Fatty acid-induced angiogenesis in first trimester placental trophoblast cells: Possible roles of cellular fatty acid-binding proteins

Life Sciences

Volumn 93, Issue 21, 2013, Pages 755-762

  Basak, Sanjay ^a,b   Das, Mrinal K ^a   Duttaroy, Asim K ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b NATIONAL INSTITUTE OF NUTRITION   (India)

Author keywords

Angiogenesis; ANGPTL4; Docosahexaenoic acid; FABP 3; FABP 4; Fatty acids; Placentation; VEGF

Indexed keywords

ANGIOPOIETIN; CONJUGATED LINOLEIC ACID; DOCOSAHEXAENOIC ACID; ESSENTIAL FATTY ACID; FATTY ACID BINDING PROTEIN; FIBROBLAST GROWTH FACTOR; LONG CHAIN FATTY ACID; PLACENTAL GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR; VASCULOTROPIN; FABP3 PROTEIN, HUMAN; FABP4 PROTEIN, HUMAN; FATTY ACID;

ANGIOGENESIS; CANCER CELL; CELL MIGRATION; CELL PROLIFERATION; CELL STIMULATION; DIET SUPPLEMENTATION; FATTY ACID METABOLISM; FATTY ACID TRANSPORT; FETUS GROWTH; FIRST TRIMESTER PREGNANCY; HUMAN; INTRAUTERINE GROWTH RETARDATION; PLACENTA CIRCULATION; PLACENTA DEVELOPMENT; PROTEIN EXPRESSION; REVIEW; TROPHOBLAST; BIOLOGICAL MODEL; CYTOLOGY; FEMALE; METABOLISM; PHYSIOLOGY; PLACENTA; PREGNANCY; VASCULARIZATION;

FATTY ACID-BINDING PROTEINS; FATTY ACIDS; FEMALE; HUMANS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PLACENTA; PREGNANCY; PREGNANCY TRIMESTER, FIRST; TROPHOBLASTS;

EID: 84887043481     PISSN: 00243205     EISSN: 18790631     Source Type: Journal    
DOI: 10.1016/j.lfs.2013.09.024     Document Type: Review

References (87)

