Trophoblast invasion and blood vessel remodeling are altered in a rat model of lifelong maternal obesity

Reproductive Sciences

Volumn 21, Issue 5, 2014, Pages 648-657

  Hayes, Emily K ^a   Tessier, Daniel R ^b   Percival, Michael E ^a   Holloway, Alison C ^a   Petrik, Jim J ^c   Gruslin, Andree ^d   Raha, Sandeep ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

obesity; placenta; trophoblast invasion; vascular remodeling

Indexed keywords

GELATINASE A; GELATINASE B; MONOCYTE CHEMOTACTIC PROTEIN 1; SMOOTH MUSCLE ACTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PARAMETERS; CELL INVASION; CONTROLLED STUDY; FEMALE; LIPID DIET; MATERNAL OBESITY; NONHUMAN; PLACENTA DEVELOPMENT; PREGNANCY OUTCOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TISSUE HOMOGENATE; TROPHOBLAST; ADVERSE EFFECTS; ANIMAL; CELL MOTION; COMPLICATION; DISEASE MODEL; LONGEVITY; OBESITY; PATHOLOGY; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATIONS; SPRAGUE DAWLEY RAT; VASCULAR REMODELING;

ANIMALS; CELL MOVEMENT; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; LONGEVITY; OBESITY; PREGNANCY; PREGNANCY COMPLICATIONS; RATS; RATS, SPRAGUE-DAWLEY; TROPHOBLASTS; VASCULAR REMODELING;

EID: 84898982483     PISSN: 19337191     EISSN: 19337205     Source Type: Journal    
DOI: 10.1177/1933719113508815     Document Type: Article

References (60)

