Back to your heart: Ubiquitin proteasome system-regulated signal transduction

Journal of Molecular and Cellular Cardiology

Volumn 52, Issue 3, 2012, Pages 526-537

  Portbury, Andrea L ^a   Ronnebaum, Sarah M ^a   Zungu, Makhosazane ^a   Patterson, Cam ^a   Willis, Monte S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

C Jun; Calcineurin; Cardiac hypertrophy; Diabetes; Estrogen receptor; FOXO; Ischemia; JNK; P53; Proteasome; Ubiquitin

Indexed keywords

ATROGIN 1; CALCINEURIN; DESMIN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MUSCLE RING FINGER 1 PROTEIN; PROTEIN MDM2; PROTEIN P53; PROTEOME; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR NFAT; UBIQUITIN;

APOPTOSIS; CONGESTIVE CARDIOMYOPATHY; DIABETES MELLITUS; HEART DEVELOPMENT; HEART DILATATION; HEART FAILURE; HEART INFARCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; HUMAN; HYPERGLYCEMIA; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REPERFUSION INJURY; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; UBIQUITINATION; UPREGULATION;

ANIMALS; CALCINEURIN; FORKHEAD TRANSCRIPTION FACTORS; HEART; HUMANS; MAP KINASE SIGNALING SYSTEM; MYOCARDIUM; PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITINATION;

EID: 84857630000     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.10.023     Document Type: Review

References (156)

1. Raiborg C., Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458:445-452.
2. Bhoj V.G., Chen Z.J. Ubiquitylation in innate and adaptive immunity. Nature 2009, 458:430-437.
3. Hofmann R.M., Pickart C.M. In vitro assembly and recognition of Lys-63 polyubiquitin chains. J Biol Chem 2001, 276:27936-27943.
4. Hoeller D., Dikic I. Targeting the ubiquitin system in cancer therapy. Nature 2009, 458:438-444.
5. Greenwood D.D. Critical bandwidth and consonance in relation to cochlear frequency-position coordinates. Hear Res 1991, 54:164-208.
6. Heemers H.V., Tindall D.J. Unraveling the complexities of androgen receptor signaling in prostate cancer cells. Cancer Cell 2009, 15:245-247.
7. Ikeda F., Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein Modifications: Beyond the Usual Suspects' review series. EMBO Rep 2008, 9:536-542.
8. Hicke L. Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2001, 2:195-201.
9. Trotman L.C., Wang X., Alimonti A., Chen Z., Teruya-Feldstein J., Yang H., et al. Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 2007, 128:141-156.
10. Hicke L. Gettin' down with ubiquitin: turning off cell-surface receptors, transporters and channels. Trends Cell Biol 1999, 9:107-112.
11. Bogoyevitch M.A., Gillespie-Brown J., Ketterman A.J., Fuller S.J., Ben-Levy R., Ashworth A., et al. Stimulation of the stress-activated mitogen-activated protein kinase subfamilies in perfused heart. p38/RK mitogen-activated protein kinases and c-Jun N-terminal kinases are activated by ischemia/reperfusion. Circ Res 1996, 79:162-173.
12. Petrich B.G., Molkentin J.D., Wang Y. Temporal activation of c-Jun N-terminal kinase in adult transgenic heart via cre-loxP-mediated DNA recombination. FASEB J 2003, 17:749-751.
13. Goldsmith Z.G., Dhanasekaran D.N. G protein regulation of MAPK networks. Oncogene 2007, 26:3122-3142.
14. Pandur P., Maurus D., Kuhl M. Increasingly complex: new players enter the Wnt signaling network. Bioessays 2002, 24:881-884.
15. Rose B.A., Force T., Wang Y. Mitogen-activated protein kinase signaling in the heart: angels versus demons in a heart-breaking tale. Physiol Rev 2010, 90:1507-1546.
16. Pandur P., Lasche M., Eisenberg L.M., Kuhl M. Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 2002, 418:636-641.
17. Zhou W., Lin L., Majumdar A., Li X., Zhang X., Liu W., et al. Modulation of morphogenesis by noncanonical Wnt signaling requires ATF/CREB family-mediated transcriptional activation of TGFbeta2. Nat Genet 2007, 39:1225-1234.
