medigraphic.com
SPANISH

TIP Revista Especializada en Ciencias Químico-Biológicas

ISSN 2395-8723 (Electronic)
ISSN 1405-888X (Print)
TIP Revista Especializada en Ciencias Químico-Biológicas
  • Contents
  • View Archive
  • Information
    • General Information        
    • Directory
  • Publish
    • Instructions for authors        
  • medigraphic.com
    • Home
    • Journals index            
    • Register / Login
  • Mi perfil

2019, Number 1

<< Back Next >>

TIP Rev Esp Cienc Quim Biol 2019; 22 (1)

General aspects of cholesterol transport in the steroidogenesis of the human placenta

Olvera-Sánchez S, Esparza-Perusquía M, Flores-Herrera O, Urban-Sosa VA, Martínez F
Full text How to cite this article

Language: Spanish
References: 73
Page: 1-9
PDF size: 399.65 Kb.


Key words:

human placenta, lipoprotein receptors, mitochondria, cholesterol transport, steroidogenesis, contact sites.

ABSTRACT

The human placenta requires cholesterol to synthesize the progesterone that maintains the relationship between the fetus and the mother, which allows it to successfully conclude pregnancy. The placenta incorporates cholesterol through the LDL obtained from the maternal blood stream by a mechanism of endocytosis. Endosomes formed by this process degrade the LDL, bind several proteins forming the late endosomes and releasing the cholesterol to syncytiotrophoblast mitochondria to transform it into pregnenolone and then, into progesterone. The soluble attachment proteins denominated SNARE participates in the transport of cholesterol in specific contact sites where the mitochondrial proteins responsible for steroidogenesis are located.


REFERENCES

  1. Adams, J.M. & Cory, S. (2001). Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci., 26, 61-66. DOI: 10.1016/S0968-0004(00)01740-0.

  2. Adams, V., Bosch, W., Schelege. J., Wallimann, T. & Brdiczka, D. (1989). Further characterization of contact sites from mitochondria of different tissues: topology of peripheral kinases. Biochim. Biophys. Acta, 981(2), 213-225. DOI: 10.1016/0005-2736(89)90031-X.

  3. Alpy, F. & Tomasetto, C. (2014). START ships lipids across interorganelle space. Biochimie, 96, 85-95. DOI: 10.1016/j.biochi.2013.09.015.

  4. Alpy, F., Rousseau, A., Schwab, Y., Legueux, F., Stoll, I., Wendling, C., Spiegelhalter, C., Kessler, P., Mathelin, C., Rio, M.C., Levine, T.P. & Tomasetto, C. (2013). STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J. Cell Sci., 126, 5500–5512. DOI: 10.1242/jcs.139295.

  5. Ashary, N., Tiwari, A. & Modi, D. (2018). Embryo Implantation: Warin times of love. Endocrinology, 159, 1188–1198. DOI: 10.1210/en.2017-03082.

  6. Baardman, M.E., Kerstjens-Frederikse, W.S., Berger, R.M.F., Bakker, M.K., Hofstra, R.M.W. & Plösch, T. (2013).The role of maternal-fetal cholesterol transport in early fetal life: current insights. Biol. Reprod., 88(24), 1-9. DOI: 10.1095/biolreprod.112.102442.

  7. Bartels, A. & O’Donoghue, K. (2011). Cholesterol in pregnancy: a review of knowns and unknowns. Obstet. Med., 4, 147–151. DOI: 10.1258/om.2011.110003.

  8. Beller, M., Thiel, K., Thul, P.J. & Jäckle, H. (2010). Lipid droplets: A dynamic organelle moves into focus. FEBS Lett, 584, 2176-2182. DOI: 10.1016/j.febslet.2010.03.022.

