Diet-induced obesity impairs endometrial stromal cell decidualization: A potential role for impaired autophagy

Human Reproduction

Volumn 31, Issue 6, 2016, Pages 1315-1326

  Rhee, Julie S ^a   Saben, Jessica L ^a   Mayer, Allyson L ^a   Schulte, Maureen B ^a   Asghar, Zeenat ^a   Stephens, Claire ^a   Chi, Maggie M Y ^a   Moley, Kelle H ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

autophagy; decidualization; implantation; obesity; reproduction

Indexed keywords

ACETYL COENZYME A CARBOXYLASE; ADENOSINE TRIPHOSPHATE; BIOLOGICAL MARKER; CYCLIC AMP; LC3B II PROTEIN; MEDROXYPROGESTERONE; MESSENGER RNA; PALMITIC ACID; PEPTIDES AND PROTEINS; PROLACTIN; PROTEIN SERINE THREONINE KINASE; SOMATOMEDIN BINDING PROTEIN 1; UNC 51 LIKE KINASE 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DECIDUALIZATION; DECIDUOMA; DIET INDUCED OBESITY; ENDOMETRIAL STROMAL CELL; ENDOMETRIUM CELL; FEMALE; FETUS; FIRST TRIMESTER PREGNANCY; FOLLICULAR PHASE; HEMATOXYLIN AND EOSIN STAINING; HUMAN; HUMAN CELL; HUMAN TISSUE; HYSTERECTOMY; IN VITRO STUDY; LIPID DIET; MALE; MATING; METABOLIC DISORDER; METABOLIC PARAMETERS; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; STAINING; STROMA CELL; SUGAR INTAKE; UTERINE TISSUE; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DECIDUA; METABOLISM; NIDATION; OBESITY; PATHOLOGY; PHOSPHORYLATION;

ANIMALS; AUTOPHAGY; BIOMARKERS; DECIDUA; DIET, HIGH-FAT; EMBRYO IMPLANTATION; FEMALE; HUMANS; MALE; MICE, INBRED C57BL; OBESITY; PALMITIC ACID; PHOSPHORYLATION; RNA, MESSENGER; STROMAL CELLS;

EID: 84973441435     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/dew048     Document Type: Article

References (47)

