MicroRNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells

Molecular and Cellular Biology

Volumn 32, Issue 24, 2012, Pages 5035-5045

  Hu, Zhigang ^a,b   Shen, Wen Jun ^a,b   Kraemer, Fredric B ^a,b   Azhar, Salman ^a,b  

^a VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOTROPIN; CYCLIC AMP; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LIPOPROTEIN; LUCIFERASE; MESSENGER RNA; MICRORNA; MICRORNA 125A; MICRORNA 455; SCAVENGER RECEPTOR; STEROID HORMONE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ADRENAL GLAND; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; CANCER CELL; CELL LINE; CONTROLLED STUDY; GRANULOSA CELL; HORMONE SYNTHESIS; LEYDIG CELL; LIVER CELL; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEROIDOGENESIS; WESTERN BLOTTING;

3' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; CHOLESTEROL ESTERS; DOWN-REGULATION; FEMALE; GRANULOSA CELLS; LEYDIG CELLS; LIPOPROTEINS, HDL; LIVER; MALE; MICE; MICRORNAS; PROGESTERONE; RATS; RATS, SPRAGUE-DAWLEY; SCAVENGER RECEPTORS, CLASS B; STEROIDS; TRANSFECTION;

RATTUS;

EID: 84871887481     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01002-12     Document Type: Article

References (84)