  9. Bhattacharjee, J., Ietta, F., Romagnoli, R., Bechi, N., Caniggia, I. & Paulesu, L. (2012). ABC transporters in human placenta and their role in maternal-fetal cholesterol transfer: ABCA1 candidate target. En Jing Zheng (Ed.). Recent Advances in Research on the Human Placenta (pp. 336-354).London: IntechOpen. ISBN 978-953-51- 0194-9 DOI: 10.5772/1211.

  10. Bianco-Miotto, T., Blundell, C., Buckberry, S., Chamley, L., Chong, S., Cottrell, E., Dawson, P., Hanna, C., Holland, O., Lewis, R.M., Moritz, K., Myatt, L., Perkins, A.V., Powell, T., Saffery, R., Sferruzzi-Perri, A., Sibley, C., Simmons, D. & O’Tierney-Ginn, P.F. (2016). IFPA meeting 2015 workshop report I: Placental mitochondrial function, transport systems and epigenetics. Placenta, 48, Suppl. 1, Trophoblast Res., 30, S3-S6. DOI: 10.1016/j. placenta.2015.11.014. 10. Bose, M., Whittal, R.M., Miller, W.L. & Bose, H.S. (2008). Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein. J. Biol. Chem., 283, 8837–8845. DOI: 10.1074/jbc. M709221200.

  11. Burton, G.J. & Fowden, A.L. (2015). The placenta: a multifaceted, transient organ. Phil. Trans. R. Soc. B, 370: 20140066. DOI: 10.1098/rstb.2014.0066.

  12. Byrns, M.C. (2014). Regulation of progesterone signaling during pregnancy: Implications for the use of progestins for the prevention of preterm birth. J. Steroid Biochem.& Mol. Biol., 139, 173– 181. DOI: 10.1016/j. jsbmb.2013.01.015.

  13. Chatuphonprasert, W., Jarukamjorn, K. & Ellinger, I. (2018). Physiology and pathophysiology of steroid biosynthesis, transport and metabolism in the human placenta. Front. Pharmacol., 9, 1027. DOI: 10.3389/fphar.2018.01027.

  14. Chien, Y., Rosal, K. & Chung, B. (2017). Function of CYP11A1 in the mitochondria. Mol. Cell Endocrinol., 441, 55-61. DOI: 10.1016/j.mce.2016.10.030.

  15. Esparza-Perusquía, M., Olvera-Sánchez, S., Flores-Herrera, O., Flores-Herrera, H., Guevara-Flores, A., Pardo, J.P., Espinosa-García, M.T. & Martínez, F. (2015). Mitochondrial proteases act on STARD3 to activate progesterone synthesis in human syncytiotrophoblast. Biochim. Biophys. Acta, 1850(1), 107-117. DOI: 10.1016/j.bbagen.2014.10.009.

  16. Fan, J. & Papadopoulos, V. (2013). Evolutionary origin of the mitochondrial cholesterol transport machinery reveals a universal mechanism of steroid hormone biosynthesis in animals. PLoS ONE, 8, e76701. DOI:10.1371/journal. pone.0076701.

  17. Flis, V.V. & Daum, G. (2013). Lipid transport between the endoplasmic reticulum and mitochondria. Cold Spring Harb Perspect Biol., 5(6), pii: a013235. DOI: 10.1101/ cshperspect.a013235.

  18. Furuhashi, M., Seo, H., Mizutani, S., Narita, O., Tomoda, Y. &, Matsui, N. (1989). Expression of low density lipoprotein receptor gene in human placenta during pregnancy. Mol. Endocrinol., 3, 1252-1256. DOI: 10.1210/mend-3-8-1252.

  19. Galluzzi, L., Kepp, O. & Kroemer, G. (2012). Mitochondria: master regulators of danger signalling. Nat. Rev. Moll. Cell Biol., 13, 780-788. DOI: 10.1038/nrm3479. *

  20. Grant, N.J., Hepp, R., Krause, W., Aunis, D., Oehme, P. & Langley, K. (1999). Differential expression of SNAP- 25 isoforms and SNAP-23 in the adrenal gland. J. Neurochem., 72(1), 363-372. DOI: 10.1046/j.1471- 4159.1999.0720363.x.

