The lipid transfer protein StarD7: Structure, function, and regulation

International Journal of Molecular Sciences

Volumn 14, Issue 3, 2013, Pages 6170-6186

  Flores Martin, Jésica ^a   Rena, Viviana ^a   Angeletti, Sofía ^a   Panzetta Dutari, Graciela M ^a   Genti Raimondi, Susana ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

catenin; ABCG2; Cell migration; Cell proliferation; SF 1; StarD7; START domain

Indexed keywords

BETA CATENIN; BREAST CANCER RESISTANCE PROTEIN; CYCLIC AMP; LIPID TRANSFER PROTEIN; PROTEIN STARD7; STEROIDOGENIC FACTOR 1; TRANSCRIPTION FACTOR 7 LIKE 2; UNCLASSIFIED DRUG;

CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TROPHOBLAST;

MAMMALIA;

EID: 84875497440     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms14036170     Document Type: Review

References (93)

1. Prinz, W.A. Lipid trafficking sans vesicles: Where, why, how? Cell 2010, 143, 870-874.
2. Holthuis, J.C.; Levine, T.P. Lipid traffic: Floppy drives and a superhighway. Nat. Rev. Mol. Cell Biol. 2005, 6, 209-220.
3. Soccio, R.E.; Breslow, J.L. StAR-Related lipid transfer (START) proteins: Mediators of intracellular lipid metabolism. J. Biol. Chem. 2003, 278, 22183-22186.
4. Thorsell, A.G.; Lee, W.H.; Persson, C.; Siponen, M.I.; Nilsson, M.; Busam, R.D.; Kotenyova, T.; Schuler, H.; Lehtio, L. Comparative structural analysis of lipid binding START domains. PLoS One 2011, 6, e19521.
5. Lee, H.; Li, Z.; Silkov, A.; Fischer, M.; Petrey, D.; Honig, B.; Murray, D. High-Throughput computational structure-based characterization of protein families: START domains and implications for structural genomics. J. Struct. Funct. Genomics 2010, 11, 51-59.
6. Ponting, C.P.; Aravind, L. START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 1999, 24, 130-132.
7. Tsujishita, Y.; Hurley, J.H. Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Biol. 2000, 7, 408-414.
8. Barros, M.H.; Johnson, A.; Gin, P.; Marbois, B.N.; Clarke, C.F.; Tzagoloff, A. The Saccharomyces cerevisiae COQ10 gene encodes a START domain protein required for function of coenzyme Q in respiration. J. Biol. Chem. 2005, 280, 42627-42635.
9. Mercier, K.A.; Mueller, G.A.; Acton, T.B.; Xiao, R.; Montelione, G.T.; Powers, R. (1)H, (13)C, and (15)N NMR assignments for the Bacillus subtilis yndB START domain. Biomol. NMR Assign. 2009, 3, 191-194.
10. Schrick, K.; Nguyen, D.; Karlowski, W.M.; Mayer, K.F. START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 2004, 5, R41.
11. Iyer, L.M.; Koonin, E.V.; Aravind, L. Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins 2001, 43, 134-144.
12. Alpy, F.; Tomasetto, C. Give lipids a START: The StAR-related lipid transfer (START) domain in mammals. J. Cell Sci. 2005, 118, 2791-2801.
13. Stocco, D.M. StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 2001, 63, 193-213.
14. Miller, W.L.; Bose, H.S. Early steps in steroidogenesis: Intracellular cholesterol trafficking. J. Lipid Res. 2011, 52, 2111-2135.
15. Romanowski, M.J.; Soccio, R.E.; Breslow, J.L.; Burley, S.K. Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain. Proc. Natl. Acad. Sci. USA 2002, 99, 6949-6954.
16. Roderick, S.L.; Chan, W.W.; Agate, D.S.; Olsen, L.R.; Vetting, M.W.; Rajashankar, K.R.; Cohen, D.E. Structure of human phosphatidylcholine transfer protein in complex with its ligand. Nat. Struct. Biol. 2002, 9, 507-511.