1. Norman JE, Reynolds RM. The consequences of obesity and excess weight gain in pregnancy. Proc Nutr Soc. 2011 ; 70 (4). 450-456
2. Perlow JH, Morgan MA, Montgomery D, Towers CV, Porto M. Perinatal outcome in pregnancy complicated by massive obesity. Am J Obstet Gynecol. 1992 ; 167 (4 pt 1). 958-962
3. Rajasingam D, Seed PT, Briley AL, Shennan AH, Poston L. A prospective study of pregnancy outcome and biomarkers of oxidative stress in nulliparous obese women. Am J Obstet Gynecol. 2009 ; 200 (4). e391 - e399
4. Wu G, Imhoff-Kunsch B, Girard AW. Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol. 2012 ; 26 (suppl 1). 4-26
5. Hayes EK, Lechowicz A, Petrik JJ, et al. Adverse fetal and neonatal outcomes associated with a life-long high fat diet: role of altered development of the placental vasculature. PLoS One. 2012 ; 7 (3). e33370
6. Khong TY, De Wolf F, Robertson WB, Brosens I. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol. 1986 ; 93 (10). 1049-1059
7. Ball E, Bulmer JN, Ayis S, Lyall F, Robson SC. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol. 2006 ; 208 (4). 535-542
8. Knofler M. Critical growth factors and signalling pathways controlling human trophoblast invasion. Int J Dev Biol. 2010 ; 54 (2-3). 269-280
9. Vercruysse L, Caluwaerts S, Luyten C, Pijnenborg R. Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta. 2006 ; 27 (1). 22-33
10. Soares MJ, Chakraborty D, Renaud SJ, et al. Regulatory pathways controlling the endovascular invasive trophoblast cell lineage. J Reprod Dev. 2012 ; 58 (3). 283-287
11. Wallace AE, Fraser R, Cartwright JE. Extravillous trophoblast and decidual natural killer cells: a remodelling partnership. Hum Reprod Update. 2012 ; 18 (4). 458-471
12. Cartwright JE, Kenny LC, Dash PR, et al. Trophoblast invasion of spiral arteries: a novel in vitro model. Placenta. 2002 ; 23 (2-3). 232-235
13. Pijnenborg R, Vercruysse L, Hanssens M. The uterine spiral arteries in human pregnancy: facts and controversies. Placenta. 2006 ; 27 (9-10). 939-958
14. Robson A, Harris LK, Innes BA, et al. Uterine natural killer cells initiate spiral artery remodeling in human pregnancy. FASEB J. 2012 ; 26 (12). 4876-4885
15. Helwig JJ, Le Bouteiller P. Physiological smooth muscle cell apoptosis contributes to the uterine vascular remodeling in human early pregnancy. Circ Res. 2007 ; 100 (6). 754-756
16. Soares MJ, Chakraborty D, Karim Rumi MA, Konno T, Renaud SJ. Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta. 2012 ; 33 (4). 233-243
17. Schmatz M, Madan J, Marino T, Davis J. Maternal obesity: the interplay between inflammation, mother and fetus. J Perinatol. 2010 ; 30 (7). 441-446
18. Roberts KA, Riley SC, Reynolds RM, et al. Placental structure and inflammation in pregnancies associated with obesity. Placenta. 2011 ; 32 (3). 247-254
19. Bauer S, Pollheimer J, Hartmann J, Husslein P, Aplin JD, Knofler M. Tumor necrosis factor-alpha inhibits trophoblast migration through elevation of plasminogen activator inhibitor-1 in first-trimester villous explant cultures. J Clin Endocrinol Metab. 2004 ; 89 (2). 812-822
20. Jovanovic M, Stefanoska I, Radojcic L, Vicovac L. Interleukin-8 (CXCL8) stimulates trophoblast cell migration and invasion by increasing levels of matrix metalloproteinase (MMP) 2 and MMP9 and integrins alpha5 and beta1. Reproduction. 2010 ; 139 (4). 789-798
21. Pavan L, Hermouet A, Tsatsaris V, et al. Lipids from oxidized low-density lipoprotein modulate human trophoblast invasion: involvement of nuclear liver X receptors. Endocrinology. 2004 ; 145 (10). 4583-4591
22. Staff AC, Ranheim T, Henriksen T. Halvorsen B. 8-Iso-prostaglandin f(2alpha) reduces trophoblast invasion and matrix metalloproteinase activity. Hypertension. 2000 ; 35 (6). 1307-1313
23. Jovanovic M, Vicovac L. Interleukin-6 stimulates cell migration, invasion and integrin expression in HTR-8/SVneo cell line. Placenta. 2009 ; 30 (4). 320-328
24. Nguyen Dinh Cat A, Briones AM, Callera GE, et al. Adipocyte-derived factors regulate vascular smooth muscle cells through mineralocorticoid and glucocorticoid receptors. Hypertension. 2011 ; 58 (3). 479-488
25. Caluwaerts S, Vercruysse L, Luyten C, Pijnenborg R. Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta. 2005 ; 26 (7). 574-584
26. Rosario GX, Konno T, Soares MJ. Maternal hypoxia activates endovascular trophoblast cell invasion. Dev Biol. 2008 ; 314 (2). 362-375
27. Geusens N, Verlohren S, Luyten C, et al. Endovascular trophoblast invasion, spiral artery remodelling and uteroplacental haemodynamics in a transgenic rat model of pre-eclampsia. Placenta. 2008 ; 29 (7). 614-623
28. Geusens N, Hering L, Verlohren S, et al. Changes in endovascular trophoblast invasion and spiral artery remodelling at term in a transgenic preeclamptic rat model. Placenta. 2010 ; 31 (4). 320-326
29. Verlohren S, Geusens N, Morton J, et al. Inhibition of trophoblast-induced spiral artery remodeling reduces placental perfusion in rat pregnancy. Hypertension. 2010 ; 56 (2). 304-310
30. Robertshaw HA, Raha S, Kaczor JJ, Tarnopolsky MA. Increased PFK activity and GLUT4 protein content in McArdle's disease. Muscle Nerve. 2008 ; 37 (4). 431-437
31. Luo J, Qiao F, Yin X. Impact of silencing MMP9 gene on the biological behaviors of trophoblasts. J Huazhong Univ Sci Technolog Med Sci. 2011 ; 31 (2). 241-245
32. Harris LK, Keogh RJ, Wareing M, et al. Invasive trophoblasts stimulate vascular smooth muscle cell apoptosis by a fas ligand-dependent mechanism. Am J Pathol. 2006 ; 169 (5). 1863-1874
