Evolutionary Origin of the Mitochondrial Cholesterol Transport Machinery Reveals a Universal Mechanism of Steroid Hormone Biosynthesis in Animals

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Fan, Jinjiang ^a   Papadopoulos, Vassilios ^a,b  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); MITOCHONDRIAL PROTEIN; MULTIENZYME COMPLEX; MULTIPROTEIN COMPLEX; STEROID; TRANSDUCEOSOME; UNCLASSIFIED DRUG;

ARTICLE; CHOLESTEROL METABOLISM; CHOLESTEROL TRANSPORT; EVOLUTION; GENE DUPLICATION; GENOME; HUMAN; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR DOCKING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; STEROIDOGENESIS;

ANIMALS; BIOLOGICAL EVOLUTION; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CHOLESTEROL; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; COMPUTATIONAL BIOLOGY; CYCLIC AMP-DEPENDENT PROTEIN KINASE RIALPHA SUBUNIT; EVOLUTION, MOLECULAR; GENE DUPLICATION; GONADAL STEROID HORMONES; HUMANS; MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, MOLECULAR; MULTIGENE FAMILY; PHYLOGENY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION DOMAINS AND MOTIFS; SIGNAL TRANSDUCTION; STEROIDS; VERTEBRATES; VOLTAGE-DEPENDENT ANION CHANNELS;

EID: 84885040249     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076701     Document Type: Article

References (101)

1. Papadopoulos V, Miller WL, (2012) Role of mitochondria in steroidogenesis. Best Pract Res Clin Endocrinol Metab 26: 771-790. doi:10.1016/j.beem.2012.05.002. PubMed: 23168279.
2. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapère JJ, et al. (2006) Translocator protein (18kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27: 402-409. doi:10.1016/j.tips.2006.06.005. PubMed: 16822554.
3. Miller WL, (2007) Mechanism of StAR's regulation of mitochondrial cholesterol import. Mol Cell Endocrinol 265: 46-50. PubMed: 17207924.
4. Fan J, Liu J, Culty M, Papadopoulos V, (2010) Acyl-coenzyme A binding domain containing. p. pp. 3 (ACBD3; PAP7; GCP60): An emerging signaling molecule. Prog Lipid Res 49: 218-234.
5. Papadopoulos V, Liu J, Culty M, (2007) Is there a mitochondrial signaling complex facilitating cholesterol import? Mol Cell Endocrinol 265-266: 59-64. doi:10.1016/j.mce.2006.12.004. PubMed: 17280776.
6. Rone MB, Fan J, Papadopoulos V, (2009) Cholesterol transport in steroid biosynthesis: Role of proteinûprotein interactions and implications in disease states. BBA-Mol. Cell Biol L1791:: 646-658.
7. Rone MB, Midzak AS, Issop L, Rammouz G, Jagannathan S, et al. (2012) Identification of a Dynamic Mitochondrial Protein Complex Driving Cholesterol Import, Trafficking, and Metabolism to Steroid Hormones. Mol Endocrinol 26: 1868-1882. doi:10.1210/me.2012-1159. PubMed: 22973050.
8. Liu J, Rone MB, Papadopoulos V, (2006) Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem 281: 38879-38893. doi:10.1074/jbc.M608820200. PubMed: 17050526.
9. Midzak A, Rone M, Aghazadeh Y, Culty M, Papadopoulos V, (2011) Mitochondrial protein import and the genesis of steroidogenic mitochondria. Mol Cell Endocrinol 336: 70-79. doi:10.1016/j.mce.2010.12.007. PubMed: 21147195.
10. Poderoso C, Converso DP, Maloberti P, Duarte A, Neuman I, et al. (2008) A mitochondrial kinase complex is essential to mediate an ERK1/2-dependent phosphorylation of a key regulatory protein in steroid biosynthesis. PLOS ONE 3: e1443. doi:10.1371/journal.pone.0001443. PubMed: 18197253.
