Heme regulates protein homeostasis at transcription, protein translation, and degradation levels
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  • 作者:Fang Yang (1)
    En-Duo Wang (1)
  • 关键词:heme ; transcription ; protein translation ; protein degradation
  • 刊名:Frontiers in Biology
  • 出版年:2010
  • 出版时间:December 2010
  • 年:2010
  • 卷:5
  • 期:6
  • 页码:516-523
  • 全文大小:179KB
  • 参考文献:1. Acharya P, Chen J J, Correia M A (2010). Hepatic heme-regulated inhibitor (HRI) eukaryotic initiation factor 2alpha kinase: a protagonist of heme-mediated translational control of CYP2B enzymes and a modulator of basal endoplasmic reticulum stress tone. Mol Pharmacol, 77(4): 575-92 CrossRef
    2. Becerra M, Lombardía-Ferreira L J, Hauser N C, Hoheisel J D, Tizon B, Cerdán M E (2002). The yeast transcriptome in aerobic and hypoxic conditions: effects of hap1, rox1, rox3 and srb10 deletions. Mol Microbiol, 43(3): 545-55 CrossRef
    3. Brower C S, Varshavsky A, Hansen I A (2009). Ablation of arginylation in the mouse N-end rule pathway: loss of fat, higher metabolic rate, damaged spermatogenesis, and neurological perturbations. PLoS ONE, 4(11): e7757 CrossRef
    4. Chen J J (2000). In: Soneberg N, Hershey J W B, Mathews M B, eds. Translational Control of Gene Expression. NY: Cold Spring Harbor Laboratory Press, 529-46
    5. Chen J J (2007). Regulation of protein synthesis by the heme-regulated eIF2α kinase: relevance to anemias. Blood, 109(7): 2693-699
    6. Chen J J, London I M (1995). Regulation of protein synthesis by hemeregulated eIF-2 alpha kinase. Trends Biochem Sci, 20(3): 105-08 CrossRef
    7. Dever T E (2002). Gene-specific regulation by general translation factors. Cell, 108(4): 545-56 CrossRef
    8. Dioum E M, Rutter J, Tuckerman J R, Gonzalez G, Gilles-Gonzalez M A, McKnight S L (2002). NPAS2: a gas-responsive transcription factor. Science, 298(5602): 2385-387 CrossRef
    9. Dohi Y, Ikura T, Hoshikawa Y, Katoh Y, Ota K, Nakanome A, Muto A, Omura S, Ohta T, Ito A, Yoshida M, Noda T, Igarashi K (2008). Bach1 inhibits oxidative stress-induced cellular senescence by impeding p53 function on chromatin. Nat Struct Mol Biol, 15(12): 1246-254 CrossRef
    10. Dunbar A Y, Kamada Y, Jenkins G J, Lowe E R, Billecke S S, Osawa Y (2004). Ubiquitination and degradation of neuronal nitric-oxide synthase in vitro: dimer stabilization protects the enzyme from proteolysis. Mol Pharmacol, 66(4): 964-69 CrossRef
    11. Etlinger J D, Goldberg A L (1980). Control of protein degradation in reticulocytes and reticulocyte extracts by hemin. J Biol Chem, 255(10): 4563-568
    12. Faller M, Matsunaga M, Yin S, Loo J A, Guo F (2007). Heme is involved in microRNA processing. Nat Struct Mol Biol, 14(1): 23-9 CrossRef
    13. Furuyama K, Kaneko K, Vargas P D (2007). Heme as a magnificent molecule with multiple missions: heme determines its own fate and governs cellular homeostasis. Tohoku J Exp Med, 213(1): 1-6 CrossRef
    14. Gattoni M, Boffi A, Sarti P, Chiancone E (1996). Stability of the hemeglobin linkage in alphabeta dimers and isolated chains of human hemoglobin. A study of the heme transfer reaction from the immobilized proteins to albumin. J Biol Chem, 271(17): 10130-0136 CrossRef
    15. Guillaumond F, Dardente H, Giguère V, Cermakian N (2005). Differential control of Bmal1 circadian transcription by REV-ERB and ROR nuclear receptors. J Biol Rhythms, 20(5): 391-03 CrossRef