18. Sugden P.H., Clerk A. "Stress-responsive" mitogen-activated protein kinases (c-Jun N-terminal kinases and p38 mitogen-activated protein kinases) in the myocardium. Circ Res 1998, 83:345-352.
19. Yin T., Sandhu G., Wolfgang C.D., Burrier A., Webb R.L., Rigel D.F., et al. Tissue-specific pattern of stress kinase activation in ischemic/reperfused heart and kidney. J Biol Chem 1997, 272:19943-19950.
20. Hreniuk D., Garay M., Gaarde W., Monia B.P., McKay R.A., Cioffi C.L. Inhibition of c-Jun N-terminal kinase 1, but not c-Jun N-terminal kinase 2, suppresses apoptosis induced by ischemia/reoxygenation in rat cardiac myocytes. Mol Pharmacol 2001, 59:867-874.
21. Knight R.J., Buxton D.B. Stimulation of c-Jun kinase and mitogen-activated protein kinase by ischemia and reperfusion in the perfused rat heart. Biochem Biophys Res Commun 1996, 218:83-88.
22. Laderoute K.R., Webster K.A. Hypoxia/reoxygenation stimulates Jun kinase activity through redox signaling in cardiac myocytes. Circ Res 1997, 80:336-344.
23. Clerk A., Fuller S.J., Michael A., Sugden P.H. Stimulation of "stress-regulated" mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J Biol Chem 1998, 273:7228-7234.
24. Laine A., Ronai Z. Ubiquitin chains in the ladder of MAPK signaling. Sci STKE 2005, 2005:re5.
25. Li H.H., Du J., Fan Y.N., Zhang M.L., Liu D.P., Li L., et al. The ubiquitin ligase MuRF1 protects against cardiac ischemia/reperfusion injury by its proteasome-dependent degradation of phospho-c-Jun. Am J Pathol 2011, 178:1043-1058.
26. Xie P., Guo S., Fan Y., Zhang H., Gu D., Li H. Atrogin-1/MAFbx enhances simulated ischemia/reperfusion-induced apoptosis in cardiomyocytes through degradation of MAPK phosphatase-1 and sustained JNK activation. J Biol Chem 2009, 284:5488-5496.
27. Guo B., Yang S.H., Witty J., Sharrocks A.D. Signalling pathways and the regulation of SUMO modification. Biochem Soc Trans 2007, 35:1414-1418.
28. Yang S.H., Sharrocks A.D. Convergence of the SUMO and MAPK pathways on the ETS-domain transcription factor Elk-1. Biochem Soc Symp 2006, 121-129.
29. Xia Y., Wang J., Xu S., Johnson G.L., Hunter T., Lu Z. MEKK1 mediates the ubiquitination and degradation of c-Jun in response to osmotic stress. Mol Cell Biol 2007, 27:510-517.
30. Lu Z., Xu S., Joazeiro C., Cobb M.H., Hunter T. The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Mol Cell 2002, 9:945-956.
31. Nateri A.S., Riera-Sans L., Da Costa C., Behrens A. The ubiquitin ligase SCFFbw7 antagonizes apoptotic JNK signaling. Science 2004, 303:1374-1378.
32. Wertz I.E., O'Rourke K.M., Zhang Z., Dornan D., Arnott D., Deshaies R.J., et al. Human de-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 2004, 303:1371-1374.
33. Gao M., Labuda T., Xia Y., Gallagher E., Fang D., Liu Y.C., et al. Jun turnover is controlled through JNK-dependent phosphorylation of the E3 ligase Itch. Science 2004, 306:271-275.
34. Dickens M., Rogers J.S., Cavanagh J., Raitano A., Xia Z., Halpern J.R., et al. A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 1997, 277:693-696.
35. Whitmarsh A.J., Cavanagh J., Tournier C., Yasuda J., Davis R.J. A mammalian scaffold complex that selectively mediates MAP kinase activation. Science 1998, 281:1671-1674.
36. Wei N., Deng X.W. Making sense of the COP9 signalosome. A regulatory protein complex conserved from Arabidopsis to human. Trends Genet 1999, 15:98-103.
37. Fang D., Elly C., Gao B., Fang N., Altman Y., Joazeiro C., et al. Dysregulation of T lymphocyte function in itchy mice: a role for Itch in TH2 differentiation. Nat Immunol 2002, 3:281-287.
