RhoA and DIAPH1 mediate adrenocorticotropin-stimulated cortisol biosynthesis by regulating mitochondrial trafficking

Endocrinology

Volumn 151, Issue 9, 2010, Pages 4313-4323

  Li, Donghui ^a   Sewer, Marion B ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUCLADESINE; COLCHICINE; CORTICOTROPIN; DIAPH1 PROTEIN, HUMAN; HYDROCORTISONE; PROTEIN BINDING; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TUBULIN MODULATOR;

BIOSYNTHESIS; DRUG EFFECTS; ENDOPLASMIC RETICULUM; FLUORESCENCE MICROSCOPY; GENETICS; HUMAN; METABOLISM; MICROTUBULE; MITOCHONDRION; MUTATION; PROCEDURES; RNA INTERFERENCE; TIME; TRANSPORT AT THE CELLULAR LEVEL; TUMOR CELL LINE; VIDEO MICROSCOPY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADRENOCORTICOTROPIC HORMONE; BIOLOGICAL TRANSPORT; BUCLADESINE; CELL LINE, TUMOR; COLCHICINE; ENDOPLASMIC RETICULUM; HUMANS; HYDROCORTISONE; MICROSCOPY, FLUORESCENCE; MICROSCOPY, VIDEO; MICROTUBULES; MITOCHONDRIA; MUTATION; PROTEIN BINDING; RHOA GTP-BINDING PROTEIN; RNA INTERFERENCE; TIME FACTORS; TUBULIN MODULATORS;

EID: 77956019869     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2010-0044     Document Type: Article

References (82)