11. Poderoso C, Maloberti P, Duarte A, Neuman I, Paz C, et al. (2009) Hormonal activation of a kinase cascade localized at the mitochondria is required for StAR protein activity. Mol Cell Endocrinol 300: 37-42. doi:10.1016/j.mce.2008.10.009. PubMed: 19007846.
12. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH, (1992) Isolation of the mitochondrial benzodiazepine receptor: association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci U S A 89: 3170-3174. doi:10.1073/pnas.89.8.3170. PubMed: 1373486.
13. Papadopoulos V, Mukhin AG, Costa E, Krueger KE, (1990) The peripheral-type benzodiazepine receptor is functionally linked to Leydig cell steroidogenesis. J Biol Chem 265: 3772-3779. PubMed: 2154488.
14. Kinnally KW, Zorov DB, Antonenko YN, Snyder SH, McEnery MW, et al. (1993) Mitochondrial benzodiazepine receptor linked to inner membrane ion channels by nanomolar actions of ligands. Proc Natl Acad Sci U S A 90: 1374-1378. doi:10.1073/pnas.90.4.1374. PubMed: 7679505.
15. Rampon C, Bouzaffour M, Ostuni MA, Dufourcq P, Girard C, et al. (2009) Translocator protein (18 kDa) is involved in primitive erythropoiesis in zebrafish. FASEB J 23: 4181-4192. doi:10.1096/fj.09-129262. PubMed: 19723704.
16. Behrman EJ, Gopalan V, (2005) Cholesterol and plants. J Chem Educ 82: 1791. doi:10.1021/ed082p1791.
17. Zinser ERWI, Paltauf FRIT, Gunt, Daum (1993) Sterol composition of yeast organelle membranes and subcellular distribution of enzymes involved in sterol metabolism. J Bacteriol 175: 2853-2858. PubMed: 8491706.
18. Brown AJ, Galea AM, (2010) Cholesterol as an evolutionary response to living with oxygen. Evolution 64: 2179-2183. PubMed: 20394667.
19. Miao L, Nielsen M, Thewalt J, Ipsen JH, Bloom M, et al. (2002) From lanosterol to cholesterol: structural evolution and differential effects on lipid bilayers. Biophys J 82: 1429-1444. doi:10.1016/S0006-3495(02)75497-0. PubMed: 11867458.
20. Desmond E, Gribaldo S, (2009) Phylogenomics of sterol synthesis: insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol Evolution 1: 364-381. PubMed: 20333205.
21. Markov GV, Tavares R, Dauphin-Villemant C, Demeneix BA, Baker ME, et al. (2009) Independent elaboration of steroid hormone signaling pathways in metazoans. Proc Natl Acad Sci U S A 106: 11913-11918. doi:10.1073/pnas.0812138106. PubMed: 19571007.
22. Stout EP, La Clair JJ, Snell TW, Shearer TL, Kubanek J, (2010) Conservation of progesterone hormone function in invertebrate reproduction. Proc Natl Acad Sci USA 107: 11859-11864. doi:10.1073/pnas.1006074107. PubMed: 20547846.
23. Fan J, Lindemann P, Feuilloley MG, Papadopoulos V, (2012) Structural and functional evolution of the translocator protein (18 kDa). Curr Mol Med 12: 369-386. doi:10.2174/156652412800163415. PubMed: 22364126.
24. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. doi:10.1093/bioinformatics/btm404. PubMed: 17846036.
25. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
26. Kumar S, Tamura K, Nei M, (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163. doi:10.1093/bib/5.2.150. PubMed: 15260895.
27. Kumar S, Nei M, Dudley J, Tamura K, (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-309. doi:10.1093/bib/bbn017. PubMed: 18417537.
28. Dayhoff MO, Schwartz RM, Orcutt BC, (1978) A model of evolutionary change in proteins. In: Dayhoff MO, eds. Washington, DC: National Biomedical Research Foundation. pp. pp. 345-352.