    16. Haas A L, Rose I A (1981). Hemin inhibits ATP-dependent ubiquitindependent proteolysis: role of hemin in regulating ubiquitin conjugate degradation. Proc Natl Acad Sci USA, 78(11): 6845-848 CrossRef
    17. Hamza I, Chauhan S, Hassett R, O’Brian M R (1998). The bacterial irr protein is required for coordination of heme biosynthesis with iron availability. J Biol Chem, 273(34): 21669-1674 CrossRef
    18. Hentze M W, Muckenthaler M U, Andrews N C (2004). Balancing acts: molecular control of mammalian iron metabolism. Cell, 117(3): 285-97 CrossRef
    19. Hickman M J, Winston F (2007). Heme levels switch the function of Hap1 of Saccharomyces cerevisiae between transcriptional activator and transcriptional repressor. Mol Cell Biol, 27(21): 7414-424 CrossRef
    20. Hoffman A E, Zheng T, Ba Y, Zhu Y (2008). The circadian gene NPAS2, a putative tumor suppressor, is involved in DNA damage response. Mol Cancer Res, 6(9): 1461-468 CrossRef
    21. Hou S, Reynolds M F, Horrigan F T, Heinemann S H, Hoshi T (2006). Reversible binding of heme to proteins in cellular signal transduction. Acc Chem Res, 39(12): 918-24 CrossRef
    22. Hu R G, Wang H, Xia Z, Varshavsky A (2008). The N-end rule pathway is a sensor of heme. Proc Natl Acad Sci USA, 105(1): 76-1 CrossRef
    23. Igarashi J, Murase M, Iizuka A, Pichierri F, Martinkova M, Shimizu T (2008). Elucidation of the heme binding site of heme-regulated eukaryotic initiation factor 2alpha kinase and the role of the regulatory motif in heme sensing by spectroscopic and catalytic studies of mutant proteins. J Biol Chem, 283(27): 18782-8791 CrossRef
    24. Igarashi J, Sato A, Kitagawa T, Yoshimura T, Yamauchi S, Sagami I, Shimizu T (2004). Activation of heme-regulated eukaryotic initiation factor 2alpha kinase by nitric oxide is induced by the formation of a five-coordinate NO-heme complex: optical absorption, electron spin resonance, and resonance raman spectral studies. J Biol Chem, 279(16): 15752-5762 CrossRef
    25. Inuzuka T, Yun B G, Ishikawa H, Takahashi S, Hori H, Matts R L, Ishimori K, Morishima I (2004). Identification of crucial histidines for heme binding in the N-terminal domain of the heme-regulated eIF2alpha kinase. J Biol Chem, 279(8): 6778-782 CrossRef
    26. Ishikawa H, Kato M, Hori H, Ishimori K, Kirisako T, Tokunaga F, Iwai K (2005). Involvement of heme regulatory motif in heme-mediated ubiquitination and degradation of IRP2. Mol Cell, 19(2): 171-81 CrossRef
    27. Kaasik K, Lee C C (2004). Reciprocal regulation of haem biosynthesis and the circadian clock in mammals. Nature, 430(6998): 467-71 CrossRef
    28. Kim Y M, Son K, Hong S J, Green A, Chen J J, Tzeng E, Hierholzer C, Billiar T R (1998). Inhibition of protein synthesis by nitric oxide correlates with cytostatic activity: nitric oxide induces phosphorylation of initiation factor eIF-2 alpha. Mol Med, 4(3): 179-90
    29. Kurosaka S, Leu N A, Zhang F, Bunte R, Saha S, Wang J, Guo C, He W, Kashina A, Bronner-Fraser M (2010). Arginylation-dependent neural crest cell migration is essential for mouse development. PLoS Genet, 6(3): e1000878 CrossRef
    30. Kwon Y T, Kashina A S, Davydov I V, Hu R G, An J Y, Seo JW, Du F, Varshavsky A (2002). An essential role of N-terminal arginylation in cardiovascular development. Science, 297(5578): 96-9 CrossRef