17. Chan, W.W.; Roderick, S.L.; Cohen, D.E. Human phosphatidylcholine transfer protein: Purification, crystallization and preliminary X-ray diffraction data. Biochim. Biophys. Acta 2002, 1596, 1-5.
18. Li, H.; Fung, K.L.; Jin, D.Y.; Chung, S.S.; Ching, Y.P.; Ng, I.O.; Sze, K.H.; Ko, B.C.; Sun, H. Solution structures, dynamics, and lipid-binding of the sterile alpha-motif domain of the deleted in liver cancer 2. Proteins 2007, 67, 1154-1166.
19. Kudo, N.; Kumagai, K.; Matsubara, R.; Kobayashi, S.; Hanada, K.; Wakatsuki, S.; Kato, R. Crystal structures of the CERT START domain with inhibitors provide insights into the mechanism of ceramide transfer. J. Mol. Biol. 2010, 396, 245-251.
20. Lavigne, P.; Najmanivich, R.; Lehoux, J.G. Mammalian StAR-related lipid transfer (START) domains with specificity for cholesterol: Structural conservation and mechanism of reversible binding. Subcell. Biochem. 2010, 51, 425-437.
21. Chen, D.; Latham, J.; Zhao, H.; Bisoffi, M.; Farelli, J. Dunaway-Mariano, D. Human brown fat inducible thioesterase variant 2 cellular localization and catalytic function. Biochemistry 2012, 51, 6990-6999.
22. Durand, S.; Angeletti, S.; Genti-Raimondi, S. GTT1/StarD7, a novel phosphatidylcholine transfer protein-like highly expressed in gestational trophoblastic tumour: Cloning and characterization. Placenta 2004, 25, 37-44.
23. Cohen, D.E.; Green, R.M.; Wu, M.K.; Beier, D.R. Cloning, tissue-specific expression, gene structure and chromosomal localization of human phosphatidylcholine transfer protein. Biochim. Biophys. Acta 1999, 1447, 265-270.
24. Angeletti, S.; Rena, V.; Nores, R.; Fretes, R.; Panzetta-Dutari, G.M.; Genti-Raimondi, S. Expression and localization of StarD7 in trophoblast cells. Placenta 2008, 29, 396-404.
25. Leman, E.S.; Magheli, A.; Yong, K.M.; Netto, G.; Hinz, S.; Getzenberg, R.H. Identification of nuclear structural protein alterations associated with seminomas. J. Cell. Biochem. 2009, 108, 1274-1279.
26. Horibata, Y.; Sugimoto, H. StarD7 mediates the intracellular trafficking of phosphatidylcholine to mitochondria. J. Biol. Chem. 2010, 285, 7358-7365.
27. Kim, W.; Bennett, E.J.; Huttlin, E.L.; Guo, A.; Li, J.; Possemato, A.; Sowa, M.E.; Rad, R.; Rush, J.; Comb, M.J.; et al. Systematic and quantitative assessment of the ubiquitin-modified proteome. Mol. Cell 2011, 44, 325-340.
28. Hornbeck, P.V.; Kornhauser, J.M.; Tkachev, S.; Zhang, B.; Skrzypek, E.; Murray, B.; Latham, V.; Sullivan, M. PhosphoSitePlus: A comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res. 2012, 40, D261-D270.
29. Bose, H.S.; Whittal, R.M.; Ran, Y.; Bose, M.; Baker, B.Y.; Miller, W.L. StAR-Like activity and molten globule behavior of StARD6, a male germ-line protein. Biochemistry 2008, 47, 2277-2288.
30. Rodriguez, M.; Li, S.S.; Harper, J.W.; Songyang, Z. An oriented peptide array library (OPAL) strategy to study protein-protein interactions. J. Biol. Chem. 2004, 279, 8802-8807.
31. Guo, L.; Ying, W.; Zhang, J.; Yuan, Y.; Qian, X.; Wang, J.; Yang, X.; He, F. Tandem affinity purification and identification of the human TSC1 protein complex. Acta. Biochim. Biophys. Sin. (Shanghai) 2010, 42, 266-273.
32. Angeletti, S.; Maggio, B.; Genti-Raimondi, S. Surface activity and interaction of StarD7 with phospholipid monolayers. Biochem. Biophys. Res. Commun. 2004, 314, 181-185.