1. Acton S, et al. 1996. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science 271:518 -520.
2. Azhar S, Leers-Sucheta S, Reaven E. 2003. Cholesterol uptake in adrenal and gonadal tissues: the SR-BI and "selective" pathway connection. Front.Biosci. 8:s998 -s1029.
3. Azhar S, Namoto A, Leers-Sucheta S, Reaven E. 1998. Simultaneous induction of an HDL receptor protein (SR-BI) and the selective uptake of HDL-cholesteryl esters in a physiologically relevant steroidogenic cell model. J. Lipid Res. 39:1616 -1628.
4. Azhar S, Nomoto A, Reaven E. 2002. Hormonal regulation of adrenal microvillar channel formation. J. Lipid Res. 43:861- 871.
5. Azhar S, Stewart D, Reaven E. 1989. Utilization of cholesterol-richlipoproteins by perfused rat adrenals. J. Lipid Res. 30:1799 -1810.
6. Azhar S, Tsai L, Maffe W, Reaven E. 1988. Cultivation of rat granulose cells in a serum-free chemically defined medium-a useful model to study lipoprotein metabolism. Biochim. Biophys. Acta 963:139 -150.
7. Azhar S, Tsai L, Reven E. 1990. Uptake and utilization of lipoprotein cholesteryl esters by rat granulose cells. Biochim. Biophys. Acta 1047:148-160.
8. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
9. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
10. Belmont PJ, Chen WJ, Thuerauf DJ, Glembotski CC. 2012. Regulation of microRNA expression in the heart by the ATF6 branch of the ER stress response. J. Mol. Cell. Cardiol. 52:1176 -1182.
11. Betel D, Wilson M, Gabow A, Marks DS, Sander C. 2008. The micro- RNA.org resource: targets and expression. Nucleic Acids Res. 36:D149- D153.
12. Bushati M, Cohen SM. 2007. MicroRNA function. Annu. Rev. Cell Dev. Biol. 23:175-205.
13. Calvo D, Gómez-Corondo D, Lasunción MA, Vega MA. 1997. CLA-1 is an 85-kD plasma membrane glycoprotein that acts as a high-affinity receptor for both native (HDL, LDL, and VLDL) lipoproteins. Arterioscler.Thromb. Vasc. Biol. 17:2341-2349.
14. Cao G, et al. 1997. Structure and localization of human gene encoding SR-BI/CLA-1: evidence for transcriptional control by steroidogenic factor 1. J. Biol. Chem. 272:33068 -33076.
15. Chekulaeva M, Filipowicz W. 2009. Mechanisms of miRNA-mediated post-transcriptional regulation in animal cells. Curr. Opin. Cell Biol. 21: 452-460.
16. Chen T, et al. 2009. MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/macrophages. Cardiovasc. Res. 83:131-139.
17. Cheng Y, et al. 2009. MicroRNA-145, a novel smooth muscle cell phenomiRNAs typic marker and modulator, controls vascular neointimal lesion formation. Circ. Res. 105:158 -166.
18. Christenson LK. 2010. MicroRNA control of ovarian function. Anim. Reprod. 7:129 -133.
19. Connelly MA, Klein SM, Azhar S, Abumrad NA. 1999. Comparison of class B scavenger receptors, CD36, and scavenger receptor BI (SR-BI), shows that both receptors mediate high-density lipoprotein-cholesteryl ester selective uptake but SR-BI exhibits a unique enhancement of cholesteryl ester uptake. J. Biol. Chem. 274:41- 47.
20. Cordes KR, et al. 2009. miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460:705-711.
21. Engelmann B, Wiedmann MK. 2010. Cellular phospholipid uptake: flexible paths to coregulate the functions of intracellular lipids. Biochim. Biophys. Acta 1801:609-616.
22. Eulalio A, Huntzinger E, Izaurralde E. 2008. Getting to the root of miRNA-mediated gene silencing. Cell 132:9 -14.
23. Fabian MR, Sonenberg N, Fillipowicz W. 2010. Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79:351- 379.
24. Faucz FR, Stratakis CA. 2010. Adrenal cortex and microRNAs: an update. Cell Cycle 9:4239-4240.
25. Fenske SA, et al. 2009. Normal hepatic cell surface localization of the high density lipoprotein receptor, scavenger receptor class B, type I, depends on all four PDA domains of PDZK1. J. Biol. Chem. 284:5797-5806.
26. Filipowicz W, Bhattacharyya SN, Sonenberg N. 2008. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9:102-114.
27. Friedman RC, Farh Burge KK-HCB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92-105.
28. Ghildiyal M, Zamore PD. 2009. Small silencing RNAs: an expanding universe. Nat. Rev. Genet. 10:94 -108.
29. Griffiths-Jones S, Saini HK, van Dongen Enright AJ. 2008. miRBase: tools for microRNA genomics. Nucleic Acids Res. 36:D154-D158.
30. Gu X, et al. 1998. The efficient cellular uptake of high density lipoprotein lipids via scavenger receptor class B type I requires not only receptormediated surface binding but also receptor-specific lipid transfer mediated by its extracellular domain. J. Biol. Chem. 273:26338 -26348.