29. Gu X, Vander VK, (2002) DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 18: 500-501. doi:10.1093/bioinformatics/18.3.500. PubMed: 11934757.
30. Gaucher EA, Gu X, Miyamoto MM, Benner SA, (2002) Predicting functional divergence in protein evolution by site-specific rate shifts. Trends Biochem Sci 27: 315-321. doi:10.1016/S0968-0004(02)02094-7. PubMed: 12069792.
31. Tsujishita Y, Hurley JH, (2000) Structure and lipid transport mechanism of a StAR-related domain. Nat Struct Mol Biol 7: 408-414. doi:10.1038/75192. PubMed: 10802740.
32. Akula N, Midzak A, Lecanu L, Papadopoulos V, (2012) Identification of small-molecule inhibitors of the steroidogenic acute regulatory protein (STARD1) by structure-based design. Bioorg Med Chem Lett 22: 4139-4143. doi:10.1016/j.bmcl.2012.04.058. PubMed: 22575868.
33. Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N, (2010) ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res gkq 399: 1-5. PubMed: 20478830.
34. Li H, Papadopoulos V, (1998) Peripheral-type benzodiazepine receptor function in cholesterol transport. Identification of a putative cholesterol recognition/interaction amino acid sequence and consensus pattern. Endocrinology 139: 4991-4997. doi:10.1210/en.139.12.4991. PubMed: 9832438.
35. Strushkevich N, MacKenzie F, Cherkesova T, Grabovec I, Usanov S, et al. (2011) Structural basis for pregnenolone biosynthesis by the mitochondrial monooxygenase system. Proc Natl Acad Sci USA 108: 10139-10143. doi:10.1073/pnas.1019441108. PubMed: 21636783.
36. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis 18: 2714-2723. doi:10.1002/elps.1150181505. PubMed: 9504803.
37. Trott O, Olson AJ, (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31: 455-461. PubMed: 19499576.
38. Fan J, Rone MB, Papadopoulos V, (2009) Translocator protein 2 is involved in cholesterol redistribution during erythropoiesis. J Biol Chem 284: 30484-30497. doi:10.1074/jbc.M109.029876. PubMed: 19729679.
39. Gu X, (1999) Statistical methods for testing functional divergence after gene duplication. Mol Biol Evol 16: 1664-1674. doi:10.1093/oxfordjournals.molbev.a026080. PubMed: 10605109.
40. Yeliseev AA, Krueger KE, Kaplan S, (1997) A mammalian mitochondrial drug receptor functions as a bacterial "oxygen" sensor. Proc Natl Acad Sci U S A 94: 5101-5106. doi:10.1073/pnas.94.10.5101. PubMed: 9144197.
41. Li H, Yao Z, Degenhardt B, Teper G, Papadopoulos V, (2001) Cholesterol binding at the cholesterol recognition/ interaction amino acid consensus (CRAC) of the peripheral-type benzodiazepine receptor and inhibition of steroidogenesis by an HIV TAT-CRAC peptide. Proc Natl Acad Sci U S A 98: 1267-1272. doi:10.1073/pnas.98.3.1267. PubMed: 11158628.
42. Bauer MP, Bridgham JT, Langenau DM, Johnson AL, Goetz FW, (2000) Conservation of steroidogenic acute regulatory (StAR) protein structure and expression in vertebrates. Mol Cell Endocrinol 168: 119-125. doi:10.1016/S0303-7207(00)00316-6. PubMed: 11064158.
43. Soccio RE, Breslow JL, (2003) StAR-related lipid transfer (START) proteins: mediators of intracellular lipid metabolism. J Biol Chem 278: 22183-22186. doi:10.1074/jbc.R300003200. PubMed: 12724317.
44. Alpy F, Tomasetto C, (2005) Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. J Cell Sci 118: 2791-2801. doi:10.1242/jcs.02485. PubMed: 15976441.