38. Perry W.L., Hustad C.M., Swing D.A., O'Sullivan T.N., Jenkins N.A., Copeland N.G. The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice. Nat Genet 1998, 18:143-146.
39. Dong C., Yang D.D., Wysk M., Whitmarsh A.J., Davis R.J., Flavell R.A. Defective T cell differentiation in the absence of Jnk1. Science 1998, 282:2092-2095.
40. Dong C., Yang D.D., Tournier C., Whitmarsh A.J., Xu J., Davis R.J., et al. JNK is required for effector T-cell function but not for T-cell activation. Nature 2000, 405:91-94.
41. Wang J. Cardiac function and disease: emerging role of small ubiquitin-related modifier. Wiley Interdiscip Rev Syst Biol Med 2011, 3:446-457.
42. Muller S., Berger M., Lehembre F., Seeler J.S., Haupt Y., Dejean A. c-Jun and p53 activity is modulated by SUMO-1 modification. J Biol Chem 2000, 275:13321-13329.
43. Klee C.B., Crouch T.H., Krinks M.H. Calcineurin: a calcium- and calmodulin-binding protein of the nervous system. Proc Natl Acad Sci U S A 1979, 76:6270-6273.
44. Okamura H., Aramburu J., Garcia-Rodriguez C., Viola J.P., Raghavan A., Tahiliani M., et al. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Mol Cell 2000, 6:539-550.
45. Suzuki E., Nishimatsu H., Satonaka H., Walsh K., Goto A., Omata M., et al. Angiotensin II induces myocyte enhancer factor 2- and calcineurin/nuclear factor of activated T cell-dependent transcriptional activation in vascular myocytes. Circ Res 2002, 90:1004-1011.
46. Molkentin J.D., Lu J.R., Antos C.L., Markham B., Richardson J., Robbins J., et al. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 1998, 93:215-228.
47. Chin E.R., Olson E.N., Richardson J.A., Yang Q., Humphries C., Shelton J.M., et al. A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 1998, 12:2499-2509.
48. Gwack Y., Sharma S., Nardone J., Tanasa B., Iuga A., Srikanth S., et al. A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 2006, 441:646-650.
49. Okamura H., Garcia-Rodriguez C., Martinson H., Qin J., Virshup D.M., Rao A. A conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol Cell Biol 2004, 24:4184-4195.
50. Fan Y., Xie P., Zhang T., Zhang H., Gu D., She M., et al. Regulation of the stability and transcriptional activity of NFATc4 by ubiquitination. FEBS Lett 2008, 582:4008-4014.
51. Ni Y.G., Wang N., Cao D.J., Sachan N., Morris D.J., Gerard R.D., et al. FoxO transcription factors activate Akt and attenuate insulin signaling in heart by inhibiting protein phosphatases. Proc Natl Acad Sci U S A 2007, 104:20517-20522.
52. Li H.H., Willis M.S., Lockyer P., Miller N., McDonough H., Glass D.J., et al. Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J Clin Invest 2007, 117:3211-3223.
53. Li H.H., Kedar V., Zhang C., McDonough H., Arya R., Wang D.Z., et al. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest 2004, 114:1058-1071.
54. Tang M., Li J., Huang W., Su H., Liang Q., Tian Z., et al. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res 2010, 88:424-433.
55. Li F., Wang X., Yi X.P., Gerdes A.M. Structural basis of ventricular remodeling: role of the myocyte. Curr Heart Fail Rep 2004, 1:5-8.
56. Liu J., Tang M., Mestril R., Wang X. Aberrant protein aggregation is essential for a mutant desmin to impair the proteolytic function of the ubiquitin-proteasome system in cardiomyocytes. J Mol Cell Cardiol 2006, 40:451-454.
57. Liu J., Chen Q., Huang W., Horak K.M., Zheng H., Mestril R., et al. Impairment of the ubiquitin-proteasome system in desminopathy mouse hearts. FASEB J 2006, 20:362-364.
58. Papanicolaou K.N., Izumiya Y., Walsh K. Forkhead transcription factors and cardiovascular biology. Circ Res 2008, 102:16-31.
59. Maiese K., Hou J., Chong Z.Z., Shang Y.C. A fork in the path: developing therapeutic inroads with FoxO proteins. Oxid Med Cell longev 2009, 2:119-129.