1. Armant DR. Autophagys expanding role in development: implantation is next. Endocrinology 2011;152:1739-1741.
2. Barth S, Glick D, Macleod KF. Autophagy: Assays and artifacts. J Pathol 2010; 221:117-124.
3. Bellver J, Pellicer A. Impact of obesity on spontaneous abortion. Am J Obstet Gynecol 2004;190:293-294.
4. Bellver J, Ayllon Y, Ferrando M, Melo M, Goyri E, Pellicer A, Remohi J, Meseguer M. Female obesity impairs in vitro fertilization outcome without affecting embryo quality. Fertil Steril 2010;93:447-454.
5. Bellver J, Martinez-Conejero JA, Labarta E, Alama P, Melo MA, Remohi J, Pellicer A, Horcajadas JA. Endometrial gene expression in the window of implantation is altered in obese women especially in association with polycystic ovary syndrome. Fertil Steril 2011;95:2335-2341, 2341. e1-8.
6. Bellver J, Pellicer A, Garcia-Velasco JA, Ballesteros A, Remohi J, Meseguer M. Obesity reduces uterine receptivity: clinical experience from 9, 587 first cycles of ovum donation with normal weight donors. Fertil Steril 2013; 100:1050-1058.
7. Benson GV, Lim H, Paria BC, Satokata I, Dey SK, Maas RL. Mechanisms of reduced fertility in Hoxa-10 mutant mice: uterine homeosis and loss of maternal Hoxa-10 expression. Development 1996;122:2687-2696.
8. Boots CE, Bernardi LA, Stephenson MD. Frequency of euploid miscarriage is increased in obese women with recurrent early pregnancy loss. Fertil Steril 2014;102:455-459.
9. Chen JR, Zhang J, LazarenkoOP, Kang P, Blackburn ML, Ronis MJ, Badger TM, Shankar K. Inhibition of fetal bone development through epigenetic down-regulation of HoxA10 in obese rats fed high-fat diet. FASEB J 2012;26:1131-1141.
10. Deb K, Reese J, Paria BC. Placenta and Trophoblast: Methods and Protocols. Totowa, NJ: Humana Press Inc., 2006.
11. Egan D, Kim J, Shaw RJ, Guan KL. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 2011;7:643-644.
12. Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: A systematic review and meta-analysis. JAMA 2013;309:71-82.
13. Frolova AI, O'Neill K, Moley KH. Dehydroepiandrosterone inhibits glucose flux through the pentose phosphate pathway in human and mouse endometrial stromal cells, preventing decidualization and implantation. Mol Endocrinol 2011;25:1444-1455.
14. Galliano D, Bellver J. Female obesity: short-and long-term consequences on the offspring. Gynecol Endocrinol 2013;29:626-631.
15. Gaudet L, Tu X, Fell D, El-Chaar D, Wu Wen S, Walker M. The effect of maternal Class III obesity on neonatal outcomes: A retrospective matched cohort study. J Matern Fetal Neonatal Med 2012;25:2281-2286.
16. Gaudet L, Ferraro ZM, Wen SW, Walker M. Maternal obesity and occurrence of fetal macrosomia: A systematic review and meta-analysis. BioMed Res Int 2014;2014:640291.
17. Herington JL, Bany BM. The conceptus increases secreted phosphoprotein 1 gene expression in the mouse uterus during the progression of decidualization mainly due to its effects on uterine natural killer cells. Reproduction 2007;133:1213-1221.
18. Hirota Y, Daikoku T, Tranguch S, Xie H, Bradshaw HB, Dey SK. Uterine-specific p53 deficiency confers premature uterine senescence and promotes preterm birth in mice. J Clin Invest 2010;120:803-815.
19. Igosheva N, Abramov AY, Poston L, Eckert JJ, Fleming TP, Duchen MR, McConnell J. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PloS One 2010;5:e10074.
20. Jungheim ES, Schoeller EL, Marquard KL, Louden ED, Schaffer JE, Moley KH. Diet-induced obesity model: Abnormal oocytes and persistent growth abnormalities in the offspring. Endocrinology 2010;151:4039-4046.
21. Jungheim ES, Louden ED, Chi MM, Frolova AI, Riley JK, Moley KH. Preimplantation exposure of mouse embryos to palmitic acid results in fetal growth restriction followed by catch-up growth in the offspring. Biol Reprod 2011;85:678-683.
22. Jungheim ES, Schon SB, Schulte MB, DeUgarte DA, Fowler SA, Tuuli MG. IVF outcomes in obese donor oocyte recipients: A systematic review and meta-analysis. Hum Reprod 2013;28:2720-2727.