31. Guo S, et al. 2010. MicroRNA miR-125a controls hematopoietic stem cell number. Proc. Natl. Acad. Sci. U. S. A. 107:14229 -14234.
32. Gwynne JT, Mahaffee DD. 1989. Rat adrenal uptake and metabolism of high density lipoprotein cholesteryl ester. J. Biol. Chem. 264:8141- 8150.
33. Herrera BM, et al. 2009. MicroRNA-125a is over-expressed in insulin target tissues in a spontaneous rat model of type 2 diabetes. BMC Med.Genomics 2:54.
34. Hiroki E, et al. 2010. Changes in microRNA expression levels correlate with clinicopathological features and prognoses in endometrial serious adenocarcinomas. Cancer Sci. 101:241-249.
35. Ji Y, et al. 1997. Scavenger receptor BI promotes high-density lipoprotein- mediated cholesterol efflux. J. Biol. Chem. 272:20982-20985.
36. Ji Y, et al. 1999. Hepatic scavenger receptor BI promotes rapid clearance of high density lipoprotein free cholesterol and its transport into bile. J.Biol. Chem. 274:33398 -33402.
37. Jordan SD, et al. 2011. Obesity-induced overexpression of miRNA-143 inhibits insulin-stimulated AKT activation and impairs glucose metabolism. Nat. Cell Biol. 13:434-446.
38. Kocher O, et al. 2003. Targeted disruption of the PDZK1 gene in mice causes tissue-specific depletion of the high density lipoprotein receptor scavenger receptor class B type I and altered lipoprotein metabolism. J.Biol. Chem. 278:52820 -52825.
39. Kozarsky KF, et al. 1997. Overexpression of the HDL receptor SR-BI alters plasma HDL and bile cholesterol levels. Nature 387:414-417.
40. Kozomara A, Griffiths-Jones S. 2011. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res. 39:D152-D157.
41. Landschulz KT, Pathak RK, Rigotti A, Krieger M, Hobbs H. 1996. Regulation of scavenger receptor class B, type I, a high density lipoprotein receptor, in liver and steroidogenic tissues of the rat. J. Clin. Invest. 98:984-995.
42. Leiva A, et al. 2011. Mechanisms regulating hepatic SR-BI expression and their impact on HDL metabolism. Atherosclerosis 217:299 -307.
43. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15-20.
44. -δδCt method. Methods 25:402-408.
45. Mishima T, et al. 2008. MicroRNA(miRNA) cloning analysis reveals sex differences in miRNA expression profiles between adult mouse testis and ovary. Reproduction 136:811- 822.
46. Muddashetty RS, et al. 2011. Reversible inhibitor of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42:673- 688.
47. Nicholls PK, et al. 2011. Hormonal regulation of sertoli cell microRNAs at spermiation. Endocrinology 152:1670 -1683.
48. Nothnick WB. 2012. The role of micro-RNAs in the female reproductive tract. Reproduction 143:559 -576.
49. Orly J, Sato G, Erickson GF. 1980. Serum suppresses the expression of hormonally induced functions in cultured granulosa cells. Cell 20:817-827.
50. Papaioannou MD, Nef S. 2010. MicroRNAs in the testis: building up male fertility. J. Androl. 31:26 -33.
51. Peng Y, et al. 2004. Scavenger receptor BI (SR-BI) clustered on microvillar extensions suggests that this plasma membrane domain is a way station for cholesterol trafficking between cells and high-density lipoprotein.Mol. Biol. Cell 15:384 -396.
52. Pieters MN, et al. 1991. Selective uptake of cholesteryl esters from apolipoprotein- E-free high-density lipoproteins by rat parenchymal cells in vivo is efficiently coupled to bile acid synthesis. Biochem. J. 280:359 -365.
53. Pittman RC, Knecht TP, Rosenbaum MS, Taylor CA, Jr. 1987. A nonendocytotic mechanism for the selective uptake of high density lipoprotein- associated cholesterol esters. J. Biol. Chem. 262:2443-2450.
54. Rao S, Park C, Sanders KM, McCarrey JR, Yan W. 2007. Cloning and expression profiling of testis-expressed microRNAs. Dev. Biol. 311:592-602.
55. Reaven E, Chen YD, Spicher M, Azhar S. 1984. Morphological evidence that high density lipoproteins are not internalized by steroid-producing cells during in situ organ perfusion. J. Clin. Invest. 74:1384 -1397.
56. Reaven E, Cortez Y, Leers-Sucheta S, Nomoto A, Azhar S. 2004. Dimerization of the scavenger receptor class B type I: formation, function, and localization in diverse cells and tissues. J. Lipid Res. 45:513-528.
57. Reaven E, Leers-Sucheta S, Nomoto A, Azhar S. 2001. Expression of scavenger receptor class B type I (SR-BI) promotes microvillar channel formation and selective cholesteryl ester transport in a heterologous reconstituted system. Proc. Natl. Acad. Sci. U. S. A. 98:1613-1618.
58. Reaven E, Nomoto A, Cortez Y, Azhar S. 2006. Consequences of overexpression of rat scavenger receptor, SR-BI, in an adrenal cell model. Nutr. Metab. (Lond.) 3:43.