33. McCarthy NJ, Bennett MR. The regulation of vascular smooth muscle cell apoptosis. Cardiovasc Res. 2000 ; 45 (3). 747-755
34. Whitley GS, Cartwright JE. Cellular and molecular regulation of spiral artery remodelling: lessons from the cardiovascular field. Placenta. 2010 ; 31 (6). 465-474
35. Harris LK, Keogh RJ, Wareing M, et al. BeWo cells stimulate smooth muscle cell apoptosis and elastin breakdown in a model of spiral artery transformation. Hum Reprod. 2007 ; 22 (11). 2834-2841
36. Wood IS, Stezhka T, Trayhurn P. Modulation of adipokine production, glucose uptake and lactate release in human adipocytes by small changes in oxygen tension. Pflugers Arch. 2011 ; 462 (3). 469-477
37. Bulmer JN, Innes BA, Levey J, Robson SC, Lash GE. The role of vascular smooth muscle cell apoptosis and migration during uterine spiral artery remodeling in normal human pregnancy. FASEB J. 2012 ; 26 (7). 2975-2985
38. Chakraborty D, Rumi MA, Konno T, Soares MJ. Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc Natl Acad Sci U S A. 2011 ; 108 (39). 16295-16300
39. Bourque SL, Dolinsky VW, Dyck JR, Davidge ST. Maternal resveratrol treatment during pregnancy improves adverse fetal outcomes in a rat model of severe hypoxia. Placenta. 2012 ; 33 (5). 449-452
40. Staun-Ram E, Goldman S, Gabarin D, Shalev E. Expression and importance of matrix metalloproteinase 2 and 9 (MMP-2 and -9) in human trophoblast invasion. Reprod Biol Endocrinol. 2004 ; 2: 59
41. Isaka K, Usuda S, Ito H, et al. Expression and activity of matrix metalloproteinase 2 and 9 in human trophoblasts. Placenta. 2003 ; 24 (1). 53-64
42. Naruse K, Lash GE, Innes BA, et al. 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. 2009 ; 24 (3). 553-561
43. Allott EH, Lysaght J, Cathcart MC, et al. MMP9 expression in oesophageal adenocarcinoma is upregulated with visceral obesity and is associated with poor tumour differentiation. Mol Carcinog. 2011 ; 52 (2). 144-154
44. Soto-Guzman A, Navarro-Tito N, Castro-Sanchez L, Martinez-Orozco R, Salazar EP. Oleic acid promotes MMP-9 secretion and invasion in breast cancer cells. Clin Exp Metastasis. 2010 ; 27 (7). 505-515
45. Mu H, Ohashi R, Yan S, et al. Adipokine resistin promotes in vitro angiogenesis of human endothelial cells. Cardiovasc Res. 2006 ; 70 (1). 146-157
46. Na KH, Lee HJ, Choi JH, et al. Dynamic alterations in integrin alpha4 expression by hypoxia are involved in trophoblast invasion during early implantation. J Cell Biochem. 2012 ; 113 (2). 685-694
47. Graham CH, Hawley TS, Hawley RG, et al. Establishment and characterization of first trimester human trophoblast cells with extended lifespan. Exp Cell Res. 1993 ; 206 (2). 204-211
48. Lash GE, Hornbuckle J, Brunt A, et al. Effect of low oxygen concentrations on trophoblast-like cell line invasion. Placenta. 2007 ; 28 (5-6). 390-398
49. Lash GE, Cartwright JE, Whitley GS, Trew AJ, Baker PN. The effects of angiogenic growth factors on extravillous trophoblast invasion and motility. Placenta. 1999 ; 20 (8). 661-667
50. Hu Y, Eastabrook G, Tan R, MacCalman CD, Dutz JP, von Dadelszen P. Decidual NK cell-derived conditioned medium enhances capillary tube and network organization in an extravillous cytotrophoblast cell line. Placenta. 2010 ; 31 (3). 213-221
51. Fraser R, Whitley GS, Johnstone AP, et al. Impaired decidual natural killer cell regulation of vascular remodelling in early human pregnancies with high uterine artery resistance. J Pathol. 2012 ; 228 (3). 322-332
52. Lolmede K, Durand de Saint Front V, Galitzky J, Lafontan M, Bouloumie A. Effects of hypoxia on the expression of proangiogenic factors in differentiated 3T3-F442A adipocytes. Int J Obes Relat Metab Disord. 2003 ; 27 (10). 1187-1195
53. Kim CS, Park HS, Kawada T, et al. Circulating levels of MCP-1 and IL-8 are elevated in human obese subjects and associated with obesity-related parameters. Int J Obes (Lond). 2006 ; 30 (9). 1347-1355
54. Frias AE, Morgan TK, Evans AE, et al. Maternal high-fat diet disturbs uteroplacental hemodynamics and increases the frequency of stillbirth in a nonhuman primate model of excess nutrition. Endocrinology. 2011 ; 152 (6). 2456-2464
55. Kovo M, Schreiber L, Ben-Haroush A, Shor S, Golan A, Bar J. Intrapartum fever at term: clinical characteristics and placental pathology. J Matern Fetal Neonatal Med. 2012 ; 25 (8). 1273-1277
56. Bar J, Schreiber L, Saruhanov E, Ben-Haroush A, Golan A, Kovo M. Placental histopathological findings in obese and nonobese women with complicated and uncomplicated pregnancies. Arch Gynecol Obstet. 2012 ; 286 (6). 1343-1347
57. Burton GJ, Woods AW, Jauniaux E, Kingdom JC. Rheological and physiological consequences of conversion of the maternal spiral arteries for uteroplacental blood flow during human pregnancy. Placenta. 2009 ; 30 (6). 473-482
58. Sivitz WI, Wayson SM, Bayless ML, Sinkey CA, Haynes WG. Obesity impairs vascular relaxation in human subjects: hyperglycemia exaggerates adrenergic vasoconstriction arterial dysfunction in obesity and diabetes. J Diabetes Complications. 2007 ; 21 (3). 149-157
59. Myers J, Hall C, Wareing M, Gillham J, Baker P. The effect of maternal characteristics on endothelial-dependent relaxation of myometrial arteries. Eur J Obstet Gynecol Reprod Biol. 2006 ; 124 (2). 158-163
60. Whitley GS, Cartwright JE. Trophoblast-mediated spiral artery remodelling: a role for apoptosis. J Anat. 2009 ; 215 (1). 21-26