33. Angeletti, S.; Sanchez, J.M.; Chamley, L.W.; Genti-Raimondi, S.; Perillo, M.A. StarD7 behaves as a fusogenic protein in model and cell membrane bilayers. Biochim. Biophys. Acta 2011, 1818, 425-433.
34. Penno, A.; Hackenbroich, G.; Thiele, C. Phospholipids and lipid droplets. Biochim. Biophys. Acta 2013, 1831, 589-594.
35. Voelker, D.R. Genetic and biochemical analysis of non-vesicular lipid traffic. Annu. Rev. Biochem. 2009, 78, 827-856.
36. Zhu, X.M.; Han, T.; Sargent, I.L.; Yin, G.W.; Yao, Y.Q. Differential expression profile of microRNAs in human placentas from preeclamptic pregnancies vs normal pregnancies. Am. J. Obstet. Gynecol. 2009, 200, 1-7.
37. Polyak, K.; Hu, M. Do myoepithelial cells hold the key for breast tumor progression? J. Mammary Gland Biol. Neoplasia 2005, 10, 231-247.
38. Jelinek, D.F.; Tschumper, R.C.; Stolovitzky, G.A.; Iturria, S.J.; Tu, Y.; Lepre, J.; Shah, N.; Kay, N.E. Identification of a global gene expression signature of B-chronic lymphocytic leukemia. Mol. Cancer Res. 2003, 1, 346-361.
39. Wiese, A.H.; Auer, J.; Lassmann, S.; Nahrig, J.; Rosenberg, R.; Hofler, H.; Ruger, R.; Werner, M. Identification of gene signatures for invasive colorectal tumor cells. Cancer Detect. Prev. 2007, 31, 282-295.
40. Ikeda, Y.; Tanji, E.; Makino, N.; Kawata, S.; Furukawa, T. MicroRNAs associated with mitogen-activated protein kinase in human pancreatic cancer. Mol. Cancer Res. 2011, 10, 259-269.
41. Xi, Y.; Nakajima, G.; Schmitz, J.C.; Chu, E.; Ju, J. Multi-Level gene expression profiles affected by thymidylate synthase and 5-fluorouracil in colon cancer. BMC Genomics 2006, 7, 68.
42. Wright, H.J.; Matthews, J.B.; Chapple, I.L.; Ling-Mountford, N.; Cooper, P.R. Periodontitis associates with a type 1 IFN signature in peripheral blood neutrophils. J. Immunol. 2008, 181, 5775-5784.
43. Kadl, A.; Meher, A.K.; Sharma, P.R.; Lee, M.Y.; Doran, A.C.; Johnstone, S.R.; Elliott, M.R.; Gruber, F.; Han, J.; Chen, W.; et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ. Res. 2010, 107, 737-746.
44. Selman, M.; Pardo, A.; Barrera, L.; Estrada, A.; Watson, S.R.; Wilson, K.; Aziz, N.; Kaminski, N.; Zlotnik, A. Gene expression profiles distinguish idiopathic pulmonary fibrosis from hypersensitivity pneumonitis. Am. J. Respir. Crit. Care Med. 2006, 173, 188-198.
45. Yung, C.K.; Halperin, V.L.; Tomaselli, G.F.; Winslow, R.L. Gene expression profiles in end-stage human idiopathic dilated cardiomyopathy: altered expression of apoptotic and cytoskeletal genes. Genomics 2004, 83, 281-297.
46. Jerez-Timaure, N.C.; Kearney, F.; Simpson, E.B.; Eisen, E.J.; Pomp, D. Characterization of QTL with major effects on fatness and growth on mouse chromosome 2. Obes. Res. 2004, 12, 1408-1420.
47. De Wilde, J.; Mohren, R.; van den Berg, S.; Boekschoten, M.; Dijk, K.W.; de Groot, P.; Muller, M.; Mariman, E.; Smit, E. Short-Term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol. Genomics 2008, 32, 360-369.
48. MacLaren, R.; Cui, W.; Simard, S.; Cianflone, K. Influence of obesity and insulin sensitivity on insulin signaling genes in human omental and subcutaneous adipose tissue. J. Lipid Res. 2008, 49, 308-323.
49. Sokolovic, M.; Sokolovic, A.; van Roomen, C.P.; Gruber, A.; Ottenhoff, R.; Scheij, S.; Hakvoort, T.B.; Lamers, W.H.; Groen, A.K. Unexpected effects of fasting on murine lipid homeostasis-Transcriptomic and lipid profiling. J. Hepatol. 2010, 52, 737-744.