  21. Hackenbrock, C.R. & Miller, K.J. (1975). The distribution of anionic sites on the surfaces of mitochondrial membranes. Visual probing with polycationic ferritin. J. Cell. Biol., 65(3), 615-630. DOI: 10.1083/jcb.65.3.615.

  22. Halasz, M. & Szekeres-Bartho, J. (2013). The role of progesterone in implantation and trophoblast invasion. J. Reprod. Immunol., 97, 43–50. DOI: 10.1016/j. jri.2012.10.011.

  23. Holland, O., Nitert, M.D., Gallo, L.A., Vejzovic, M., Fisher, J.J. & Perkins A.V. (2017a). Placental mitochondrial function and structure in gestational Disorders. Placenta, 54, 2-9.DOI: 10.1016/j.placenta.2016.12.012.

  24. Holland, O.J., Hickey, A.J.J., Alvsaker, A., Moran, S., Hedges, C., Chamley, L.W. & Perkins, A.V. (2017b). Changes in mitochondrial respiration in the human placenta over gestation. Placenta, 57, 102-112. DOI: 10.1016/j. placenta.2017.06.011.

  25. Horvath, S.E. & Daum, G. (2013). Lipids of mitochondria. Prog. Lipid Res., 52, 590-614. DOI: 10.1016/j. plipres.2013.07.002.

  26. Issop, L., Fan, J., Lee, S., Rone, M.B., Basu, K., Mui, J. & Papadopoulos, V. (2015).Mitochondria-associated membrane formation in hormone-stimulated Leydig cell steroidogenesis: Role of ATAD3. Endocrinology, 1: 334- 345. DOI: 10.1210/en.2014-1503.

  27. Jägerström, M.S., Polesie, S., Wickström, Y., Johansson, B.R., Schroder, H.D., Højlund, K. & Boström, P. (2009). Lipid droplets interact with mitochondria using SNAP23. Cell Biol. Int., 33(9), 934-940. DOI: 10.1016/j. cellbi.2009.06.011.

  28. Kaiser, J. (2014). Gearing up for a closer look at the human placenta. Science, 344(6188), 1073. DOI: 10.1126/ science.344.6188.1073.

  29. LaVoie, H.A. & King, S.R. (2009). Transcriptional regulation of steroidogenic genes: STARD1, CYP11A1 and HSD3B. Exp. Biol. Med. (Maywood), 234, 880-907. DOI: 10.3181/0903-MR-97.

  30. Marriott, K.S., Prasad, M., Thapliyal, V. & Bose, H.S. (2012). σ-1 Receptor at the mitochondrial-associated endoplasmic reticulum membrane is responsible for mitochondrial metabolic regulation. J. Pharmacol. Exp.Ther., 343, 578- 586. DOI: 10.1124/jpet.112.198168.

  31. Martin, L.A., Kennedy, B.E. & Karten, B. (2014). Mitochondrial cholesterol: mechanisms of import and effects on mitochondrial function. J. Bioenerg. Biomembr., 48(2), 137-151. DOI: 10.1007/s10863-014-9592-6.

  32. Martínez, F. & Strauss, J.F. 3rd (1997). Regulation of mitochondrial cholesterol metabolism. Subcell. Biochem., 28, 205-234. PMID: 9090296.

  33. Mesmin, B., Antonny, B. & Drin, G. (2013). Insights into the mechanisms of sterol transport between organelles. Cell. Mol. Life Sci., 70, 3405–3421.DOI: 10.1007/s00018-012- 1247-3.

  34. Miller, W.L. & Bose, H.S. (2011). Early steps in steroidogenesis: intracellular cholesterol trafficking. J. Lipid Res., 52, 2111-2135. DOI: 10.1194/jlr.R016675.