1. R.H. Adams, and K. Alitalo Molecular regulation of angiogenesis and lymphangiogenesis Nat Rev Mol Cell Biol 8 2007 464 478
2. L.P. Aiello, and J.S. Wong Role of vascular endothelial growth factor in diabetic vascular complications Kidney Int Suppl 77 2000 S113 S119
3. E.D. Albrecht, and G.J. Pepe Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy Int J Dev Biol 54 2010 397 408
4. D. Bagga, L. Wang, R. Farias-Eisner, J.A. Glaspy, and S.T. Reddy Differential effects of prostaglandin derived from omega-6 and omega-3 polyunsaturated fatty acids on COX-2 expression and IL-6 secretion Proc Natl Acad Sci U S A 100 2003 1751 1756
5. S. Basak, and A.K. Duttaroy Leptin induces tube formation in first-trimester extravillous trophoblast cells Eur J Obstet Gynecol Reprod Biol 2012
6. S. Basak, and A.K. Duttaroy Effects of fatty acids on angiogenic activity in the placental extravillous trophoblast cells Prostaglandins Leukot Essent Fatty Acids 88 2013 155 162
7. S. Basak, and A.K. Duttaroy cis-9, trans-11 conjugated linoleic acid stimulates expression of angiopoietin like-4 in the placental extravillous trophoblast cells Biochim Biophys Acta 1831 2013 834 843
8. M.A. Belury Dietary conjugated linoleic acid in health: physiological effects and mechanisms of action Annu Rev Nutr 22 2002 505 531
9. T. Biron-Shental, W.T. Schaiff, C.K. Ratajczak, I. Bildirici, D.M. Nelson, and Y. Sadovsky Hypoxia regulates the expression of fatty acid-binding proteins in primary term human trophoblasts Am J Obstet Gynecol 197 2007 516 [e1-6]
10. G. Calviello, F. Di Nicuolo, S. Gragnoli, E. Piccioni, S. Serini, and N. Maggiano n - 3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1alpha induction pathway Carcinogenesis 25 2004 2303 2310
11. F.M. Campbell, P.G. Bush, J.H. Veerkamp, and A.K. Dutta-Roy Detection and cellular localization of plasma membrane-associated and cytoplasmic fatty acid-binding proteins in human placenta Placenta 19 1998 409 415
12. S.E. Carlson Docosahexaenoic acid supplementation in pregnancy and lactation Am J Clin Nutr 89 2009 678S 684S
13. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
14. O. Cataltepe, M.C. Arikan, E. Ghelfi, C. Karaaslan, Y. Ozsurekci, K. Dresser, Y. Li, T.W. Smith, and S. Cataltepe Fatty Acid Binding Protein 4 Is Expressed in Distinct Endothelial and Non-endothelial Cell Populations in Glioblastoma Neuropathol Appl Neurobiol 38 5 2012 400 410
15. T. Chaiworapongsa, R. Romero, Z.A. Savasan, J.P. Kusanovic, G. Ogge, and E. Soto Maternal plasma concentrations of angiogenic/anti-angiogenic factors are of prognostic value in patients presenting to the obstetrical triage area with the suspicion of preeclampsia J Matern Fetal Neonatal Med 24 2011 1187 1207
16. J. Chen Src may be involved in the anti-cancer effect of conjugated linoleic acid. Comment on: CLA reduces breast cancer cell growth and invasion through ER and PI3K/Akt pathways Chem Biol Interact 186 2010 250 251 [author reply 2-3]
17. A.K. Duttaroy Transport of fatty acids across the human placenta: a review Prog Lipid Res 48 2009 52 61
18. A.K. Dutta-Roy Insulin mediated processes in platelets, erythrocytes and monocytes/macrophages: effects of essential fatty acid metabolism Prostaglandins Leukot Essent Fatty Acids 51 1994 385 399
19. A.K. Dutta-Roy Cellular uptake of long-chain fatty acids: role of membrane-associated fatty-acid-binding/transport proteins Cell Mol Life Sci 57 2000 1360 1372
20. A.K. Dutta-Roy Transport mechanisms for long-chain polyunsaturated fatty acids in the human placenta Am J Clin Nutr 71 2000 315S 322S
21. A.K. Dutta-Roy, N. Gopalswamy, and D.V. Trulzsch Prostaglandin E1 binds to Z protein of rat liver Eur J Biochem 162 1987 615 619
22. H. Elmasri, C. Karaaslan, Y. Teper, E. Ghelfi, M. Weng, and T.A. Ince Fatty acid binding protein 4 is a target of VEGF and a regulator of cell proliferation in endothelial cells FASEB J 23 2009 3865 3873
23. H. Elmasri, E. Ghelfi, C.W. Yu, S. Traphagen, M. Cernadas, and H. Cao Endothelial cell-fatty acid binding protein 4 promotes angiogenesis: role of stem cell factor/c-kit pathway Angiogenesis 15 2012 457 468