45. Murcia M, Faráldo-Gómez JD, Maxfield FR, Roux B, (2006) Modeling the structure of the StART domains of MLN64 and StAR proteins in complex with cholesterol. J Lipid Res 47: 2614-2630. doi:10.1194/jlr.M600232-JLR200. PubMed: 16990645.
46. Thorsell AG, Lee WH, Persson C, Siponen MI, Nilsson M, et al. (2011) Comparative structural analysis of lipid binding START domains. PLOS ONE 6: e19521. doi:10.1371/journal.pone.0019521. PubMed: 21738568.
47. Guidotti A, Forchetti CM, Corda MG, Konkel D, Bennett CD, et al. (1983) Isolation, characterization, and purification to homogeneity of an endogenous polypeptide with agonistic action on benzodiazepine receptors. Proc Natl Acad Sci U S A 80: 3531-3535. doi:10.1073/pnas.80.11.3531. PubMed: 6304714.
48. Shoyab M, Gentry LE, Marquardt H, Todaro GJ, (1986) Isolation and characterization of a putative endogenous benzodiazepineoid (endozepine) from bovine and human brain. J Biol Chem 261: 11968-11973. PubMed: 3745175.
49. Costa E, Guidotti A, (1991) Diazepam binding inhibitor(DBI): a peptide with multiple biological actions. Life Sci 49: 325-344. doi:10.1016/0024-3205(91)90440-M. PubMed: 1649940.
50. Cavallaro S, Pani L, Guidotti A, Costa E, (1993) ACTH-induced mitochondrial DBI receptor (MDR) and diazepam binding inhibitor (DBI) expression in adrenals of hypophysectomized rats is not cause-effect related to its immediate steroidogenic action. Life Sci 53: 1137-1147. doi:10.1016/0024-3205(93)90550-M. PubMed: 8396705.
51. Papadopoulos V, Guarneri P, Kreuger KE, Guidotti A, Costa E, (1992) Pregnenolone biosynthesis in C6-2B glioma cell mitochondria: regulation by a mitochondrial diazepam binding inhibitor receptor. Proc Natl Acad Sci U S A 89: 5113-5117. doi:10.1073/pnas.89.11.5113. PubMed: 1317581.
52. Papadopoulos V, (1993) Peripheral-type benzodiazepine/diazepam binding inhibitor receptor: biological role in steroidogenic cell function. Endocr Rev 14: 222-240. doi:10.1210/er.14.2.222. PubMed: 8391980.
53. Soupene E, Serikov V, Kuypers FA, (2008) Characterization of an acyl-coenzyme A binding protein predominantly expressed in human primitive progenitor cells. J Lipid Res 49: 1103-1112. doi:10.1194/jlr.M800007-JLR200. PubMed: 18268358.
54. Burton M, Rose TM, Faergeman NJ, Knudsen J, (2005) Evolution of the acyl-CoA binding protein (ACBP). Biochem J 392: 299-307. doi:10.1042/BJ20050664. PubMed: 16018771.
55. Liu J, Matyakhina L, Han Z, Sandrini F, Bei T, et al. (2003) Molecular cloning, chromosomal localization of human peripheral-type benzodiazepine receptor and PKA regulatory subunit type 1A (PRKAR1A)-associated protein PAP7, and studies in PRKAR1A mutant cells and tissues. FASEB J 17: 1189-1191. PubMed: 12692076.
56. Malmberg AB, Brandon EP, Idzerda RL, Liu H, McKnight GS, et al. (1997) Diminished inflammation and nociceptive pain with preservation of neuropathic pain in mice with a targeted mutation of the type I regulatory subunit of cAMP-dependent protein kinase. J Neurosci 17: 7462-7470. PubMed: 9295392.