  35. Miller, W.L. (2013). Steroid hormone synthesis in mitochondria. Mol. Cell Endocrinol., 379, 62-73. DOI. 10.1016/j.mce.2013.04.014.

  36. Monreal-Flores, J., Espinosa-García, M.T., García-Regalado, A., Arechavaleta-Velasco, F. & Martínez, F. (2017). The heat shock protein 60 promotes progesterone synthesis in mitochondria of JEG-3 cells. Reprod. Biol., 17, 154-161. DOI: 10.1016/j.repbio.2017.04.001.

  37. Morel, Y., Roucher, F., Plotton, I., Goursaud, C., Tardy, V. & Mallet, D. (2016). Evolution of steroids during pregnancy: Maternal, placental and fetal synthesis. Ann. Endocrinol. (Paris), 77(2), 82-89. DOI: 10.1016/j.ando.2016.04.023. 2016.

  38. Morohaku, K., Pelton, S.H., Daugherty, D.J., Butler, W.R., Deng, W. & Selvaraj, V. (2014). Translocator protein/ peripheral benzodiazepine receptor is not required for steroid hormone biosynthesis. Endocrinology, 155(1), 89–97. DOI: 10.1210/en.2013-1556.

  39. Navarrete, J., Flores-Herrera, O., Uribe, A. & Martínez, F. (1999). Differences in cholesterol incorporation into mitochondria from hepatoma AS-30D and human term placenta. Placenta, 20(4), 285-291. DOI: 10.1053/ plac.1998.0374.

  40. Olvera-Sánchez, S., Espinosa-García, M.T., Monreal, J., Flores-Herrera, O. & Martinez, F. (2011). Mitochondrial heat shock protein participates in placental steroidogenesis. Placenta, 32, 222-229. DOI: 10.1016/j. placenta.2010.12.018.

  41. Pagler, T.A., Golsabahi, S., Doringer, M., Rhode, S., Schutz, G.J., Pavelka, M., Wadsack, C., Gauster, M., Lohninger, A., Laggner, H., Strobl, W. & Stangl, H. (2006). A Chinese hamster ovarian cell line imports cholesterol by high density lipoprotein degradation. J. Biol. Chem., 281, 38159-38171. DOI: 10.1074/jbc.M603334200

  42. Papadopoulos, V. & Miller, W.L. (2012). Role of mitochondria in steroidogenesis. Best Pract. Res. Clin. Endocrinol. Metab., 26(6), 771-790. DOI: 10.1016/j. beem.2012.05.002.

  43. Papadopoulos, V. (1993). Peripheral-type benzodiazepine/ diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr. Rev., 14, 222-240. DOI: 10.1210/edrv-14-2-222.

  44. Paul, S., Gupta, P.D., Jailkhani, B.L. & Talwar, G.P. (1980). Resistance of human syncytiotrophoblast to hypotonic and thermal stress. J. Reprod. Fertil., 58(1), 183-187. PMID: 7359476.

  45. Paul, S., Jailkhani, B.L. & Talwar, G.P. (1978). Isolation and functional maintenance in culture of syncytiotrophoblasts from human placenta. Indian J. Exp. Biol., 16, 1226- 1235. PMID: 750412.

  46. Pawlak, K.J., Prasad, M., Thomas, J.L., Whittal, R.M. & Bose, H.S. (2011). Inner mitochondrial translocase Tim50 interacts with 3β-hydroxysteroid dehydrogenase type 2 to regulate adrenal and gonadal steroidogenesis. J. Biol.Chem., 286(45), 39130-39140. DOI: 10.1074/jbc. M111.290031.

  47. Poderoso, C., Duarte, A., Cooke, M., Orlando, U., Gottifredi, V., Solano, A.R. Lemos, J.R. & Podestá, E.J. (2013). The spatial and temporal regulation of the hormonal signal. Role of mitochondria in the formation of a protein complex required for the activation of cholesterol transport and steroids synthesis. Mol. Cell. Endocrinol., 371, 26–33. DOI: 10.1016/j.mce.2012.12.024.