    31. Lamas S, Lowenstein C J, Michel T (2007). Nitric oxide signaling comes of age: 20 years and thriving. Cardiovasc Res, 75(2): 207-09 CrossRef
    32. Lan C, Lee H C, Tang S, Zhang L (2004). A novel mode of chaperone action: heme activation of Hap1 by enhanced association of Hsp90 with the repressed Hsp70-Hap1 complex. J Biol Chem, 279(26): 27607-7612 CrossRef
    33. Lee K S, Raymond L D, Schoen B, Raymond G J, Kett L, Moore R A, Johnson L M, Taubner L, Speare J O, Onwubiko H A, Baron G S, Caughey WS, Caughey B (2007). Hemin interactions and alterations of the subcellular localization of prion protein. J Biol Chem, 282(50): 36525-6533 CrossRef
    34. Leu N A, Kurosaka S, Kashina A, Bergmann A (2009). Conditional Tek promoter-driven deletion of arginyltransferase in the germ line causes defects in gametogenesis and early embryonic lethality in mice. PLoS ONE, 4(11): e7734 CrossRef
    35. Levicán G, Katz A, de Armas M, Nú?ez H, Orellana O (2007). Regulation of a glutamyl-tRNA synthetase by the heme status. Proc Natl Acad Sci USA, 104(9): 3135-140 CrossRef
    36. Liao M, Pabarcus MK, Wang Y, Hefner C, Maltby D A, Medzihradszky K F, Salas-Castillo S P, Yan J, Maher J J, Correia M A (2007). Impaired dexamethasone-mediated induction of tryptophan 2,3-dioxygenase in heme-deficient rat hepatocytes: translational control by a hepatic eIF2alpha kinase, the heme-regulated inhibitor. J Pharmacol Exp Ther, 323(3): 979-89 CrossRef
    37. Lim E J, Joung Y H, Jung SM, Park S H, Park J H, Kim S Y, Hwang T S, Hong D Y, Chung S C, Ye S K, Moon E S, Park E U, Park T, Chung I M, Yang Y M (2010). Hemin inhibits cyclin D1 and IGF-1 expression via STAT5b under hypoxia in ERalpha-negative MDAMB 231 breast cancer cells. Int J Oncol, 36(5): 1243-251
    38. Mense S M, Zhang L (2006). Heme: a versatile signaling molecule controlling the activities of diverse regulators ranging from transcription factors to MAP kinases. Cell Res, 16(8): 681-92 CrossRef
    39. Meyron-Holtz E G, Ghosh M C, Rouault T A (2004). Mammalian tissue oxygen levels modulate iron-regulatory protein activities in vivo. Science, 306(5704): 2087-090 CrossRef
    40. Monson E K, Weinstein M, Ditta G S, Helinski D R (1992). The FixL protein of Rhizobium meliloti can be separated into a heme-binding oxygen-sensing domain and a functional C-terminal kinase domain. Proc Natl Acad Sci USA, 89(10): 4280-284 CrossRef
    41. Ogawa K, Sun J, Taketani S, Nakajima O, Nishitani C, Sassa S, Hayashi N, Yamamoto M, Shibahara S, Fujita H, Igarashi K (2001). Heme mediates derepression of Maf recognition element through direct binding to transcription repressor Bach1. EMBO J, 20(11): 2835-843 CrossRef
    42. Oglesby-Sherrouse A G, Vasil M L, Rénia L (2010). Characterization of a heme-regulated non-coding RNA encoded by the prrF locus of Pseudomonas aeruginosa. PLoS ONE, 5(4): e9930 CrossRef
    43. Qi Z, Hamza I, O’Brian M R (1999). Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci USA, 96(23): 13056-3061 CrossRef
    44. Rafie-Kolpin M, Chefalo P J, Hussain Z, Hahn J, Uma S, Matts R L, Chen J J (2000). Two heme-binding domains of heme-regulated eukaryotic initiation factor-2alpha kinase. N terminus and kinase insertion. J Biol Chem, 275(7): 5171-178