57. Oyen O, Myklebust F, Scott JD, Cadd GG, McKnight GS, et al. (1990) Subunits of cyclic adenosine 3', 5'-monophosphate-dependent protein kinase show differential and distinct expression patterns during germ cell differentiation: alternative polyadenylation in germ cells gives rise to unique smaller-sized mRNA species. Biol Reprod 43: 46-54. doi:10.1095/biolreprod43.1.46. PubMed: 2393692.
58. Lacapère JJ, Papadopoulos V, (2003) Peripheral-type benzodiazepine receptor: structure and function of a cholesterol-binding protein in steroid and bile acid biosynthesis. Steroids 68: 569-585. doi:10.1016/S0039-128X(03)00101-6. PubMed: 12957662.
59. Kamath RS, Fraser AG, Dong Y, Poulin G, Durbin R, et al. (2003) Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421: 231-237. doi:10.1038/nature01278. PubMed: 12529635.
60. Feyereisen R, (2006) Evolution of insect P450. Biochem Soc T 34: 1252-1255. doi:10.1042/BST0341252.
61. Guzov VM, Unnithan GC, Chernogolov AA, Feyereisen R, (1998) CYP12A1, a mitochondrial cytochrome P450 from the house fly. Arch Biochem Biophys 359: 231-240. doi:10.1006/abbi.1998.0901. PubMed: 9808765.
62. Rewitz KF, O'Connor MB, Gilbert LI, (2007) Molecular evolution of the insect Halloween family of cytochrome P450s: phylogeny, gene organization and functional conservation. Insect Biochem Mol Biol 37: 741-753. doi:10.1016/j.ibmb.2007.02.012. PubMed: 17628274.
63. Lewis DFV, Lee-Robichaud P, (1998) Molecular modelling of steroidogenic cytochromes P450 from families CYP11, CYP17, CYP19 and CYP21 based on the CYP102 crystal structure. J Steroid Biochem Mol Biol 66: 217-233. doi:10.1016/S0960-0760(98)00032-6. PubMed: 9744519.
64. Lewis DFV, Watson E, Lake BG, (1998) Evolution of the cytochrome P450 superfamily: sequence alignments and pharmacogenetics. Mutat Res- Rev Genet 410: 245-270.
65. Cauet G, Balbuena D, Achstetter T, Dumas B, (2001) CYP11A1 stimulates the hydroxylase activity of CYP11B1 in mitochondria of recombinant yeast in vivo and in vitro. Eur J Biochem 268: 4054-4062. doi:10.1046/j.1432-1327.2001.02319.x. PubMed: 11454000.
66. Bose M, Whittal RM, Miller WL, Bose HS, (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. PubMed: 18250166.
67. Crompton M, (2000) Mitochondrial intermembrane junctional complexes and their role in cell death. J Physiol 529: 11-21. doi:10.1111/j.1469-7793.2000.00011.x. PubMed: 11080247.
68. Garnier M, Dimchev AB, Boujrad N, Price JM, Musto NA, et al. (1994) In vitro reconstitution of a functional peripheral-type benzodiazepine receptor from mouse Leydig tumor cells. Mol Pharmacol 45: 201-211. PubMed: 8114671.
69. Gilquin B, Taillebourg E, Cherradi N, Hubstenberger A, Gay O, et al. (2010) The AAA+ ATPase ATAD3A controls mitochondrial dynamics at the interface of the inner and outer membranes. Mol Cell Biol 30: 1984-1996. doi:10.1128/MCB.00007-10. PubMed: 20154147.
70. Li S, Rousseau D, (2012) ATAD3, a vital membrane bound mitochondrial ATPase involved in tumor progression. J Bioenerget Biomembr, 44: 1-9. PubMed: 22318359.
71. Harner M, Körner C, Walther D, Mokranjac D, Kaesmacher J, et al. (2011) The mitochondrial contact site complex, a determinant of mitochondrial architecture. EMBO J 30: 4356-4370. doi:10.1038/emboj.2011.379. PubMed: 22009199.