60. Ronnebaum S.M., Patterson C. The FoxO family in cardiac function and dysfunction. Annu Rev Physiol 2010, 72:81-94.
61. Tremblay M.L., Giguere V. Phosphatases at the heart of FoxO metabolic control. Cell Metab 2008, 7:101-103.
62. Colao A. The GH-IGF-I axis and the cardiovascular system: clinical implications. Clin Endocrinol 2008, 69:347-358.
63. Alessi D.R., James S.R., Downes C.P., Holmes A.B., Gaffney P.R., Reese C.B., et al. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr Biol 1997, 7:261-269.
64. Sarbassov D.D., Guertin D.A., Ali S.M., Sabatini D.M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307:1098-1101.
65. Meier R., Alessi D.R., Cron P., Andjelkovic M., Hemmings B.A. Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase Bbeta. J Biol Chem 1997, 272:30491-30497.
66. Brownawell A.M., Kops G.J., Macara I.G., Burgering B.M. Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the forkhead transcription factor AFX. Mol Cell Biol 2001, 21:3534-3546.
67. Biggs W.H., Meisenhelder J., Hunter T., Cavenee W.K., Arden K.C. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci U S A 1999, 96:7421-7426.
68. Brunet A., Kanai F., Stehn J., Xu J., Sarbassova D., Frangioni J.V., et al. 14-3-3 transits to the nucleus and participates in dynamic nucleocytoplasmic transport. J Cell Biol 2002, 156:817-828.
69. Plas D.R., Thompson C.B. Akt activation promotes degradation of tuberin and FOXO3a via the proteasome. J Biol Chem 2003, 278:12361-12366.
70. Huang H., Regan K.M., Wang F., Wang D., Smith D.I., van Deursen J.M., et al. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc Natl Acad Sci U S A 2005, 102:1649-1654.
71. Li F., Xie P., Fan Y., Zhang H., Zheng L., Gu D., et al. C terminus of Hsc70-interacting protein promotes smooth muscle cell proliferation and survival through ubiquitin-mediated degradation of FoxO1. J Biol Chem 2009, 284:20090-20098.
72. Yang J.Y., Zong C.S., Xia W., Yamaguchi H., Ding Q., Xie X., et al. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat Cell Biol 2008, 10:138-148.
73. Hu M.C., Lee D.F., Xia W., Golfman L.S., Ou-Yang F., Yang J.Y., et al. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 2004, 117:225-237.
74. Kato S., Ding J., Pisck E., Jhala U.S., Du K. COP1 functions as a FoxO1 ubiquitin E3 ligase to regulate FoxO1-mediated gene expression. J Biol Chem 2008, 283:35464-35473.
75. Brenkman A.B., de Keizer P.L., van den Broek N.J., Jochemsen A.G., Burgering B.M. Mdm2 induces mono-ubiquitination of FOXO4. PLoS One 2008, 3:e2819.
76. van der Horst A., de Vries-Smits A.M., Brenkman A.B., van Triest M.H., van den Broek N., Colland F., et al. FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat Cell Biol 2006, 8:1064-1073.
77. Morris J.B., Kenney B., Huynh H., Woodcock E.A. Regulation of the proapoptotic factor FOXO1 (FKHR) in cardiomyocytes by growth factors and alpha1-adrenergic agonists. Endocrinology 2005, 146:4370-4376.
78. Yue T.L., Bao W., Gu J.L., Cui J., Tao L., Ma X.L., et al. Rosiglitazone treatment in Zucker diabetic Fatty rats is associated with ameliorated cardiac insulin resistance and protection from ischemia/reperfusion-induced myocardial injury. Diabetes 2005, 54:554-562.
79. Chen Y., Park S., Li Y., Missov E., Hou M., Han X., et al. Alterations of gene expression in failing myocardium following left ventricular assist device support. Physiol Genomics 2003, 14:251-260.
80. Hannenhalli S., Putt M.E., Gilmore J.M., Wang J., Parmacek M.S., Epstein J.A., et al. Transcriptional genomics associates FOX transcription factors with human heart failure. Circulation 2006, 114:1269-1276.
81. Philip-Couderc P., Tavares N.I., Roatti A., Lerch R., Montessuit C., Baertschi A.J. Forkhead transcription factors coordinate expression of myocardial KATP channel subunits and energy metabolism. Circ Res 2008, 102:e20-e35.