    45. Raghuram S, Stayrook K R, Huang P, Rogers P M, Nosie A K, McClure D B, Burris L L, Khorasanizadeh S, Burris T P, Rastinejad F (2007). Identification of heme as the ligand for the orphan nuclear receptors REV-ERBalpha and REV-ERBbeta. Nat Struct Mol Biol, 14(12): 1207-213 CrossRef
    46. Reichard J F, Sartor M A, Puga A (2008). BACH1 is a specific repressor of HMOX1 that is inactivated by arsenite. J Biol Chem, 283(33): 22363-2370 CrossRef
    47. Ripperger J A (2006). Mapping of binding regions for the circadian regulators BMAL1 and CLOCK within the mouse Rev-erbalpha gene. Chronobiol Int, 23(1-): 135-42 CrossRef
    48. Salahudeen A A, Thompson J W, Ruiz J C, Ma H W, Kinch L N, Li Q, Grishin N V, Bruick R K (2009). An E3 ligase possessing an ironresponsive hemerythrin domain is a regulator of iron homeostasis. Science, 326(5953): 722-26 CrossRef
    49. Severance S, Hamza I (2009). Trafficking of heme and porphyrins in metazoa. Chem Rev, 109(10): 4596-616 CrossRef
    50. Severance S, Rajagopal A, Rao A U, Cerqueira G C, Mitreva M, El-Sayed N M, Krause M, Hamza I, Chisholm A D (2010). Genomewide analysis reveals novel genes essential for heme homeostasis in Caenorhabditis elegans. PLoS Genet, 6(7): e1001044 CrossRef
    51. Sun J, Hoshino H, Takaku K, Nakajima O, Muto A, Suzuki H, Tashiro S, Takahashi S, Shibahara S, Alam J, Taketo M M, Yamamoto M, Igarashi K (2002). Hemoprotein Bach1 regulates enhancer availability of heme oxygenase-1 gene. EMBO J, 21(19): 5216-224 CrossRef
    52. Suzuki H, Tashiro S, Hira S, Sun J, Yamazaki C, Zenke Y, Ikeda-Saito M, Yoshida M, Igarashi K (2004). Heme regulates gene expression by triggering Crm1-dependent nuclear export of Bach1. EMBO J, 23(13): 2544-553 CrossRef
    53. Tsai A (1994). How does NO activate hemeproteins? FEBS Lett, 341(2-): 141-45 CrossRef
    54. Uma S, Yun B G, Matts R L (2001). The heme-regulated eukaryotic initiation factor 2alpha kinase. A potential regulatory target for control of protein synthesis by diffusible gases. J Biol Chem, 276(18): 14875-4883
    55. Varshavsky A (1996). The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci USA, 93(22): 12142-2149 CrossRef
    56. Vierstra R D, Sullivan M L (1988). Hemin inhibits ubiquitin-dependent proteolysis in both a higher plant and yeast. Biochemistry, 27(9): 3290-295 CrossRef
    57. Wakasugi K (2007). Human tryptophanyl-tRNA synthetase binds with heme to enhance its aminoacylation activity. Biochemistry, 46(40): 11291-1298 CrossRef
    58. Wehner K A, Schütz S, Sarnow P (2010). OGFOD1, a novel modulator of eukaryotic translation initiation factor 2alpha phosphorylation and the cellular response to stress. Mol Cell Biol, 30(8): 2006-016 CrossRef
    59. Wu N, Yin L, Hanniman E A, Joshi S, Lazar M A (2009). Negative feedback maintenance of heme homeostasis by its receptor, Reverbalpha. Genes Dev, 23(18): 2201-209 CrossRef
    60. Yang F, Xia X, Lei H Y, Wang E D (2010). Hemin binds to human cytoplasmic arginyl-tRNA synthetase and inhibits its catalytic activity. J Biol Chem, doi: 10.1074/jbc.M110.159913 (in press)
    61. Yang J, Ishimori K, O’Brian M R (2005). Two heme binding sites are involved in the regulated degradation of the bacterial iron response regulator (Irr) protein. J Biol Chem, 280(9): 7671-676 CrossRef