50. Rome, S.; Clement, K.; Rabasa-Lhoret, R.; Loizon, E.; Poitou, C.; Barsh, G.S.; Riou, J.P.; Laville, M.; Vidal, H. Microarray profiling of human skeletal muscle reveals that insulin regulates approximately 800 genes during a hyperinsulinemic clamp. J. Biol. Chem. 2003, 278, 18063-18068.
51. Kostek, M.C.; Chen, Y.W.; Cuthbertson, D.J.; Shi, R.; Fedele, M.J.; Esser, K.A.; Rennie, M.J. Gene expression responses over 24 h to lengthening and shortening contractions in human muscle: Major changes in CSRP3, MUSTN1, SIX1, and FBXO32. Physiol. Genomics 2007, 31, 42-52.
52. Park, C.C.; Gale, G.D.; de Jong, S.; Ghazalpour, A.; Bennett, B.J.; Farber, C.R.; Langfelder, P.; Lin, A.; Khan, A.H.; Eskin, E.; et al. Gene networks associated with conditional fear in mice identified using a systems genetics approach. BMC Syst. Biol. 2011, 5, 43.
53. Wada, K.; Howard, J.T.; McConnell, P.; Whitney, O.; Lints, T.; Rivas, M.V.; Horita, H.; Patterson, M.A.; White, S.A.; Scharff, C.; et al. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc. Natl. Acad. Sci. USA 2006, 103, 15212-15217.
54. Lee, H.S.; Park, M.H.; Yang, S.J.; Park, K.C.; Kim, N.S.; Kim, Y.S.; Kim, D.I.; Yoo, H.S.; Choi, E.J.; Yeom, Y.I. Novel candidate targets of Wnt/beta-catenin signaling in hepatoma cells. Life Sci. 2007, 80, 690-698.
55. Fuerer, C.; Nusse, R.; Ten Berge, D. Wnt signalling in development and disease. Max delbruck center for molecular medicine meeting on wnt signaling in development and disease. EMBO Rep. 2008, 9, 134-138.
56. Sonderegger, S.; Husslein, H.; Leisser, C.; Knofler, M. Complex expression pattern of Wnt ligands and frizzled receptors in human placenta and its trophoblast subtypes. Placenta 2007, 28, S97-S102.
57. Pollheimer, J.; Loregger, T.; Sonderegger, S.; Saleh, L.; Bauer, S.; Bilban, M.; Czerwenka, K.; Husslein, P.; Knofler, M. Activation of the canonical wingless/T-cell factor signaling pathway promotes invasive differentiation of human trophoblast. Am. J. Pathol. 2006, 168, 1134-1147.
58. Getsios, S.; Chen, G.T.; MacCalman, C.D. Regulation of beta-catenin mRNA and protein levels in human villous cytotrophoblasts undergoing aggregation and fusion in vitro: Correlation with E-cadherin expression. J. Reprod. Fertil. 2000, 119, 59-68.
59. Wong, N.C.; Novakovic, B.; Weinrich, B.; Dewi, C.; Andronikos, R.; Sibson, M.; Macrae, F.; Morley, R.; Pertile, M.D.; Craig, J.M.; et al. Methylation of the adenomatous polyposis coli (APC) gene in human placenta and hypermethylation in choriocarcinoma cells. Cancer Lett. 2008, 268, 56-62.
60. Hewitt, D.P.; Mark, P.J.; Dharmarajan, A.M.; Waddell, B.J. Placental expression of secreted frizzled related protein-4 in the rat and the impact of glucocorticoid-induced fetal and placental growth restriction. Biol. Reprod. 2006, 75, 75-81.
61. Sonderegger, S.; Haslinger, P.; Sabri, A.; Leisser, C.; Otten, J.V.; Fiala, C.; Knofler, M. Wingless (Wnt)-3A induces trophoblast migration and matrix metalloproteinase-2 secretion through canonical Wnt signaling and protein kinase B/AKT activation. Endocrinology 2010, 151, 211-220.
62. Sonderegger, S.; Pollheimer, J.; Knofler, M. Wnt signalling in implantation, decidualisation and placental differentiation-Review. Placenta 2010, 31, 839-847.