  48. Prasad, M., Kaur, J., Pawlak, K.J., Bose, M., Whittal, R.M. & Bose, H.S. (2015). Mitochondria associated ERMembrane (MAM) regulates steroidogenic activity via StAR-VDAC2 interaction. J. Biol. Chem., 290, 2604- 2616. DOI: 10.1074/jbc.M114.605808.

  49. Rajapaksha, M., Kaur, J., Bose, M., Whittal, R.M. & Bose, H.S. (2013). Cholesterol-mediated conformational changes in the steroidogenic acute regulatory protein are essential for steroidogenesis. Biochemistry, 52, 7242−7253. DOI: 10.1021/bi401125v.

  50. Rajapaksha, M., Kaur, J., Prasad, M., Pawlak, K.J., Marshall, B., Perry, E.W., Whittal, R.M. & Bose, H.S. (2016). An outer mitochondrial translocase, Tom22, is crucial for inner mitochondrial steroidogenic regulation in adrenal and gonadal tissues. Mol. Cell Biol., 36(6), 1032-1047. DOI: 10.1128/MCB.01107-15;

  51. Rasola, A. & Bernardi, P. (2014). The mitochondrial permeability transition pore and its adaptive responses in tumor cells. Cell Calcium, 56(6), 437-445. DOI: 10.1016/j.ceca.2014.10.003.

  52. Sanderson, J.T. (2009). Placental and Fetal Steroidogenesis Human. En: Lafond, J. & Vaillancourt, C. (Ed.). Embryogenesis: Methods and Protocols. (pp. 127-136) Nueva York:HumanaPress.DOI 10.1007/978-1-60327- 009-0 7.

  53. Simpson, E.R. & MacDonald, P.C. (1981). Endocrine physiology of the placenta. Annu. Rev. Physiol., 43, 163- 188. DOI: 10.1146/annurev.ph.43.030181.001115

  54. Soffientini, U. & Graham, A. (2016). Intracellular cholesterol transport proteins: roles in health and disease. Clin. Sci., 130, 1843–1859 DOI: 10.1042/CS20160339

  55. Steegmaier, M., Oorschot, V., Klumperman, J. & Scheller, R.H. (2000). Syntaxin 17 is abundant in steroidogenic cells and implicated in smooth endoplasmic reticulum membrane dynamics. Mol. Biol. Cell, 11(8), 2719-2731. DOI: 10.1091/mbc.11.8.2719.

  56. Strauss, J.F.3rd, Kishida, T., Christenson, L.K., Fujimoto, T. & Hiroi, H. (2003). StAR domain proteins and the intracellular trafficking of cholesterol in steroidogenic cells. Mol. Cell, Endocrinol., 202, 59-65. DOI: 10.1016/ S0303-7207(03)00063-7.

  57. Suen, D.F., Norris, K.L. & Youle, R.J. (2008). Mitochondrial dynamics and apoptosis. Genes Dev., 22, 1577-1590. DOI: 10.1101/gad.1658508.

  58. Tait, S.W. & Green, D.R. (2012). Mitochondria and cell signalling. J. Cell Sci., 125, 807-815. DOI: 10.1242/ jcs.099234.

  59. Tu, L.N., Morohaku, K., Manna, P.R., Pelton, S.H., Butler, W.R., Stocco, D.M. & Selvaraj, V. (2014). Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis. J. Biol. Chem., 289, 40, 27444– 27454. DOI: 10.1074/jbc.M114.578286.

  60. Tuckey, R.C., Headlam, M.J, Bose, H.S. & Miller, W.L. (2002). Transfer of cholesterol between phospholipid vesicles mediated by the steroidogenic acute regulatory protein (StAR). J. Biol. Chem., 277, 47123-28. DOI: 10.1074/jbc.M206965200.