24. L.Y. Fang, T.Y. Wong, W.F. Chiang, and Y.L. Chen Fatty-acid-binding protein 5 promotes cell proliferation and invasion in oral squamous cell carcinoma J Oral Pathol Med 39 2010 342 348
25. S.J. Fishman, and J.B. Mulliken Hemangiomas and vascular malformations of infancy and childhood Pediatr Clin North Am 40 1993 1177 1200
26. J. Folkman, and M. Klagsbrun Angiogenic factors Science 235 1987 442 447
27. R.S. Ganu, R.A. Harris, K. Collins, and K.M. Aagaard Early origins of adult disease: approaches for investigating the programmable epigenome in humans, nonhuman primates, and rodents ILAR J 53 2012 306 321
28. O. Gealekman, A. Burkart, M. Chouinard, S.M. Nicoloro, J. Straubhaar, and S. Corvera Enhanced angiogenesis in obesity and in response to PPARgamma activators through adipocyte VEGF and ANGPTL4 production Am J Physiol Endocrinol Metab 295 2008 E1056 E1064
29. E. Ghelfi, C.W. Yu, H. Elmasri, M. Terwelp, C.G. Lee, and V. Bhandari Fatty acid binding protein 4 regulates VEGF-induced airway angiogenesis and inflammation in a transgenic mouse model: implications for asthma Am J Pathol 182 2013 1425 1433
30. T. Ghosh-Choudhury, C.C. Mandal, K. Woodruff, P. St Clair, G. Fernandes, and G.G. Choudhury Fish oil targets PTEN to regulate NFkappaB for downregulation of anti-apoptotic genes in breast tumor growth Breast Cancer Res Treat 118 2009 213 228
31. J.F. Glatz, and G.J. van der Vusse Cellular fatty acid-binding proteins: their function and physiological significance Prog Lipid Res 35 1996 243 282
32. M. Gottlicher, A. Demoz, D. Svensson, P. Tollet, R.K. Berge, and J.A. Gustafsson Structural and metabolic requirements for activators of the peroxisome proliferator-activated receptor Biochem Pharmacol 46 1993 2177 2184
33. E.A. Hamed, M.M. Zakary, R.M. Abdelal, and E.M. Abdel Moneim Vasculopathy in type 2 diabetes mellitus: role of specific angiogenic modulators J Physiol Biochem 67 2011 339 349
34. W.E. Hardman (n - 3) fatty acids and cancer therapy J Nutr 134 2004 3427S 3430S
35. I.B. Helland, L. Smith, K. Saarem, O.D. Saugstad, and C.A. Drevon Maternal supplementation with very-long-chain n - 3 fatty acids during pregnancy and lactation augments children's IQ at 4 years of age Pediatrics 111 2003 e39 e44
36. K.M. Hoagland, K.G. Maier, C. Moreno, M. Yu, and R.J. Roman Cytochrome P450 metabolites of arachidonic acid: novel regulators of renal function Nephrol Dial Transplant 16 2001 2283 2285
37. S.M. Innis Essential fatty acids in growth and development Prog Lipid Res 30 1991 39 103
38. S.M. Innis Fatty acids and early human development Early Hum Dev 83 2007 761 766
39. S.M. Innis, and R.W. Friesen Essential n - 3 fatty acids in pregnant women and early visual acuity maturation in term infants Am J Clin Nutr 87 2008 548 557
40. Y. Jin, M. Arita, Q. Zhang, D.R. Saban, S.K. Chauhan, and N. Chiang Anti-angiogenesis effect of the novel anti-inflammatory and pro-resolving lipid mediators Invest Ophthalmol Vis Sci 50 2009 4743 4752
41. G.M. Johnsen, S. Basak, M.S. Weedon-Fekjaer, A.C. Staff, and A.K. Duttaroy Docosahexaenoic acid stimulates tube formation in first trimester trophoblast cells, HTR8/SVneo Placenta 32 2011 626 632
42. K. Kajimoto, S. Takayanagi, S. Sasaki, H. Akita, and H. Harashima RNA interference-based silencing reveals the regulatory role of fatty acid-binding protein 4 in the production of IL-6 and vascular endothelial growth factor in 3T3-L1 adipocytes Endocrinology 153 2012 5629 5636
43. M. Kamiyama, A. Pozzi, L. Yang, L.M. DeBusk, R.M. Breyer, and P.C. Lin EP2, a receptor for PGE2, regulates tumor angiogenesis through direct effects on endothelial cell motility and survival Oncogene 25 2006 7019 7028
44. T. Kanayasu, I. Morita, J. Nakao-Hayashi, N. Asuwa, C. Fujisawa, and T. Ishii Eicosapentaenoic acid inhibits tube formation of vascular endothelial cells in vitro Lipids 26 1991 271 276