63. Fitzgerald, J.S.; Germeyer, A.; Huppertz, B.; Jeschke, U.; Knofler, M.; Moser, G.; Scholz, C.; Sonderegger, S.; Toth, B.; Markert, U.R. Governing the invasive trophoblast: Current aspects on intra-and extracellular regulation. Am. J. Reprod. Immunol. 2010, 63, 492-505.
64. Rena, V.; Angeletti, S.; Panzetta-Dutari, G.; Genti-Raimondi, S. Activation of beta-catenin signalling increases StarD7 gene expression in JEG-3 cells. Placenta 2009, 30, 876-883.
65. Morohashi, K.; Hatano, O.; Nomura, M.; Takayama, K.; Hara, M.; Yoshii, H.; Takakusu, A.; Omura, T. Function and distribution of a steroidogenic cell-specific transcription factor, Ad4BP. J. Steroid Biochem. Mol. Biol. 1995, 53, 81-88.
66. Parker, K.L.; Rice, D.A.; Lala, D.S.; Ikeda, Y.; Luo, X.; Wong, M.; Bakke, M.; Zhao, L.; Frigeri, C.; Hanley, N.A.; et al. Steroidogenic factor 1: An essential mediator of endocrine development. Recent Prog. Horm. Res. 2002, 57, 19-36.
67. Lavoie, H.A.; King, S.R. Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B. Exp. Biol. Med. (Maywood) 2009, 234, 880-907.
68. Mulholland, D.J.; Dedhar, S.; Coetzee, G.A.; Nelson, C.C. Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know? Endocr. Rev. 2005, 26, 898-915.
69. Rena, V.; Flores-Martín, J.; Angeletti, S.; Panzetta-Dutari, G.; Genti-Raimondi, S. StarD7 gene expression in trophoblast cells: Contribution of SF-1 and Wnt-b-catenin signalling. Mol. Endocrinol. 2011, 8, 1364-1375.
70. Mizusaki, H.; Kawabe, K.; Mukai, T.; Ariyoshi, E.; Kasahara, M.; Yoshioka, H.; Swain, A.; Morohashi, K. Dax-1 (dosage-sensitive sex reversal-adrenal hypoplasia congenita critical region on the X chromosome, gene 1) gene transcription is regulated by wnt4 in the female developing gonad. Mol. Endocrinol. 2003, 17, 507-519.
71. Schinner, S.; Willenberg, H.S.; Krause, D.; Schott, M.; Lamounier-Zepter, V.; Krug, A.W.; Ehrhart-Bornstein, M.; Bornstein, S.R.; Scherbaum, W.A. Adipocyte-Derived products induce the transcription of the StAR promoter and stimulate aldosterone and cortisol secretion from adrenocortical cells through the Wnt-signaling pathway. Int. J. Obes. (Lond.) 2007, 31, 864-870.
72. Parakh, T.N.; Hernandez, J.A.; Grammer, J.C.; Weck, J.; Hunzicker-Dunn, M.; Zeleznik, A.J.; Nilson, J.H. Follicle-Stimulating hormone/cAMP regulation of aromatase gene expression requires beta-catenin. Proc. Natl. Acad. Sci. USA 2006, 103, 12435-12440.
73. Gardner, S.; Stavrou, E.; Rischitor, P.E.; Faccenda, E.; Pawson, A.J. Targeting mediators of Wnt signalling pathways by GnRH in gonadotropes. J. Mol. Endocrinol. 2010, 44, 195-201.
74. Hossain, A.; Saunders, G.F. Synergistic cooperation between the beta-catenin signaling pathway and steroidogenic factor 1 in the activation of the Mullerian inhibiting substance type II receptor. J. Biol. Chem. 2003, 278, 26511-26516.
75. Salisbury, T.B.; Binder, A.K.; Nilson, J.H. Welcoming beta-catenin to the gonadotropin-releasing hormone transcriptional network in gonadotropes. Mol. Endocrinol. 2008, 22, 1295-1303.
76. Gummow, B.M.; Winnay, J.N.; Hammer, G.D. Convergence of Wnt signaling and steroidogenic factor-1 (SF-1) on transcription of the rat inhibin alpha gene. J. Biol. Chem. 2003, 278, 26572-26579.
77. Clevers, H.; Nusse, R. Wnt/beta-catenin signaling and disease. Cell 2012, 149, 1192-1205.