82. Sengupta A., Molkentin J.D., Paik J.H., DePinho R.A., Yutzey K.E. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 2011, 286:7468-7478.
83. Pikkarainen S., Kennedy R.A., Marshall A.K., Thamel L., Lay K., Kriz T.A., et al. Regulation of expression of the rat orthologue of mouse double minute 2 (MDM2) by H(2)O(2)-induced oxidative stress in neonatal rat cardiac myocytes. J Biol Chem 2009, 284:27195-27210.
84. Zhang C., Xu Z., He X.R., Michael L.H., Patterson C. CHIP, a cochaperone/ubiquitin ligase that regulates protein quality control, is required for maximal cardioprotection after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 2005, 288:H2836-H2842.
85. Kubbutat M.H., Jones S.N., Vousden K.H. Regulation of p53 stability by Mdm2. Nature 1997, 387:299-303.
86. Honda R., Tanaka H., Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997, 420:25-27.
87. Li M., Brooks C.L., Wu-Baer F., Chen D., Baer R., Gu W. Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 2003, 302:1972-1975.
88. Lohrum M.A., Woods D.B., Ludwig R.L., Balint E., Vousden K.H. C-terminal ubiquitination of p53 contributes to nuclear export. Mol Cell Biol 2001, 21:8521-8532.
89. Manfredi J.J. The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev 2010, 24:1580-1589.
90. Rodriguez M.S., Desterro J.M., Lain S., Lane D.P., Hay R.T. Multiple C-terminal lysine residues target p53 for ubiquitin-proteasome-mediated degradation. Mol Cell Biol 2000, 20:8458-8467.
91. Krummel K.A., Lee C.J., Toledo F., Wahl G.M. The C-terminal lysines fine-tune P53 stress responses in a mouse model but are not required for stability control or transactivation. Proc Natl Acad Sci U S A 2005, 102:10188-10193.
92. Feng L., Lin T., Uranishi H., Gu W., Xu Y. Functional analysis of the roles of posttranslational modifications at the p53 C terminus in regulating p53 stability and activity. Mol Cell Biol 2005, 25:5389-5395.
93. Chan W.M., Mak M.C., Fung T.K., Lau A., Siu W.Y., Poon R.Y. Ubiquitination of p53 at multiple sites in the DNA-binding domain. Mol Cancer Res 2006, 4:15-25.
94. Li M., Chen D., Shiloh A., Luo J., Nikolaev A.Y., Qin J., et al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416:648-653.
95. Ringshausen I., O'Shea C.C., Finch A.J., Swigart L.B., Evan G.I. Mdm2 is critically and continuously required to suppress lethal p53 activity in vivo. Cancer Cell 2006, 10:501-514.
96. McDonough H., Patterson C. CHIP: a link between the chaperone and proteasome systems. Cell Stress Chaperones 2003, 8:303-308.
97. Weger S., Hammer E., Heilbronn R. Topors acts as a SUMO-1 E3 ligase for p53 in vitro and in vivo. FEBS Lett 2005, 579:5007-5012.
98. Rajendra R., Malegaonkar D., Pungaliya P., Marshall H., Rasheed Z., Brownell J., et al. Topors functions as an E3 ubiquitin ligase with specific E2 enzymes and ubiquitinates p53. J Biol Chem 2004, 279:36440-36444.
99. Yang W., Rozan L.M., McDonald E.R., Navaraj A., Liu J.J., Matthew E.M., et al. CARPs are ubiquitin ligases that promote MDM2-independent p53 and phospho-p53ser20 degradation. J Biol Chem 2007, 282:3273-3281.
100. Chen D., Kon N., Li M., Zhang W., Qin J., Gu W. ARF-BP1/Mule is a critical mediator of the ARF tumor suppressor. Cell 2005, 121:1071-1083.
101. Grossman S.R., Deato M.E., Brignone C., Chan H.M., Kung A.L., Tagami H., et al. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 2003, 300:342-344.
102. Yamasaki S., Yagishita N., Sasaki T., Nakazawa M., Kato Y., Yamadera T., et al. Cytoplasmic destruction of p53 by the endoplasmic reticulum-resident ubiquitin ligase 'Synoviolin'. EMBO J 2007, 26:113-122.