23. Kien CL, Bunn JY, Stevens R, Bain J, Ikayeva O, Crain K, Koves TR, Muoio DM. Dietary intake of palmitate and oleate has broad impact on systemic and tissue lipid profiles in humans. Am J Clin Nutr 2014; 99:436-445.
24. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 2011;13:132-141.
25. Krikun G, Mor G, Lockwood C. The immortalization of human endometrial cells. Methods Mol Med 2006;121:79-83.
26. Large MJ, DeMayo FJ. The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol Cell Endocrinol 2012;358:155-165.
27. Las G, Serada SB, Wikstrom JD, Twig G, Shirihai OS. Fatty acids suppress autophagic turnover in beta-cells. J Biol Chem 2011;286:42534-42544.
28. Lee JE, Oh HA, Song H, Jun JH, Roh CR, Xie H, Dey SK, Lim HJ. Autophagy regulates embryonic survival during delayed implantation. Endocrinology 2011;152:2067-2075.
29. Luzzo KM, Wang Q, Purcell SH, Chi M, Jimenez PT, Grindler N, Schedl T, Moley KH. High fat diet induced developmental defects in the mouse: oocyte meiotic aneuploidy and fetal growth retardation/brain defects. PLoS One 2012;7:e49217.
30. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: A vicious cycle or a double-edged sword? Antioxid Redox Signal 2007; 9:2277-2293.
31. Mei S, Ni HM, Manley S, Bockus A, Kassel KM, Luyendyk JP, Copple BL, Ding WX. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J Pharmacol Exp Ther 2011; 339:487-498.
32. Mei J, Zhu XY, Jin LP, Duan ZL, Li DJ, Li MQ. Estrogen promotes the survival of human secretory phase endometrial stromal cells via CXCL12/CXCR4 up-regulation-mediated autophagy inhibition. Hum Reprod 2015;30: 1677-1689.
33. ModesittSC, HsuJY, ChowbinaSR, LawrenceRT, HoehnKL. Notall fat isequal: differential gene expression and potential therapeutic targets in subcutaneous adipose, visceral adipose, and endometrium of obese women with and without endometrial cancer. Int J Gynecol Cancer 2012;22:732-741.
34. Moley KH, Colditz GA. Effects of obesity on hormonally driven cancer in women. Sci Transl Med 2016;8:323ps3.
35. Moragianni VA, Jones SM, Ryley DA. The effect of body mass index on the outcomes of first assisted reproductive technology cycles. Fertil Steril 2012;98:102-108.
36. Ogden CL. Prevalence of obesity in the United States, 2009-2010. NCHS Data Brief 2012;82:1-8.
37. Rabinowitz JD, White E. Autophagy and metabolism. Science 2010; 330:1344-1348.
38. Rasmussen CA, Hashizume K, Orwig KE, Xu L, Soares MJ. Decidual prolactin-related protein: heterologous expression and characterization. Endocrinology 1996;137:5558-5566.
39. Ricchi M, Odoardi MR, Carulli L, Anzivino C, Ballestri S, Pinetti A, Fantoni LI, Marra F, Bertolotti M, Banni S et al. Differential effect of oleic and palmitic acid on lipid accumulation and apoptosis in cultured hepatocytes. J Gastroenterol Hepatol 2009;24:830-840.
40. Schroder AL, Pelch KE, Nagel SC. Estrogen modulates expression of putative housekeeping genes in the mouse uterus. Endocrine 2009; 35:211-219.
41. Talmor A, Dunphy B. Female obesity and infertility. Best Pract Res Clin Obstet Gynaecol 2015;29:498-506.
42. Tsai JH, Schulte M, O'Neill K, Chi MM, Frolova AI, Moley KH. Glucosamine inhibits decidualization of human endometrial stromal cells and decreases litter sizes in mice. Biol Reprod 2013;89:16.
43. Weikel KA, Cacicedo JM, Ruderman NB, Ido Y. Glucose and palmitate uncouple AMPK from autophagy in human aortic endothelial cells. Am J Physiol Cell Physiol 2015;308:C249-C263.
44. WorldHealthOrganization. Diet, nutrition and the prevention of chronic diseases. WHO Technical Report Series, No. 916. World Health Organization, 2003; p. 88.
45. Wu LL, Dunning KR, Yang X, RussellDL, LaneM, Norman RJ, Robker RL. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology 2010; 151:5438-5445.
46. Yardeni T, Eckhaus M, Morris HD, Huizing M, Hoogstraten-Miller S. Retro-orbital injections in mice. Lab Animal 2011;40:155-160.
47. Zhu H, Hou CC, Luo LF, Hu YJ, Yang WX. Endometrial stromal cells and decidualized stromal cells: origins, transformation and functions. Gene 2014;551:1-14.