45. J.X. Kang, and A. Liu The role of the tissue omega-6/omega-3 fatty acid ratio in regulating tumor angiogenesis Cancer Metastasis Rev 32 2013 201 210
46. J.X. Kang, and K.H. Weylandt Modulation of inflammatory cytokines by omega-3 fatty acids Subcell Biochem 49 2008 133 143
47. H.J. Kim, C.A. Vosseler, P.C. Weber, and W. Erl Docosahexaenoic acid induces apoptosis in proliferating human endothelial cells J Cell Physiol 204 2005 881 888
48. B. Koletzko, I. Cetin, and T. Brenna Consensus statement: Dietary fat intakes for pregnant and lactating women Br J Nutr 98 2007 873 877
49. A.V. Kulkarni, S.S. Mehendale, H.R. Yadav, and S.R. Joshi Reduced placental docosahexaenoic acid levels associated with increased levels of sFlt-1 in preeclampsia Prostaglandins Leukot Essent Fatty Acids 84 2011 51 55
50. Y. Kusakari, E. Ogawa, Y. Owada, N. Kitanaka, H. Watanabe, and M. Kimura Decreased keratinocyte motility in skin wound on mice lacking the epidermal fatty acid binding protein gene Mol Cell Biochem 284 2006 183 188
51. Q. Li, Q. Zhang, M. Wang, S. Zhao, J. Ma, and N. Luo Eicosapentaenoic acid modifies lipid composition in caveolae and induces translocation of endothelial nitric oxide synthase Biochimie 89 2007 169 177
52. F. Louwen, C. Muschol-Steinmetz, J. Reinhard, A. Reitter, and J. Yuan A lesson for cancer research: placental microarray gene analysis in preeclampsia Oncotarget 3 2012 759 773
53. T. Maraldi, C. Prata, C. Caliceti, F. Vieceli Dalla Sega, L. Zambonin, and D. Fiorentini VEGF-induced ROS generation from NAD(P)H oxidases protects human leukemic cells from apoptosis Int J Oncol 36 2010 1581 1589
54. M. Massaro, E. Scoditti, M.A. Carluccio, M.C. Campana, and R. De Caterina Omega-3 fatty acids, inflammation and angiogenesis: basic mechanisms behind the cardioprotective effects of fish and fish oils Cell Mol Biol (Noisy-le-grand) 56 2010 59 82
55. N. Matesanz, G. Park, H. McAllister, W. Leahey, A. Devine, and G.E. McVeigh Docosahexaenoic acid improves the nitroso-redox balance and reduces VEGF-mediated angiogenic signaling in microvascular endothelial cells Invest Ophthalmol Vis Sci 51 2010 6815 6825
56. T. Morisada, Y. Kubota, T. Urano, T. Suda, and Y. Oike Angiopoietins and angiopoietin-like proteins in angiogenesis Endothelium 13 2006 71 79
57. A.V. Mousiolis, P. Kollia, C. Skentou, and I.E. Messinis Effects of leptin on the expression of fatty acid-binding proteins in human placental cell cultures Mol Med Rep 5 2012 497 502
58. S.I. Murota, M. Onodera, and I. Morita Regulation of angiogenesis by controlling VEGF receptor Ann N Y Acad Sci 902 2000 208 212 [discussion 12-3]
59. M.J. Murray, and B.A. Lessey Embryo implantation and tumor metastasis: common pathways of invasion and angiogenesis Semin Reprod Endocrinol 17 1999 275 290
60. J. Nevo, A. Mai, S. Tuomi, T. Pellinen, O.T. Pentikainen, and P. Heikkila Mammary-derived growth inhibitor (MDGI) interacts with integrin alpha-subunits and suppresses integrin activity and invasion Oncogene 29 2010 6452 6463
61. D. Nie, M. Lamberti, A. Zacharek, L. Li, K. Szekeres, and K. Tang Thromboxane A(2) regulation of endothelial cell migration, angiogenesis, and tumor metastasis Biochem Biophys Res Commun 267 2000 245 251
62. R. Pai, I.L. Szabo, B.A. Soreghan, S. Atay, H. Kawanaka, and A.S. Tarnawski PGE(2) stimulates VEGF expression in endothelial cells via ERK2/JNK1 signaling pathways Biochem Biophys Res Commun 286 2001 923 928
63. J. Patel, K. Landers, R.H. Mortimer, and K. Richard Regulation of hypoxia inducible factors (HIF) in hypoxia and normoxia during placental development Placenta 31 2010 951 957
64. R. Pola, E. Gaetani, A. Flex, T.R. Aprahamian, M. Bosch-Marce, and D.W. Losordo Comparative analysis of the in vivo angiogenic properties of stable prostacyclin analogs: a possible role for peroxisome proliferator-activated receptors J Mol Cell Cardiol 36 2004 363 370
65. L.P. Reynolds, and D.A. Redmer Angiogenesis in the placenta Biol Reprod 64 2001 1033 1040
66. N. Salem Jr., B. Litman, H.Y. Kim, and K. Gawrisch Mechanisms of action of docosahexaenoic acid in the nervous system Lipids 36 2001 945 959