103. Chatterjee A., Mir S.A., Dutta D., Mitra A., Pathak K., Sarkar S. Analysis of p53 and NF-kappaB signaling in modulating the cardiomyocyte fate during hypertrophy. J Cell Physiol 2010.
104. Sano M., Minamino T., Toko H., Miyauchi H., Orimo M., Qin Y., et al. p53-induced inhibition of Hif-1 causes cardiac dysfunction during pressure overload. Nature 2007, 446:444-448.
105. Birks E.J., Latif N., Enesa K., Folkvang T., Luong le A., Sarathchandra P., et al. Elevated p53 expression is associated with dysregulation of the ubiquitin-proteasome system in dilated cardiomyopathy. Cardiovasc Res 2008, 79:472-480.
106. Naito A.T., Okada S., Minamino T., Iwanaga K., Liu M.L., Sumida T., et al. Promotion of CHIP-mediated p53 degradation protects the heart from ischemic injury. Circ Res 2010, 106:1692-1702.
107. Yu X.Y., Geng Y.J., Liang J.L., Lin Q.X., Lin S.G., Zhang S., et al. High levels of glucose induce apoptosis in cardiomyocyte via epigenetic regulation of the insulin-like growth factor receptor. Exp Cell Res 2010, 316:2903-2909.
108. Fiordaliso F., Leri A., Cesselli D., Limana F., Safai B., Nadal-Ginard B., et al. Hyperglycemia activates p53 and p53-regulated genes leading to myocyte cell death. Diabetes 2001, 50:2363-2375.
109. Kobayashi S., Mao K., Zheng H., Wang X., Patterson C., O'Connell T.D., et al. Diminished GATA4 protein levels contribute to hyperglycemia-induced cardiomyocyte injury. J Biol Chem 2007, 282:21945-21952.
110. Couse J.F., Lindzey J., Grandien K., Gustafsson J.A., Korach K.S. Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinology 1997, 138:4613-4621.
111. Lindberg M.K., Moverare S., Skrtic S., Gao H., Dahlman-Wright K., Gustafsson J.A., et al. Estrogen receptor (ER)-beta reduces ERalpha-regulated gene transcription, supporting a "ying yang" relationship between ERalpha and ERbeta in mice. Mol Endocrinol 2003, 17:203-208.
112. Saito T., Ciobotaru A., Bopassa J.C., Toro L., Stefani E., Eghbali M. Estrogen contributes to gender differences in mouse ventricular repolarization. Circ Res 2009, 105:343-352.
113. Meyer M.R., Barton M. ERalpha, ERbeta, and gpER: novel aspects of oestrogen receptor signalling in atherosclerosis. Cardiovasc Res 2009, 83:605-610.
114. Adams M.R., Kaplan J.R., Manuck S.B., Koritnik D.R., Parks J.S., Wolfe M.S., et al. Inhibition of coronary artery atherosclerosis by 17-beta estradiol in ovariectomized monkeys. Lack of an effect of added progesterone. Arteriosclerosis 1990, 10:1051-1057.
115. Murphy E. Estrogen signaling and cardiovascular disease. Circ Res 2011, 109:687-696.
116. Blanquart C., Barbier O., Fruchart J.C., Staels B., Glineur C. Peroxisome proliferator-activated receptor alpha (PPARalpha) turnover by the ubiquitin-proteasome system controls the ligand-induced expression level of its target genes. J Biol Chem 2002, 277:37254-37259.
117. Dace A., Zhao L., Park K.S., Furuno T., Takamura N., Nakanishi M., et al. Hormone binding induces rapid proteasome-mediated degradation of thyroid hormone receptors. Proc Natl Acad Sci U S A 2000, 97:8985-8990.
118. Boudjelal M., Wang Z., Voorhees J.J., Fisher G.J. Ubiquitin/proteasome pathway regulates levels of retinoic acid receptor gamma and retinoid X receptor alpha in human keratinocytes. Cancer Res 2000, 60:2247-2252.
119. Eckert R.L., Mullick A., Rorke E.A., Katzenellenbogen B.S. Estrogen receptor synthesis and turnover in MCF-7 breast cancer cells measured by a density shift technique. Endocrinology 1984, 114:629-637.
120. Alarid E.T., Bakopoulos N., Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 1999, 13:1522-1534.
121. Devin-Leclerc J., Meng X., Delahaye F., Leclerc P., Baulieu E.E., Catelli M.G. Interaction and dissociation by ligands of estrogen receptor and Hsp90: the antiestrogen RU 58668 induces a protein synthesis-dependent clustering of the receptor in the cytoplasm. Mol Endocrinol 1998, 12:842-854.