1. Arlt W, Stewart PM 2005 Adrenal corticosteroid biosynthesis, metabolism, and action. Endocrinol Metab Clin North Am 34:293-313, viii
2. Miller WL 2002 Androgen biosynthesis from cholesterol to DHEA. Mol Cell Endocrinol 198:7-14
3. Waterman MR, Keeney DS 1996 Diverse molecular mechanisms regulate the expression of steroid hydroxylase genes required for production of ligands for nuclear receptors. In: Jefcoate CR, ed. Physiological functions of cytochrome P450 in relation to structure and regulation. Greenwich, CT: JAI Press, Inc.; 81-102
4. Sewer MB, Waterman MR 2003 ACTH modulation of transcription factors responsible for steroid hydroxylase gene expression in the adrenal cortex. Microsc Res Tech 61:300-307
5. Sewer MB, Dammer EB, Jagarlapudi S 2007 Transcriptional regulation of adrenocortical steroidogenic gene expression. Drug Metab Rev 39:371-388
6. Miller WL 2007 StAR search - what we know about how the steroidogenic acute regulatory protein mediates cholesterol import. Mol Endocrinol 21:589-601
7. Miller WL 2005 Minireview: regulation of steroidogenesis by electron transfer. Endocrinology 146:2544-2550
8. Whitehouse BJ, Gyles SL, Squires PE, Sayed SB, Burns CJ, Persaud SJ, Jones PM 2002 Interdependence of steroidogenesis and shape changes in Y1 adrenocortical cells: studies with inhibitors of phosphoprotein phosphatases. J Endocrinol 172:583-593
9. Shiver TM, Sackett DL, Knipling L, Wolff J 1992 Intermediate filaments and steroidogenesis in adrenal Y-1 cells: acrylamide stimulation of steroid production. Endocrinology 131:201-207
10. Sackett DL, Wolff J 1986 Cyclic AMP-independent stimulation of steroidogenesis in Y-1 adrenal tumor cells by antimitotic agents. Biochim Biophys Acta 888:163-170 (Pubitemid 16026200)
11. Rajan VP, Menon KM 1985 Involvement of microtubules in lipoprotein degradation and utilization for steroidogenesis in cultured rat luteal cells. Endocrinology 117:2408-2416
12. Lee LJ, Chen JS, Ko TL, Wang SM 2001 Mechanism of colchicine-induced steroidogenesis in rat adrenocortical cells. J Cell Biochem 81:162-171
13. Hall PF, Almahbobi G 1997 Roles of microfilaments and intermediate filaments in adrenal steroidogenesis. Microsc Res Tech 36:463-479
14. Cortese F, Wolf J 1978 Cytochalasin-stimulated steroidogenesis from high density lipoproteins. J Cell Biol 77:507-516
15. Rainey WE, Shay JW, Mason JI 1984 The effect of cytochalasin D on steroid production and stress fiber organization in cultured bovine adrenocortical cells. Mol Cell Endocrinol 35:189-197
16. Rainey WE, Kramer RE, Mason JI, Shay JW 1985 The effects of Taxol, a microtubule-stabilizing drug, on steroidogenic cells. J Cell Physiol 123:17-24
17. Denkova R, Ivanov I, Dimitrova M 1992 Microtubules and regulation of granulosa cell steroidogenesis by porcine granulosa cell conditioned medium. Endocr Regul 26:195-199 (Pubitemid 23217868)
18. Carnegie JA, Tsang BK 1987 Microtubules and the calcium-dependent regulation of rat granulosa cell steroidogenesis. Biol Reprod 36:1007-1015
19. Carnegie JA, Dardick I, Tsang BK 1987 Microtubules and the gonadotropic regulation of granulosa cell steroidogenesis. Endocrinology 120:819-828
20. Benis R, Mattson P 1989 Microtubules, organelle transport, and steroidogenesis in cultured adrenocortical tumor cells. 1. An ultrastructural analysis of cells in which basal and ACTH-induced steroidogenesis was inhibited by Taxol. Tissue Cell 21:479-494
21. Benis R, Mattson P 1989 Microtubules, organelle transport, and steroidogenesis in cultured adrenocortical tumor cells. 2. Reversibility of Taxol's inhibition of basal and ACTH-induced steroidogenesis is unaccompanied by reversibility of Taxol-induced changes in cell ultrastructure. Tissue Cell 21:687-698
22. Nan X, Potma EO, Xie XS 2006 Nonperturbative chemical imaging of organelle transport in living cells with coherent anti-strokes Raman scattering microscopy. Biophys J 91:728-735
23. Morris RL, Hollenbeck PJ 1995 Axonal transport of mitochondria along microtubules and F-actin in living vertebrate neurons. J Cell Biol 131:1315-1326
24. Ball EH, Singer SJ 1982 Mitochondria are associated with microtubules and not with intermediate filaments in cultured fibroblasts. Proc Natl Acad Sci USA 79:123-126 (Pubitemid 12181498)
25. Yi M, Weaver D, Hajnóczky G 2004 Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 167:661-672
26. Summerhayes IC, Wong D, Chen LB 1983 Effect of microtubules and intermediate filaments on mitochondrial distribution. J Cell Sci 61:87-105
27. Stromer MH, Bendayan M 1990 Immunocytochemical identification of cytoskeletal linkages to smooth muscle cell nuclei and mitochondria. Cell Motil Cytoskeleton 17:11-18 (Pubitemid 20313041)
28. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N 1998 Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell 93:1147-1158
29. Miki H, Okada Y, Hirokawa N 2005 Analysis of the kinesin superfamily: insights into the structure and function. Trends Cell Biol 15:467-476
30. Kwok BH, Kapoor TM 2007 Microtubule flux: drivers wanted. Curr Opin Cell Biol 19:36-42
31. Hollenbeck PJ, Saxton WM 2005 The axonal transport of mitochondria. J Cell Sci 118:5411-5419
32. Gross SP 2004 Hither and yon: a review of bi-directional microtubule-based transport. Phys Biol 1:R1-R11
33. Ridley AJ 2006 Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol 16:522-529
34. Raftopoulou M, Hall A 2004 Cell migration: Rho GTPases lead the way. Dev Biol 265:23-32 (Pubitemid 38018819)
35. Jaffe AB, Hall A 2005 Rho GTPases: biochemistry and biology. Annu Rev Cell Dev Biol 21:247-269
36. Hall A 2005 Rho GTPases and the control of cell behaviour. Biochem Soc Trans 33:891-895
37. Watanabe N, Madaule P, Reid T, Ishizaki T, Watanabe G, Kakizuka A, Saito Y, Nakao K, Jockusch BM, Narumiya S 1997 p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J 16:3044-3056
38. Rose R, Weyand M, Lammers M, Ishizaki T, Ahmadian MR, Wittinghofer A 2005 Structural and mechanistic insights into the interaction between Rho and mammalian Dia. Nature 435:513-518
39. Otomo T, Otomo C, Tomchick DR, Machius M, Rosen MK 2005 Structural basis of Rho GTPase-mediated activation of the formin mDia1. Mol Cell 18:273-281
40. Li F, Higgs HN 2005 Dissecting requirements for auto-inhibition of actin nucleation by the formin, mDia1. J Biol Chem 280:6986-6992 (Pubitemid 40341254)
41. Li F, Higgs HN 2003 The mouse formin mDia1 is a potent actin nucleation factor regulated by autoinhibition. Curr Biol 13:1335-1340
42. Alberts AS 2001 Identification of a carboxyl-terminal diaphanous-related formin homology protein autoregulatory domain. J Biol Chem 276:2824-2830
43. Watanabe N, Kato T, Fujita A, Ishizaki T, Narumiya S 1999 Cooperation between mDia1 and ROCK in Rho-induced actin reorganization. Nat Cell Biol 1:136-143 (Pubitemid 129656017)
44. Ishizaki T, Morishima Y, Okamoto M, Furuyashiki T, Kato T, Narumiya S 2001 Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat Cell Biol 3:8-14
45. Lammers M, Rose R, Scrima A, Wittinghofer A 2005 The regulation of mDia1 by autoinhibition and its release by Rho*GTP. EMBO J 24:4176-4187
46. Rainey WE, Bird IM, Mason JI 1994 The NCI-H295 cell line: a pluripotent model for human adrenocortical studies. Mol Cell Endocrinol 100:45-50
47. Staels B, Hum DW, Miller WL 1993 Regulation of steroidogenesis in NCI-H295 cells: a cellular model of the human fetal adrenal. Mol Endocrinol 7:423-433 (Pubitemid 23104530)
48. Fehrenbacher KL, Yang HC, Gay AC, Huckaba TM, Pon LA 2004 Live cell imaging of mitochondrial movement along actin cables in budding yeast. Curr Biol 14:1996-2004
49. Knowles MK, Guenza MG, Capaldi RA, Marcus AH 2002 Cytoskeletal- assisted dynamics of the mitochondrial reticulum in living cells. Proc Natl Acad Sci USA 99:14772-14777
50. Shprung T, Gozes I 2009 A novel method for analyzing mitochondrial movement: inhibition by paclitaxel in a pheochromocytoma cell model. J Mol Neurosci 37:254-262
51. Janes ME, Chu KM, Clark AJ, King PJ 2008 Mechanisms of adrenocorticotropin- induced activation of extracellularly regulated kinase 1/2 mitogen-activated protein kinase in the human H295R adrenal cell line. Endocrinology 149:1898-1905
52. Mountjoy KG, Bird IM, Rainey WE, Cone RD 1994 ACTH induces up-regulation of ACTH receptor mRNA in mouse and human adrenocortical cell lines. Mol Cell Endocrinol 99:R17-R20
53. Bird IM, Hanley NA, Word RA, Mathis JM, McCarthy JL, Mason JI, Rainey WE 1993 Human NCI-H295 adrenocortical carcinoma cells; a model for angiotensin-II-responsive aldosterone secretion. Endocrinology 133:1555-1561
54. Glater EE, Megeath LJ, Stowers RS, Schwarz TL 2006 Axonal transport of mitochondria requires milton to recruit kinesin heavy chain and is light chain independent. J Cell Biol 173:545-557
55. 2+ signals? Sci STKE 280:pe18
56. Fransson S, Ruusala A, Aspenström P 2006 The atypical Rho GT-Pases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun 344:500-510
57. Boldogh IR, Pon LA 2007 Mitochondria on the move. Trends Cell Biol 17:502-510
58. Qiu RG, Chen J, McCormick F, Symons M 1995 A role for Rho in Ras transformation. Proc Natl Acad Sci USA 92:11781-11785
59. Lang P, Gesbert F, Delespine-Carmagnat M, Stancou R, Pouchelet M, Bertoglio J 1996 Protein kinase A phosphorylation of RhoA mediates the morphological and functional effects of cyclic AMP in cytotoxic lymphocytes. EMBO J 15:510-519
