Maternal nutrition modifies trophoblast giant cell phenotype and fetal growth in mice

Reproduction

Volumn 149, Issue 6, 2015, Pages 563-575

  Watkins, Adam J ^a,b   Lucas, Emma S ^a   Marfy Smith, Stephanie ^a   Bates, Nicola ^c   Kimber, Susan J ^c   Fleming, Tom P ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b ASTON UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; FETUS DEVELOPMENT; FETUS GROWTH; GIANT CELL; IN VITRO STUDY; MATERNAL NUTRITION; MOUSE; NIDATION; NONHUMAN; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROTEIN DIET; PROTEIN RESTRICTION; SIGNAL TRANSDUCTION; TROPHOBLAST; YOLK SAC; ANIMAL; CELL MOTION; CYTOLOGY; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; REPRODUCTION;

MAMMALIA; MUS;

ANIMALS; CELL MOVEMENT; DIET, PROTEIN-RESTRICTED; FEMALE; FETAL DEVELOPMENT; GIANT CELLS; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE; PHOSPHORYLATION; PLACENTATION; PREGNANCY; SIGNAL TRANSDUCTION; TROPHOBLASTS;

EID: 84930636970     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-14-0667     Document Type: Article

References (55)

1. Adamson SL, Lu Y, Whiteley KJ, Holmyard D, Hemberger M, Pfarrer C & Cross JC 2002 Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Developmental Biology 250 358-373. (doi:10.1006/dbio.2002.0773)
2. Armitage JA, Khan IY, Taylor PD, Nathanielsz PW & Poston L 2004 Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? Journal of Physiology 561 355-377. (doi:10.1113/jphysiol.2004.072009)
3. Auman HJ, Nottoli T, Lakiza O, Winger Q, Donaldson S & Williams T 2002 Transcription factor AP-2γ is essential in the extra-embryonic lineages for early postimplantation development. Development 129 2733-2747.
4. Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD & Knofler M 2004 Tumor necrosis factor-α inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. Journal of Clinical Endocrinology and Metabolism 89 812-822. (doi:10.1210/jc.2003-031351)
5. Bevilacqua EM & Abrahamsohn PA 1988 Ultrastructure of trophoblast giant cell transformation during the invasive stage of implantation of the mouse embryo. Journal of Morphology 198 341-351. (doi:10.1002/jmor.1051980308)
6. Brown DG, Warren VN, Pahlsson P & Kimber SJ 1993 Carbohydrate antigen expression in murine embryonic stem cells and embryos. I. Lacto and neo-lacto determinants. Histochemical Journal 25 452-463. (doi:10.1007/BF00157810)
7. Caluwaerts S, Pijnenborg R, Luyten C & Van Assche FA 2000 Growth characteristics of diabetic rat ectoplacental cones in vivo and in vitro. Diabetologia 43 939-945. (doi:10.1007/s001250051473)
8. Centrella M, Canalis E, McCarthy TL, Stewart AF, Orloff JJ & Insogna KL 1989 Parathyroid hormone-related protein modulates the effect of transforming growth factor-β on deoxyribonucleic acid and collagen synthesis in fetal rat bone cells. Endocrinology 125 199-208. (doi:10.1210/endo-125-1-199)
9. Chen PY, Ganguly A, Rubbi L, Orozco LD, Morselli M, Ashraf D, Jaroszewicz A, Feng S, Jacobsen SE, Nakano A et al. 2013 Intrauterine calorie restriction affects placental DNA methylation and gene expression. Physiological Genomics 45 565-576. (doi:10.1152/physiolgenomics.00034.2013)
10. Coan PM, Vaughan OR, McCarthy J, Mactier C, Burton GJ, Constancia M & Fowden AL 2011 Dietary composition programmes placental phenotype in mice. Journal of Physiology 589 3659-3670. (doi:10.1113/jphysiol.2011.208629)