72. Wang XJ, Dyson MT, Mondillo C, Patrignani Z, Pignataro O, et al. (2002) Interaction between arachidonic acid and cAMP signaling pathways enhances steroidogenesis and StAR gene expression in MA-10 Leydig tumor cells. Mol Cell Endocrinol 188: 55-63. doi:10.1016/S0303-7207(01)00748-1. PubMed: 11911946.
73. Cano F, Poderoso C, Cornejo Maciel F, Castilla R, Maloberti P, et al. (2006) Protein tyrosine phosphatases regulate arachidonic acid release, StAR induction and steroidogenesis acting on a hormone-dependent arachidonic acid-preferring acyl-CoA synthetase. J Steroid Biochem Mol Biol 99: 197-202. doi:10.1016/j.jsbmb.2006.01.003. PubMed: 16630718.
74. Castilla R, Gadaleta M, Castillo AF, Duarte A, Neuman I, et al. (2008) New enzymes involved in the mechanism of action of epidermal growth factor in a clonal strain of Leydig tumor cells. Endocrinology 149: 3743-3752. doi:10.1210/en.2007-1580. PubMed: 18388199.
75. Van Horn CG, Caviglia JM, Li LO, Wang S, Granger DA, et al. (2005) Characterization of recombinant long-chain rat acyl-CoA synthetase isoforms 3 and 6: identification of a novel variant of isoform 6. Biochemistry 44: 1635-1642. doi:10.1021/bi047721l. PubMed: 15683247.
76. Stocco DM, Wang X, Jo Y, Manna PR, (2005) Multiple signaling pathways regulating steroidogenesis and steroidogenic acute regulatory protein expression: more complicated than we thought. Mol Endocrinol 19: 2647-2659. doi:10.1210/me.2004-0532. PubMed: 15831519.
77. Jefcoate CR, McNamara BC, Artemenko I, Yamazaki T, (1992) Regulation of cholesterol movement to mitochondrial cytochrome< i> P 450scc in steroid hormone synthesis. J Steroid Biochem Mol Biol 43: 751-767. doi:10.1016/0960-0760(92)90305-3. PubMed: 22217822.
78. Gilbert LI, Rybczynski R, Warren JT, (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47: 883-916. doi:10.1146/annurev.ento.47.091201.145302. PubMed: 11729094.
79. Mazet F, (2002) Gene duplication and divergence in the early evolution of vertebrates. Curr Opin Genet Dev 12: 393-396. doi:10.1016/S0959-437X(02)00315-5. PubMed: 12100882.
80. Bose HS, Sugawara T, Strauss JF, Miller WL, (1996) The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. N Engl J Med 335: 1870-1878. doi:10.1056/NEJM199612193352503. PubMed: 8948562.
81. Bhangoo A, Anhalt H, Ten S, King SR, (2006) Phenotypic variations in lipoid congenital adrenal hyperplasia. Pediatr Endocrinol Rev 3: 258-271. PubMed: 16639391.
82. Sierra A, (2004) Neurosteroids: the StAR protein in the brain. J Neuroendocrinol 16: 787-793. doi:10.1111/j.1365-2826.2004.01226.x. PubMed: 15344917.
83. Rewitz KF, Styrishave B, Løbner-Olesen A, Andersen O, (2006) Marine invertebrate cytochrome P450: emerging insights from vertebrate and insect analogies. Comp Biochem Physiol C Toxicol Pharmacol 143: 363-381. doi:10.1016/j.cbpc.2006.04.001. PubMed: 16769251.
84. Kurzchalia TV, Ward S, (2003) Why do worms need cholesterol? Nat Cell Biol 5: 684-688. doi:10.1038/ncb0803-684. PubMed: 12894170.
85. Baker ME, (2002) Albumin, steroid hormones and the origin of vertebrates. J Endocrinol 175: 121-127. doi:10.1677/joe.0.1750121. PubMed: 12379496.
86. Thornton JW, Need E, Crews D, (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301: 1714-1717. doi:10.1126/science.1086185. PubMed: 14500980.