122. Dauvois S., Danielian P.S., White R., Parker M.G. Antiestrogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc Natl Acad Sci U S A 1992, 89:4037-4041.
123. Magro E.M., Martinez J.M. Statistical trial of succinylcholine. Rev Esp Anestesiol Reanim 1975, 22:1-35.
124. Laios I., Journe F., Laurent G., Nonclercq D., Toillon R.A., Seo H.S., et al. Mechanisms governing the accumulation of estrogen receptor alpha in MCF-7 breast cancer cells treated with hydroxytamoxifen and related antiestrogens. J Steroid Biochem Mol Biol 2003, 87:207-221.
125. Alarid E.T., Preisler-Mashek M.T., Solodin N.M. Thyroid hormone is an inhibitor of estrogen-induced degradation of estrogen receptor-alpha protein: estrogen-dependent proteolysis is not essential for receptor transactivation function in the pituitary. Endocrinology 2003, 144:3469-3476.
126. Tsai K.S., Yang R.S., Liu S.H. Benzo[a]pyrene regulates osteoblast proliferation through an estrogen receptor-related cyclooxygenase-2 pathway. Chem Res Toxicol 2004, 17:679-684.
127. Galigniana M.D., Harrell J.M., Housley P.R., Patterson C., Fisher S.K., Pratt W.B. Retrograde transport of the glucocorticoid receptor in neurites requires dynamic assembly of complexes with the protein chaperone hsp90 and is linked to the CHIP component of the machinery for proteasomal degradation. Brain Res Mol Brain Res 2004, 123:27-36.
128. Stenoien D.L., Nye A.C., Mancini M.G., Patel K., Dutertre M., O'Malley B.W., et al. Ligand-mediated assembly and real-time cellular dynamics of estrogen receptor alpha-coactivator complexes in living cells. Mol Cell Biol 2001, 21:4404-4412.
129. Shang Y., Hu X., DiRenzo J., Lazar M.A., Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000, 103:843-852.
130. Reid G., Hubner M.R., Metivier R., Brand H., Denger S., Manu D., et al. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol Cell 2003, 11:695-707.
131. Fan M., Park A., Nephew K.P. CHIP (carboxyl terminus of Hsc70-interacting protein) promotes basal and geldanamycin-induced degradation of estrogen receptor-alpha. Mol Endocrinol 2005, 19:2901-2914.
132. Dai Q., Zhang C., Wu Y., McDonough H., Whaley R.A., Godfrey V., et al. CHIP activates HSF1 and confers protection against apoptosis and cellular stress. EMBO J 2003, 22:5446-5458.
133. Ballinger C.A., Connell P., Wu Y., Hu Z., Thompson L.J., Yin L.Y., et al. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 1999, 19:4535-4545.
134. Tateishi Y., Kawabe Y., Chiba T., Murata S., Ichikawa K., Murayama A., et al. Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor. EMBO J 2004, 23:4813-4823.
135. Nordmeyer J., Eder S., Mahmoodzadeh S., Martus P., Fielitz J., Bass J., et al. Upregulation of myocardial estrogen receptors in human aortic stenosis. Circulation 2004, 110:3270-3275.
136. Hayward C.S., Kalnins W.V., Kelly R.P. Acute effects of 17beta-estradiol on ventricular and vascular hemodynamics in postmenopausal women. Am J Physiol Heart Circ Physiol 2000, 279:H2277-H2284.
137. Patten R.D., Pourati I., Aronovitz M.J., Alsheikh-Ali A., Eder S., Force T., et al. 17 Beta-estradiol differentially affects left ventricular and cardiomyocyte hypertrophy following myocardial infarction and pressure overload. J Card Fail 2008, 14:245-253.
138. van Eickels M., Grohe C., Cleutjens J.P., Janssen B.J., Wellens H.J., Doevendans P.A. 17beta-estradiol attenuates the development of pressure-overload hypertrophy. Circulation 2001, 104:1419-1423.
139. Donaldson C., Eder S., Baker C., Aronovitz M.J., Weiss A.D., Hall-Porter M., et al. Estrogen attenuates left ventricular and cardiomyocyte hypertrophy by an estrogen receptor-dependent pathway that increases calcineurin degradation. Circ Res 2009, 104:265-275. 11p following 75.