11. Dowling RJ, Topisirovic I, Fonseca BD & Sonenberg N 2010 Dissecting the role of mTOR: lessons from mTOR inhibitors. Biochimica et Biophysica Acta 1804 433-439. (doi:10.1016/j.bbapap.2009.12.001)
12. Eckert JJ, Porter R, Watkins AJ, Burt E, Brooks S, Leese HJ, Humpherson PG, Cameron IT & Fleming TP 2012 Metabolic induction and early responses of mouse blastocyst developmental programming following maternal low protein diet affecting life-long health. PLoS ONE 7 e52791. (doi:10.1371/journal.pone.0052791)
13. El-Hashash AH & Kimber SJ 2004 Trophoblast differentiation in vitro: establishment and characterisation of a serum-free culture model for murine secondary trophoblast giant cells. Reproduction 128 53-71. (doi:10.1530/rep.1.00149)
14. El-Hashash AH, Esbrit P & Kimber SJ 2005 PTHrP promotes murine secondary trophoblast giant cell differentiation through induction of endocycle, upregulation of giant-cell-promoting transcription factors and suppression of other trophoblast cell types. Differentiation 73 154-174. (doi:10.1111/j.1432-0436.2005.00013.x)
15. El-Hashash AH, Warburton D & Kimber SJ 2010 Genes and signals regulating murine trophoblast cell development. Mechanisms of Development 127 1-20. (doi:10.1016/j.mod.2009.09.004)
16. Fowden AL, Sferruzzi-Perri AN, Coan PM, Constancia M & Burton GJ 2009 Placental efficiency and adaptation: endocrine regulation. Journal of Physiology 587 3459-3472. (doi:10.1113/jphysiol.2009.173013)
17. Gabory A, Ferry L, Fajardy I, Jouneau L, Gothie JD, Vige A, Fleur C, Mayeur S, Gallou-Kabani C, Gross MS et al. 2012 Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLoS ONE 7 e47986. (doi:10.1371/journal.pone.0047986)
18. Gaccioli F, White V, Capobianco E, Powell TL, Jawerbaum A & Jansson T 2013 Maternal overweight induced by a diet with high content of saturated fat activates placental mTOR and eIF2α signaling and increases fetal growth in rats. Biology of Reproduction 89 96. (doi:10.1095/biolreprod.113.109702)
19. Georgiades P, Ferguson-Smith AC & Burton GJ 2002 Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23 3-19. (doi:10.1053/plac.2001.0738)
20. Gheorghe CP, Goyal R, Holweger JD & Longo LD 2009 Placental gene expression responses to maternal protein restriction in the mouse. Placenta 30 411-417. (doi:10.1016/j.placenta.2009.03.002)
21. Hanson MA & Gluckman PD 2014 Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiological Reviews 94 1027-1076. (doi:10.1152/physrev.00029.2013)
22. Hayes EK, Tessier DR, Percival ME, Holloway AC, Petrik JJ, Gruslin A & Raha S 2014 Trophoblast invasion and blood vessel remodeling are altered in a rat model of lifelong maternal obesity. Reproductive Sciences 21 648-657. (doi:10.1177/1933719113508815)
23. Hemberger M, Hughes M & Cross JC 2004 Trophoblast stem cells differentiate in vitro into invasive trophoblast giant cells. Developmental Biology 271 362-371. (doi:10.1016/j.ydbio.2004.03.040)
24. Jansson N, Pettersson J, Haafiz A, Ericsson A, Palmberg I, Tranberg M, Ganapathy V, Powell TL & Jansson T 2006 Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. Journal of Physiology 576 935-946.
25. Jansson T, Aye IL & Goberdhan DC 2012 The emerging role of mTORC1 signaling in placental nutrient-sensing. Placenta 33 (Suppl 2) e23-e29. (doi:10.1016/j.placenta.2012.05.010)
26. Jovanovic M, Stefanoska I, Radojcic L & Vicovac L 2010 Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP)2 and MMP9 and integrins α5 and β1. Reproduction 139 789-798. (doi:10.1530/REP-09-0341)