67. M.D. Salvado, A. Alfranca, J.Z. Haeggstrom, and J.M. Redondo Prostanoids in tumor angiogenesis: therapeutic intervention beyond COX-2 Trends Mol Med 18 2012 233 243
68. P. Sapieha, A. Stahl, J. Chen, M.R. Seaward, K.L. Willett, and N.M. Krah 5-Lipoxygenase metabolite 4-HDHA is a mediator of the antiangiogenic effect of omega-3 polyunsaturated fatty acids Sci Transl Med 3 2011 69ra12
69. C.M. Scifres, B. Chen, D.M. Nelson, and Y. Sadovsky Fatty acid binding protein 4 regulates intracellular lipid accumulation in human trophoblasts J Clin Endocrinol Metab 96 2011 E1083 E1091
70. C.M. Scifres, J.M. Catov, and H. Simhan Maternal serum fatty acid binding protein 4 (FABP4) and the development of preeclampsia J Clin Endocrinol Metab 97 2012 E349 E356
71. E. Scoditti, M. Massaro, M.A. Carluccio, A. Distante, C. Storelli, and R. De Caterina PPARgamma agonists inhibit angiogenesis by suppressing PKCalpha- and CREB-mediated COX-2 expression in the human endothelium Cardiovasc Res 86 2010 302 310
72. X. Shangguan, F. Liu, H. Wang, J. He, and M. Dong Alterations in serum adipocyte fatty acid binding protein and retinol binding protein-4 in normal pregnancy and preeclampsia Clin Chim Acta 407 2009 58 61
73. A.P. Simopoulos Omega-3 fatty acids in inflammation and autoimmune diseases J Am Coll Nutr 21 2002 495 505
74. W.L. Smith The eicosanoids and their biochemical mechanisms of action Biochem J 259 1989 315 324
75. L. Spencer, C. Mann, M. Metcalfe, M. Webb, C. Pollard, and D. Spencer The effect of omega-3 FAs on tumour angiogenesis and their therapeutic potential Eur J Cancer 45 2009 2077 2086
76. A.E. Sterescu, E. Rousseau-Harsany, C. Farrell, J. Powell, M. David, and J. Dubois The potential efficacy of omega-3 fatty acids as anti-angiogenic agents in benign vascular tumors of infancy Med Hypotheses 66 2006 1121 1124
77. J. Storch, and A.E. Thumser Tissue-specific functions in the fatty acid-binding protein family J Biol Chem 285 2010 32679 32683
78. M. Szymczak, M. Murray, and N. Petrovic Modulation of angiogenesis by omega-3 polyunsaturated fatty acids is mediated by cyclooxygenases Blood 111 2008 3514 3521
79. S. Takahashi Vascular endothelial growth factor (VEGF), VEGF receptors and their inhibitors for antiangiogenic tumor therapy Biol Pharm Bull 34 2011 1785 1788
80. Z. Tian, Z.A. Zhao, X.H. Liang, X.H. Zhang, A.G. Sha, and Z.R. Zhang Expression and function of fatty acid-binding protein 4 during mouse decidualization Fertil Steril 95 2011 2749 2752 [e1-5]
81. A. Tolle, S. Suhail, M. Jung, K. Jung, and C. Stephan Fatty acid binding proteins (FABPs) in prostate, bladder and kidney cancer cell lines and the use of IL-FABP as survival predictor in patients with renal cell carcinoma BMC Cancer 11 2011 302
82. R.J. Torry, and B.J. Rongish Angiogenesis in the uterus: potential regulation and relation to tumor angiogenesis Am J Reprod Immunol 27 1992 171 179
83. D.S. Torry, H.S. Wang, T.H. Wang, M.R. Caudle, and R.J. Torry Preeclampsia is associated with reduced serum levels of placenta growth factor Am J Obstet Gynecol 179 1998 1539 1544
84. M. Tsuji, S.I. Murota, and I. Morita Docosapentaenoic acid (22:5, n - 3) suppressed tube-forming activity in endothelial cells induced by vascular endothelial growth factor Prostaglandins Leukot Essent Fatty Acids 68 2003 337 342
85. R. Uauy, D.R. Hoffman, P. Peirano, D.G. Birch, and E.E. Birch Essential fatty acids in visual and brain development Lipids 36 2001 885 895
86. S.P. Yang, I. Morita, and S.I. Murota Eicosapentaenoic acid attenuates vascular endothelial growth factor-induced proliferation via inhibiting Flk-1 receptor expression in bovine carotid artery endothelial cells J Cell Physiol 176 1998 342 349
87. Y.M. Yuan, S.H. Fang, X.D. Qian, L.Y. Liu, L.H. Xu, and W.Z. Shi Leukotriene D4 stimulates the migration but not proliferation of endothelial cells mediated by the cysteinyl leukotriene cyslt(1) receptor via the extracellular signal-regulated kinase pathway J Pharmacol Sci 109 2009 285 292