    62. Yang J, Kim K D, Lucas A, Drahos K E, Santos C S, Mury S P, Capelluto D G, Finkielstein C V (2008). A novel heme-regulatory motif mediates heme-dependent degradation of the circadian factor period 2. Mol Cell Biol, 28(15): 4697-711 CrossRef
    63. Yang J, Panek H R, O’Brian M R (2006). Oxidative stress promotes degradation of the Irr protein to regulate haem biosynthesis in Bradyrhizobium japonicum. Mol Microbiol, 60(1): 209-18 CrossRef
    64. Yin L, Wu N, Curtin J C, Qatanani M, Szwergold N R, Reid R A, Waitt G M, Parks D J, Pearce K H, Wisely G B, Lazar M A (2007). Reverbalpha, a heme sensor that coordinates metabolic and circadian pathways. Science, 318(5857): 1786-789 CrossRef
    65. Yin L, Wu N, Lazar MA (2010). Nuclear receptor Rev-erbalpha: a heme receptor that coordinates circadian rhythm and metabolism. Nucl Recept Signal, 8: e001 CrossRef
    66. Zenke-Kawasaki Y, Dohi Y, Katoh Y, Ikura T, Ikura M, Asahara T, Tokunaga F, Iwai K, Igarashi K (2007). Heme induces ubiquitination and degradation of the transcription factor Bach1. Mol Cell Biol, 27(19): 6962-971 CrossRef
    67. Zhang L, Guarente L (1995). Heme binds to a short sequence that serves a regulatory function in diverse proteins. EMBO J, 14(2): 313-20
    68. Zhang L, Hach A (1999). Molecular mechanism of heme signaling in yeast: the transcriptional activator Hap1 serves as the key mediator. Cell Mol Life Sci, 56(5-): 415-26 CrossRef
  • 作者单位:Fang Yang (1)
    En-Duo Wang (1)

    1. State Key Laboratory of Molecular Biology, Institute of Biochemistry and Cell Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, 200031, China
  • ISSN:1674-7992
文摘
Heme, as a prosthetic group of proteins, is an iron-protoporphyrin involved in a wide range of cellular functions. Cellular heme levels vary due to the accurate balance of its synthesis and degradation. The “heme sensor protein-is currently a focus of investigation because heme has been found as a cellular signaling messenger involved in various biologic processes, including gene expression, protein localization, protein stability and microRNA processing. Several eukaryotic transcriptional factors can be regulated by heme, including heme activator protein (Hap1), Bach1, REV-erbα, and neuronal PAS domain protein 2 (NPAS2). Especially, the two circadian transcriptional factors serving as the heme sensor, REV-erbα and NPAS2, coordinate the circadian clock with metabolic pathways. It is well established that heme regulates the activity of heme-regulated eukaryotic initiation factor 2α (eIF2α) kinase (HRI), which serves as a feedback inhibitor of protein translation in both erythroid and non-erythroid cells. Additionally, heme is involved in protein degradation by inducing the degradation of several proteins such as the iron response regulator (Irr), iron regulatory protein 2 (IRP2), Bach1, and circadian factor period 2 (Per2). The N-end rule ubiquitin-dependent protein degradation pathway has also been identified as a sensor of heme, which blocks the function of arginyl-tRNA protein transferase (ATE1) and E3 ubiquitin ligase. In this review, we summarize the regulatory roles of heme at the levels of transcription, protein translation, and protein degradation, highlighting the role of heme in maintaining cellular homeostasis.

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