140. Fliegner D., Schubert C., Penkalla A., Witt H., Kararigas G., Dworatzek E., et al. Female sex and estrogen receptor-beta attenuate cardiac remodeling and apoptosis in pressure overload. Am J Physiol Regul Integr Comp Physiol 2010, 298:R1597-R1606.
141. Pedram A., Razandi M., Lubahn D., Liu J., Vannan M., Levin E.R. Estrogen inhibits cardiac hypertrophy: role of estrogen receptor-beta to inhibit calcineurin. Endocrinology 2008, 149:3361-3369.
142. Skavdahl M., Steenbergen C., Clark J., Myers P., Demianenko T., Mao L., et al. Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy. Am J Physiol Heart Circ Physiol 2005, 288:H469-H476.
143. Kararigas G., Fliegner D., Gustafsson J.A., Regitz-Zagrosek V. Role of the estrogen/estrogen-receptor-beta axis in the genomic response to pressure overload-induced hypertrophy. Physiol Genomics 2011, 43:438-446.
144. Deschamps A.M., Murphy E., Sun J. Estrogen receptor activation and cardioprotection in ischemia reperfusion injury. Trends Cardiovasc Med 2010, 20:73-78.
145. Baker L., Meldrum K.K., Wang M., Sankula R., Vanam R., Raiesdana A., et al. The role of estrogen in cardiovascular disease. J Surg Res 2003, 115:325-344.
146. Zhai P., Eurell T.E., Cotthaus R.P., Jeffery E.H., Bahr J.M., Gross D.R. Effects of dietary phytoestrogen on global myocardial ischemia-reperfusion injury in isolated female rat hearts. Am J Physiol Heart Circ Physiol 2001, 281:H1223-H1232.
147. Angele M.K., Schwacha M.G., Ayala A., Chaudry I.H. Effect of gender and sex hormones on immune responses following shock. Shock 2000, 14:81-90.
148. Vornehm N.D., Wang M., Abarbanell A., Herrmann J., Weil B., Tan J., et al. Acute postischemic treatment with estrogen receptor-alpha agonist or estrogen receptor-beta agonist improves myocardial recovery. Surgery 2009, 146:145-154.
149. Booth E.A., Obeid N.R., Lucchesi B.R. Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 2005, 289:H2039-H2047.
150. Jeanes H.L., Tabor C., Black D., Ederveen A., Gray G.A. Oestrogen-mediated cardioprotection following ischaemia and reperfusion is mimicked by an oestrogen receptor (ER)alpha agonist and unaffected by an ER beta antagonist. J Endocrinol 2008, 197:493-501.
151. Wang M., Crisostomo P., Wairiuko G.M., Meldrum D.R. Estrogen receptor-alpha mediates acute myocardial protection in females. Am J Physiol Heart Circ Physiol 2006, 290:H2204-H2209.
152. Babiker F.A., Lips D.J., Delvaux E., Zandberg P., Janssen B.J., Prinzen F., et al. Oestrogen modulates cardiac ischaemic remodelling through oestrogen receptor-specific mechanisms. Acta Physiol (Oxf) 2007, 189:23-31.
153. Gabel S.A., Walker V.R., London R.E., Steenbergen C., Korach K.S., Murphy E. Estrogen receptor beta mediates gender differences in ischemia/reperfusion injury. J Mol Cell Cardiol 2005, 38:289-297.
154. Wang M., Crisostomo P.R., Markel T., Wang Y., Lillemoe K.D., Meldrum D.R. Estrogen receptor beta mediates acute myocardial protection following ischemia. Surgery 2008, 144:233-238.
155. Wang M., Wang Y., Weil B., Abarbanell A., Herrmann J., Tan J., et al. Estrogen receptor beta mediates increased activation of PI3K/Akt signaling and improved myocardial function in female hearts following acute ischemia. Am J Physiol Regul Integr Comp Physiol 2009, 296:R972-R978.
156. Liu H., Pedram A., Kim J.K. Oestrogen prevents cardiomyocyte apoptosis by suppressing p38alpha-mediated activation of p53 and by down-regulating p53 inhibition on p38beta. Cardiovasc Res 2011, 89:119-128.