27. Kavitha JV, Rosario FJ, Nijland MJ, McDonald TJ, Wu G, Kanai Y, Powell TL, Nathanielsz PW & Jansson T 2014 Down-regulation of placental mTOR, insulin/IGF-I signaling, and nutrient transporters in response to maternal nutrient restriction in the baboon. FASEB Journal 28 1294-1305. (doi:10.1096/fj.13-242271)
28. Kim E 2009 Mechanisms of amino acid sensing in mTOR signaling pathway. Nutrition Research and Practice 3 64-71. (doi:10.4162/nrp.2009.3.1.64)
29. Kim DW, Young SL, Grattan DR & Jasoni CL 2014 Obesity during pregnancy disrupts placental morphology, cell proliferation, and inflammation in a sex-specific manner across gestation in the mouse. Biology of Reproduction 90 130. (doi:10.1095/biolreprod.113.117259)
30. Kwong WY, Wild AE, Roberts P, Willis AC & Fleming TP 2000 Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127 4195-4202.
31. Lager S, Samulesson AM, Taylor PD, Poston L, Powell TL & Jansson T 2014 Diet-induced obesity in mice reduces placental efficiency and inhibits placental mTOR signaling. Physiological Reports 2 e00242. (doi:10.1002/phy2.242)
32. Ma Y, Zhu MJ, Uthlaut AB, Nijland MJ, Nathanielsz PW, Hess BW & Ford SP 2011 Upregulation of growth signaling and nutrient transporters in cotyledons of early to mid-gestational nutrient restricted ewes. Placenta 32 255-263. (doi:10.1016/j.placenta.2011.01.007)
33. Malandro MS, Beveridge MJ, Kilberg MS & Novak DA 1996 Effect of lowprotein diet-induced intrauterine growth retardation on rat placental amino acid transport. American Journal of Physiology 271 C295-C303.
34. O'Brien PJ, Koi H, Parry S, Brass LF, Strauss JF III, Wang LP, Tomaszewski JE & Christenson LK 2003 Thrombin receptors and protease-activated receptor-2 in human placentation: receptor activation mediates extravillous trophoblast invasion in vitro. American Journal of Pathology 163 1245-1254. (doi:10.1016/S0002-9440(10)63484-0)
35. Pavan L, Hermouet A, Tsatsaris V, Therond P, Sawamura T, Evain-Brion D & Fournier T 2004 Lipids from oxidized low-density lipoprotein modulate human trophoblast invasion: involvement of nuclear liver X receptors. Endocrinology 145 4583-4591. (doi:10.1210/en.2003-1747)
36. Roos S, Jansson N, Palmberg I, Saljo K, Powell TL & Jansson T 2007 Mammalian target of rapamycin in the human placenta regulates leucine transport and is down-regulated in restricted fetal growth. Journal of Physiology 582 449-459. (doi:10.1113/jphysiol.2007.129676)
37. Rosario FJ, Jansson N, Kanai Y, Prasad PD, Powell TL & Jansson T 2011 Maternal protein restriction in the rat inhibits placental insulin, mTOR, and STAT3 signaling and down-regulates placental amino acid transporters. Endocrinology 152 1119-1129. (doi:10.1210/en.2010-1153)
38. Rossant J & Cross JC 2001 Placental development: lessons from mouse mutants. Nature Reviews. Genetics 2 538-548. (doi:10.1038/35080570)
39. Salafia CM, Zhang J, Miller RK, Charles AK, Shrout P & Sun W 2007 Placental growth patterns affect birth weight for given placental weight. Birth Defects Research. Part A, Clinical and Molecular Teratology 79 281-288. (doi:10.1002/bdra.20345)
40. Sato Y, Fujiwara H, Higuchi T, Yoshioka S, Tatsumi K, Maeda M & Fujii S 2002 Involvement of dipeptidyl peptidase IV in extravillous trophoblast invasion and differentiation. Journal of Clinical Endocrinology and Metabolism 87 4287-4296. (doi:10.1210/jc.2002-020038)