59. Reaven E, et al. 1998. Expression and microvillar localization of scavenger receptor, class B, type I (a high density lipoprotein receptor) in luteinized and hormone-desensitized rat ovarian models. Endocrinology 139:2847-2856.
60. Reaven E, Tsai L, Azhar S. 1995. Cholesterol uptake by the "selective" pathway of ovarian granulose cells: early intracellular events. J. Lipid Res. 36:1602-1607.
61. Reaven E, Tsai L, Azhar S. 1996. Intracellular events in the "selective" transport of lipoprotein-derived cholesteryl esters. J. Biol. Chem. 271: 16208-16217.
62. Reaven E, Zhan L, Nomoto A, Leers-Sucheta S, Azhar S. 2000. Expression and microvillar localization of scavenger receptor class B, type I (SRBI) and selective cholesteryl ester uptake in Leydig cells from rat testis. J.Lipid Res. 41:343-356.
63. Riester A, et al. 2012. ACTH-dependent regulation of microRNA as endogenous modulators of glucocorticoid receptor expression in the adrenal gland. Endocrinology 153:212-222.
64. Rigotti A, et al. 1996. Regulation by adrenocorticotropic hormone of the in vivo expression of scavenger receptor class B type I (SR-BI), a high density lipoprotein receptor, in steroidogenic cells of the murine adrenal gland. J. Biol. Chem. 271:33545-33549.
65. Rigotti A, Miettinen HE, Krieger M. 2003. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr. Rev. 24:357-387.
66. Rigotti A, et al. 1997. A targeted mutation in the murine gene encoding the high density lipoprotein (HDL) receptor scavenger receptor class B type I reveals its key role inHDLmetabolism. Proc. Natl. Acad. Sci. U. S. A.94:12610 -12615.
67. Robins SJ, Fasulo JM. 1997. High density lipoproteins, but not other lipoproteins, provide a vehicle for sterol transport to bile. J. Clin. Invest.99:380 -384.
68. Romero DG, Plonczynski MW, Carvajal CA, Gomez-Sanchez EP, Gomez- Sanchez CE. 2008. Microribonucleic acid-21 increases aldosterone secretion and proliferation in H295R human adrenocortical cells. Endocrinology 149:2477-2483.
69. Sachdeva M, Mo Y-Y. 2010. MicroRNA-145 suppresses cell invasion and metastasis by directly targeting mucin-1. Cancer Res. 70:378 -387.
70. Sanders MM, Midgley AR, Jr. 1982. Rat granulose cell differentiation: an in vitro model. Endocrinology 111:614-624.
71. Sanders MM, Midgley AR, Jr. 1983. Cyclic nucleotides can induce luteinizing hormone receptors in cultured granulosa cells. Endocrinology 112:1382-1388.
72. Scott GK, et al. 2007. Coordinate suppression of ERBB2 and ERBB3 by enforced expression of micro-RNA miR-125a or miR-125b. J. Biol. Chem. 282:1479 -1486.
73. Segura MF, et al. 2010. Melanoma microRNA signature predicts postrecurrence survival. Clin. Cancer Res. 16:1577-1586.
74. Temel RE, et al. 1997. Scavenger receptor class B, type I (SR-BI) is the major route of delivery of high density lipoprotein cholesterol to the steroidogenic pathway in cultured mouse adrenocortical cells. Proc. Natl.Acad. Sci. U. S. A. 94:13600 -13605.
75. Ujifuku K, et al. 2010. miR-195, miR-455-3p and miR-10a(*) are implicated in acquired temozolomide resistance in glioblastoma multiforme cells. Cancer Lett. 296:241-248.
76. Varban ML, et al. 1998. Targeted mutation reveals a central role for SR-BI in hepatic selective uptake of high density lipoprotein cholesterol. Proc. Natl. Acad. Sci. U. S. A. 95:4619-4624.
77. Williams DL, Wong JS, Hamilton RL. 2002. SR-BI is required for microvillar channel formation and the localization of HDL particles to the surface of adrenocortical cells in vivo. J. Lipid Res. 43:544 -549.
78. Wu L, Belasco JG2005. Micro-RNA regulation of the mammalian lin-26 gene during neuronal differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 25:9198 -9208.
79. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS. 2009. MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137:647- 658.
80. Xu S, Linher-Melville K, Yang BB, Wu D, Li J. 2011. Micro-RNA378 (miR-378) regulates ovarian estradiol production by targeting aromatase. Endocrinology 152:3941-3951.
81. Yao N, et al. 2010. Follicle-stimulating hormone regulation of microRNA expression on progesterone production in cultured rat granulosa cells. Endocrine 38:158 -166.
82. Zhang Y, et al. 2009. MicroRNA 125a and its regulation of the p53 tumor suppressor gene. FEBS Lett. 583:3725-3730.
83. Zhao H, Rakovic A. 2008. MicroRNAs and mammalian ovarian development. Semin. Reprod. Med. 26:461- 468.
84. 1 regulators. Mol. Cancer Res. 9:960 -975.