaling provokes preterm birth in mice. Proc Natl Acad Sci USA. 2011;108:18073–18078.
51. Gawriluk TR, Ko C, Hong X, Christenson LK, Rucker EB 3rd. Beclin-1 deficiency in the murine ovary results in the reduction of progesterone production to promote preterm labor. Proc Natl Acad Sci USA. 2014;111:E4194–E4203.
52. Agrawal V, Hirsch E. Intrauterine infection and preterm labor. Semin Fetal Neonatal Med. 2012;17:12–19.
53. Agrawal V, Jaiswal MK, Mallers T, et al. Altered autophagic flux enhances inflammatory responses during inflammation-induced preterm labor. Sci Rep 2015;5:9410.
54. Brickle A, Tran HT, Lim R, Liong S, Lappas M. Autophagy, which is decreased in labouring fetal membranes, regulates IL-1beta production via the inflammasome. Placenta. 2015;36:1393–1404.
55. Symington JW, Wang C, Twentyman J, et al. ATG16L1 deficiency in macrophages drives clearance of uropathogenic E. coli in an IL-1beta-dependent manner. Mucosal Immunol. 2015;8:1388–1399.
56. Cao B, Mysorekar IU. Intracellular bacteria in placental basal plate localize to extravillous trophoblasts. Placenta. 2014;35:139–142.
57. Robbins JR, Bakardjiev AI. Pathogens and the placental fortress. Curr Opin Microbiol. 2012;15:36–43.
58. Doulaveris G, Orfanelli T, Benn K, Zervoudakis I, Skupski D, Witkin SS. A polymorphism in an autophagy-related gene, ATG16L1, influences time to delivery in women with an unfavorable cervix who require labor induction. J Perinat Med. 2013;41:411–414.