41. Scott IC, Anson-Cartwright L, Riley P, Reda D & Cross JC 2000 The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Molecular and Cellular Biology 20 530-541. (doi:10.1128/MCB.20.2.530-541.2000)
42. Sferruzzi-Perri AN, Vaughan OR, Haro M, Cooper WN, Musial B, Charalambous M, Pestana D, Ayyar S, Ferguson-Smith AC, Burton GJ et al. 2013 An obesogenic diet during mouse pregnancy modifies maternal nutrient partitioning and the fetal growth trajectory. FASEB Journal 27 3928-3937. (doi:10.1096/fj.13-234823)
43. Simmons DG & Cross JC 2005 Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Developmental Biology 284 12-24. (doi:10.1016/j.ydbio.2005.05.010)
44. Simmons DG, Fortier AL & Cross JC 2007 Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Developmental Biology 304 567-578. (doi:10.1016/j.ydbio.2007.01.009)
45. Soares MJ, Konno T & Alam SM 2007 The prolactin family: effectors of pregnancy-dependent adaptations. Trends in Endocrinology and Metabolism 18 114-121. (doi:10.1016/j.tem.2007.02.005)
46. Staff AC, Ranheim T, Henriksen T & Halvorsen B 2000 8-Iso-prostaglandin f(2α) reduces trophoblast invasion and matrix metalloproteinase activity. Hypertension 35 1307-1313. (doi:10.1161/01.HYP.35.6.1307)
47. Sun C, Velazquez MA, Marfy-Smith S, Sheth B, Cox A, Johnston DA, Smyth N & Fleming TP 2014 Mouse early extra-embryonic lineages activate compensatory endocytosis in response to poor maternal nutrition. Development 141 1140-1150. (doi:10.1242/dev.103952)
48. Vaughan OR, Sferruzzi-Perri AN, Coan PM & Fowden AL 2011 Environmental regulation of placental phenotype: implications for fetal growth. Reproduction, Fertility, and Development 24 80-96. (doi:10.1071/RD11909)
49. Wang H, Zhou D & Pan Y-X 2014 Low protein diet during gestation and lactation induces autophagy-related gene LC3 in the liver of rat dams (737.5). FASEB Journal 28. (http://www.fasebj.org/citmgr?gca=fasebj%3B28%2F1-Supplement%2F737.5)
50. Watkins AJ, Ursell E, Panton R, Papenbrock T, Hollis L, Cunningham C, Wilkins A, Perry VH, Sheth B, Kwong WY et al. 2008 Adaptive responses by mouse early embryos to maternal diet protect fetal growth but predispose to adult onset disease. Biology of Reproduction 78 299-306. (doi:10.1095/biolreprod.107.064220)
51. Watkins AJ, Lucas ES, Torrens C, Cleal JK, Green L, Osmond C, Eckert JJ, Gray WP, Hanson MA & Fleming TP 2010 Maternal low-protein diet during mouse pre-implantation development induces vascular dysfunction and altered renin-angiotensin-system homeostasis in the offspring. British Journal of Nutrition 103 1762-1770. (doi:10.1017/S0007114509993783)
52. Watkins AJ, Lucas ES, Wilkins A, Cagampang FR & Fleming TP 2011 Maternal periconceptional and gestational low protein diet affects mouse offspring growth, cardiovascular and adipose phenotype at 1 year of age. PLoS ONE 6 e28745. (doi:10.1371/journal.pone.0028745)
53. Xu G, Guimond MJ, Chakraborty C & Lala PK 2002 Control of proliferation, migration, and invasiveness of human extravillous trophoblast by decorin, a decidual product. Biology of Reproduction 67 681-689. (doi:10.1095/biolreprod67.2.681)
54. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS & Burton GJ 2008 Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. American Journal of Pathology 173 451-462. (doi:10.2353/ajpath.2008.071193)
55. Zorn TM, Zuniga M, Madrid E, Tostes R, Fortes Z, Giachini F & San Martin S 2011 Maternal diabetes affects cell proliferation in developing rat placenta. Histology and Histopathology 26 1049-1056.