  61. Tuckey, R.C., Bose, H.S., Czerwionka, I. & Miller, W.L. (2004). Molten globule structure and steroidogenic activity of N-218 MLN64 in human placental mitochondria. Endocrinology, 145, 1700-1707. DOI: 10.1210/en.2003- 1034.

  62. Uribe, A. Strauss, J.F. 3rd & Martínez, F. (2003). Contact sites from human placental mitochondria: characterization and role in progesterone synthesis. Arch. Biochem. Biophys., 413(2), 172-181. DOI: 10.1016/S0003- 9861(03)00097-3.

  63. van der Kant, R., Zondervan, I., Janssen, L. & Neefjes, J. (2013). Cholesterol-binding molecules MLN64 and ORP1L mark distinct late endosomes with transporters ABCA3 and NPC1. J. Lipid Res., 54, 2153–2165. DOI: 10.1194/jlr.M037325

  64. van Leusden, H. & Villee, C.A. (1965).The de novo synthesis of sterols and steroids -from acetate by preparations of human term placenta. Steroids, 6, 31-45. DOI: 10.1016/0039-128X(65)90031-0.

  65. Vaughan, O.R. & Fowden, A.L. (2016). Placental metabolism: substrate requirements and the response to stress. Reprod. Dom. Anim., 51 (Suppl. 2), 25-35.DOI: 10.1111/ rda.12797.

  66. Wadsack, C., Hammer, A., Levak-Frank, S., Desoye, G., Kozarsky, K.F., Hirschmugl, B., Sattler, W. & Malle, E. (2003). Selective cholesteryl ester uptake from high density lipoprotein by human first trimester and term villous trophoblast cells. Placenta, 24, 31-43. DOI: 10.1053/plac.2002.0912.

  67. Watari, H., Arakane, F., Moog-Lutz, C., Kallen, C.B., Tomasetto, C., Gerton, G.L., Rio, M.C., Baker, M.E. & Strauss, J.F. 3rd. (1997). MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. Proc. Natl. Acad. Sci. USA, 94(16), 8462-8467doi.org/10.1073/ pnas.94.16.8462

  68. Winkel, C.A., MacDonald, P.C. & Simpson, E.R. (1981). The role of receptor-mediated low-density lipoprotein uptake and degradation in the regulation of progesterone biosynthesis and cholesterol metabolism by human trophoblasts. Placenta, (Suppl. 3), 133-143. PMID: 6306642.

  69. Winkel, C.A., Snyder, J.M., MacDonald, P.C. & Simpson, E.R. (1980). Regulation of cholesterol and progesterone synthesis in human placental cells in culture by serum lipoproteins. Endocrinology, 106, 1054-1060. DOI: 10.1210/endo-106-4-1054.

  70. Woollett, L.A. (2011). Transport of maternal cholesterol to the fetal circulation. Placenta, 32 (Suppl. 2), S218-21. DOI: 10.1016/j.placenta.2011.01.011.

  71. Yang, H., Galea, A., Sytnyk, V. & Crossley, M. (2012). Controlling the size of lipid droplets: lipid and protein factors. Curr. Opin. Cell Biol., 24, 509-516. DOI: 10.1016/j.ceb.2012.05.012.

  72. Zelewski, L. & Villee, C.A. (1966). The biosynthesis of squalene, lanosterol, and cholesterol by minced human placenta. Biochemistry, 5,1805-1814. PMID: 5963423.

  73. Zamzami, N. & Kroemer, G. (2001). The mitochondrion in apoptosis: how Pandora’s Box opens. Nat. Rev. Mol. Cell Biol., 2(1), 67-71.DOI: 10.1038/35048073




2020     |     www.medigraphic.com

Mi perfil

C?MO CITAR (Vancouver)

TIP Rev Esp Cienc Quim Biol. 2019;22