60. Murdoch WJ 1996 Microtubular dynamics in granulosa cells of periovulatory follicles and granulosa-derived (large) lutein cells of sheep: relationships to the steroidogenic folliculo-luteal shift and functional luteolysis. Biol Reprod 54:1135-1140
61. Gregoraszczuk EL, Stlomczynska M 1996 The cytoskeleton proteins and LH-regulated steroidogenesis of porcine luteal cells. Folia Histochem Cytobiol 34:35-39
62. Feuilloley M, Contesse V, Lefebvre H, Delarue C, Vaudry H 1994 Effects of selective disruption of cytoskeletal elements on steroid secretion by human adrenocortical slices. Am J Physiol 266:E202-E210 (Pubitemid 24099272)
63. Gasman S, Kalaidzidis Y, Zerial M 2003 RhoD regulates endosome dynamics through Diaphanous-related Formin and Src tyrosine kinase. Nat Cell Biol 5:195-204
64. Grosse R, Copeland JW, Newsome TP, Way M, Treisman R 2003 A role for VASP in RhoA-Diaphanous signalling to actin dynamics and SRF activity. EMBO J 22:3050-3061 (Pubitemid 36758625)
65. Gopinath SD, Narumiya S, Dhawan J 2007 The RhoA effector mDiaphanous regulates MyoD expression and cell cycle progression via SRF-dependent and SRF-independent pathways. J Cell Sci 120:3086-3098
66. Copeland JW, Treisman R 2002 The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization. Mol Biol Cell 13:4088-4099
67. Dong JM, Leung T, Manser E, Lim L 1998 cAMP-induced morphological changes are counteracted by the activated RhoA small GTPase and the Rho kinase ROKα. J Biol Chem 273:22554-22562
68. Qiao J, Huang F, Lum H 2003 PKA inhibits RhoA: a protection mechanism against endothelial barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 284:L972-L980
69. Chen Y, Wang Y, Yu H, Wang F, Xu W 2005 The cross talk between protein kinase A- and RhoA-mediated signaling in cancer cells. Exp Biol Med 230:731-741 (Pubitemid 41565942)
70. Nusser N, Gosmanova E, Makarova N, Fujiwara Y, Yang L, Guo F, Luo Y, Zheng Y, Tigyi G 2006 Serine phosphorylation differentially affects RhoA binding to effectors: implications to NGF-induced neurite outgrowth. Cell Signal 18:704-714
71. Rolli-Derkinderen M, Sauzeau V, Boyer L, Lemichez E, Baron C, Henrion D, Loirand G, Pacaud P 2005 Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells. Circ Res 96:1152-1160
72. Bione S, Sala C, Manzini C, Arrigo G, Zuffardi O, Banfi S, Borsani G, Jonveaux P, Philippe C, Zuccotti M, Ballabio A, Toniolo D 1998 A human homologue of the Drosophila melanogaster diaphanous gene is disrupted in a patient with premature ovarian failure: evidence for conserved function in oogenesis and implications for human sterility. Am J Hum Genet 62:533-541
73. Lartey J, Smith M, Pawade J, Strachan B, Mellor H, López Bernal A 2007 Up-regulation of myometrial RHO effector proteins (PKN1 and DIAPH1) and CPI-17 (PPP1R14A) phosphorylation in human pregnancy is associated with increased GTP-RHOA in spontaneous preterm labor. Biol Reprod 76:971-982
74. Sir-Petermann T, Maliqueo M, Angel B, Lara HE, Pérez-Bravo F, Recabarren SE 2002 Maternal serum androgens in pregnant women with polycystic ovary syndrome: possible implications in prenatal androgenization. Hum Reprod 17:2573-2579 (Pubitemid 35174106)
75. Yildiz BO, Azziz R 2007 The adrenal and polycystic ovary syndrome. Rev Endocr Metab Disord 8:331-342
76. Steckler T, Wang J, Bartol FF, Roy SK, Padmanabhan V 2005 Fetal programming: prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 146:3185-3193
77. Sarma HN, Manikkam M, Herkimer C, Dell'Orco J, Welch KB, Foster DL, Padmanabhan V 2005 Fetal programming: excess prenatal testosterone reduces postnatal luteinizing hormone, but not follicle-stimulating hormone responsiveness, to estradiol negative feedback in the female. Endocrinology 146:4281-4291
78. Padmanabhan V, Manikkam M, Recabarren S, Foster D 2006 Prenatal testosterone programs reproductive and metabolic dysfunction in the female. Mol Cell Endocrinol 246:165-174
79. Tee MK, Dong Q, Miller WL 2008 Pathways leading to phosphorylation of P450c17 and to the posttranslational regulation of androgen biosynthesis. Endocrinology 149:2667-2677
80. Asif AR, Steffgen J, Metten M, Grunewald RW, Müller GA, Bahn A, Burckhardt G, Hagos Y 2005 Presence of organic anion transporters 3 (OAT3) and 4 (OAT4) in human adrenocortical cells. Pflugers Arch 450:88-95
81. Asif AR, Ljubojevic M, Sabolic I, Shnitsar V, Metten M, Anzai N, Müller GA, Burckhardt G, Hagos Y 2006 Regulation of steroid hormone biosynthesis enzymes and organic anion transporters by forskolin and DHEA-S treatment in adrenocortical cells. Am J Physiol Endocrinol Metab 291:E1351-E1359
82. Olkkonen VM, Levine TP 2004 Oxysterol binding proteins: in more than one place at one time? Biochem Cell Biol 82:87-98