87. Grieneisen ML, Warren JT, Gilbert LI, (1993) Early steps in ecdysteroid biosynthesis: evidence for the involvement of cytochrome P-450 enzymes. Insect Biochem Mol Biol 23: 13-23. doi:10.1016/0965-1748(93)90077-6. PubMed: 8485514.
88. Guryev O, Carvalho RA, Usanov S, Gilep A, Estabrook RW, (2003) A pathway for the metabolism of vitamin D3: unique hydroxylated metabolites formed during catalysis with cytochrome P450scc (CYP11A1). Proc Natl Acad Sci USA 100: 14754-14759. doi:10.1073/pnas.2336107100. PubMed: 14657394.
89. Slominski AT, Kim TK, Chen J, Nguyen MN, Li W, et al. (2012) Cytochrome P450scc-dependent metabolism of 7-dehydrocholesterol in placenta and epidermal keratinocytes. Int J Biochem Cell Biol, 44: 2003-18. PubMed: 22877869.
90. Snyder MJ, Van Antwerpen R, (1998) Evidence for a diazepam-binding inhibitor (DBI) benzodiazepine receptor-like mechanism in ecdysteroidogenesis by the insect prothoracic gland. Cell Tissue Res 294: 161-168. doi:10.1007/s004410051166. PubMed: 9724466.
91. Ishay JS, Fuksman E, Ermakov NY, Plotkin M, (2006) Diazepam inhibits reproduction and reproductive behavior of oriental hornet. A possible role for the peripheral-type benzodiazepine receptor. Physiol Chem Phys Med NMR 38: 31-42. PubMed: 17405410.
92. Sieglaff DH, Duncan KA, Brown MR, (2005) Expression of genes encoding proteins involved in ecdysteroidogenesis in the female mosquito, Aedes aegypti. Insect Biochem Mol Biol 35: 471-490. doi:10.1016/j.ibmb.2005.01.011. PubMed: 15804580.
93. Russell MJ, Martin W, (2004) The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci 29: 358-363. doi:10.1016/j.tibs.2004.05.007. PubMed: 15236743.
94. Aghazadeh Y, Rone MB, Blonder J, Ye X, Veenstra TD, et al. (2012) Hormone-induced 14-3-3g adaptor protein regulates steroidogenic acute regulatory protein activity and steroid biosynthesis in MA-10 Leydig cells. J Biol Chem 287: 15380-15394. doi:10.1074/jbc.M112.339580. PubMed: 22427666.
95. Miller WL, Auchus RJ, (2011) The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr Rev 32: 81-151. doi:10.1210/er.2010-0013. PubMed: 21051590.
96. Bourre JM, Clément M, Gérard D, Legrand R, Chaudière J, (1990) Precursors for cholesterol synthesis (7-dehydrocholesterol, 7-dehydrodesmosterol, and desmosterol): cholesterol/7-dehydrocholesterol ratio as an Index of development and aging in PNS but not in CNS. J Neurochem 54: 1196-1199. doi:10.1111/j.1471-4159.1990.tb01948.x. PubMed: 2156015.
97. Saitou N, Nei M, (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425. PubMed: 3447015.
98. Kyte J, Doolittle RF, (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105-132. doi:10.1016/0022-2836(82)90515-0. PubMed: 7108955.
99. Berka K, Hanák O, Sehnal D, Banáš P, Navrátilová V, et al. (2012) MOLEonline. p. pp. 2.0: interactive web-based analysis of biomacromolecular channels. Nucleic Acids Res 40: W222-W227.
100. Brown MR, Sieglaff DH, Rees HH, (2009) Gonadal ecdysteroidogenesis in Arthropoda: occurrence and regulation. Annu Rev Entomol 54: 105-125. doi:10.1146/annurev.ento.53.103106.093334. PubMed: 18680437.
101. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 39: D561-D568. doi:10.1093/nar/gkq973. PubMed: 21045058.