78. Shishova, E.Y.; Stoll, J.M.; Ersoy, B.A.; Shrestha, S.; Scapa, E.F.; Li, Y.; Niepel, M.W.; Su, Y.; Jelicks, L.A.; Stahl, G.L.; et al. Genetic ablation or chemical inhibition of phosphatidylcholine transfer protein attenuates diet-induced hepatic glucose production. Hepatology 2011, 54, 664-674.
79. Ullmannova, V.; Popescu, N.C. Expression profile of the tumor suppressor genes DLC-1 and DLC-2 in solid tumors. Int. J. Oncol. 2006, 29, 1127-1132.
80. Durkin, M.E.; Ullmannova, V.; Guan, M.; Popescu, N.C. Deleted in liver cancer 3 (DLC-3), a novel Rho GTPase-activating protein, is downregulated in cancer and inhibits tumor cell growth. Oncogene 2007, 26, 4580-4589.
81. Olayioye, M.A.; Hoffmann, P.; Pomorski, T.; Armes, J.; Simpson, R.J.; Kemp, B.E.; Lindeman, G.J.; Visvader, J.E. The phosphoprotein StarD10 is overexpressed in breast cancer and cooperates with ErbB receptors in cellular transformation. Cancer Res. 2004, 64, 3538-3544.
82. Al-Khan, A.; Aye, I.L.; Barsoum, I.; Borbely, A.; Cebral, E.; Cerchi, G.; Clifton, V.L.; Collins, S.; Cotechini, T.; Davey, A.; et al. IFPA Meeting 2010 Workshops Report II: Placental pathology; trophoblast invasion; fetal sex; parasites and the placenta; decidua and embryonic or fetal loss; trophoblast differentiation and syncytialisation. Placenta 2011, 32, S90-S99.
83. Flores-Martin, J.; Rena, V.; Marquez, S.; Panzetta-Dutari, G.M.; Genti-Raimondi, S. StarD7 knockdown modulates ABCG2 expression, cell migration, proliferation, and differentiation of human choriocarcinoma JEG-3 cells. PLoS One 2012, 7, e44152.
84. Robey, R.W.; To, K.K.; Polgar, O.; Dohse, M.; Fetsch, P.; Dean, M.; Bates, S.E. ABCG2: A perspective. Adv. Drug Deliv. Rev. 2009, 61, 3-13.
85. Ni, Z.; Mao, Q., ATP-Binding cassette efflux transporters in human placenta. Curr. Pharm. Biotechnol. 2011, 12, 674-685.
86. Vahakangas, K.; Myllynen, P. Drug transporters in the human blood-placental barrier. Br. J. Pharmacol. 2009, 158, 665-678.
87. Quazi, F.; Molday, R.S. Lipid transport by mammalian ABC proteins. Essays Biochem. 2011, 50, 265-290.
88. Evseenko, D.A.; Paxton, J.W.; Keelan, J.A. The xenobiotic transporter ABCG2 plays a novel role in differentiation of trophoblast-like BeWo cells. Placenta 2007, 28, S116-S120.
89. Evseenko, D.A.; Paxton, J.W.; Keelan, J.A. ABC drug transporter expression and functional activity in trophoblast-like cell lines and differentiating primary trophoblast. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290, R1357-R1365.
90. Evseenko, D.A.; Murthi, P.; Paxton, J.W.; Reid, G.; Emerald, B.S.; Mohankumar, K.M.; Lobie, P.E.; Brennecke, S.P.; Kalionis, B.; Keelan, J.A. The ABC transporter BCRP/ABCG2 is a placental survival factor, and its expression is reduced in idiopathic human fetal growth restriction. FASEB J. 2007, 21, 3592-3605.
91. Flores-Martín, J.; Rena, V.; Márquez, S.; Panzetta-Dutari, G.M.; Genti-Raimondi, S. StarD7 siRNA modulates ABCG2 expression, cell migration and proliferation in epithelial cell lines. Biocell 2012, 66, 36.
92. Vaitukaitis, J.L.; Ebersole, E.R. Evidence for altered synthesis of human chorionic gonadotropin in gestational trophoblastic tumors. J. Clin. Endocrinol. Metab. 1976, 42, 1048-1055.
93. Kharfi, A.; Giguere, Y.; de Grandpre, P.; Moutquin, J.M.; Forest, J.C. Human chorionic gonadotropin (hCG) may be a marker of systemic oxidative stress in normotensive and preeclamptic term pregnancies. Clin. Biochem. 2005, 38, 717-721.