Intracellular protein degradation in mammalian cells: recent developments

Cellular and Molecular Life Sciences - Tập 66 - Trang 2427-2443 - 2009
Erwin Knecht1,2, Carmen Aguado2, Jaime Cárcel1, Inmaculada Esteban2, Juan Miguel Esteve1, Ghita Ghislat1, José Félix Moruno1, José Manuel Vidal1, Rosana Sáez3
1Centro de Investigación Príncipe Felipe, Valencia, Spain
2Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER), ISCIII, Valencia, Spain
3Departamento de Biología Celular, Universidad de Valencia, Burjassot, Spain

Tóm tắt

In higher organisms, dietary proteins are broken down into amino acids within the digestive tract but outside the cells, which incorporate the resulting amino acids into their metabolism. However, under certain conditions, an organism loses more nitrogen than is assimilated in the diet. This additional loss was found in the past century to come from intracellular proteins and started an intensive research that produced an enormous expansion of the field and a dispersed literature. Therefore, our purpose is to provide an updated summary of the current knowledge on the proteolytic machinery involved in intracellular protein degradation and its physiological and pathological relevance, especially addressed to newcomers in the field who may find further details in more specialized reviews. However, even providing a general overview, this is an extremely wide field and, therefore, we mainly focus on mammalian cells, while other cells will be mentioned only for comparison purposes.

Tài liệu tham khảo

Ciechanover A (2005) Intracellular protein degradation: from a vague idea through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting. Cell Death Differ 12:1178–1190 Hershko A (2005) The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ 12:1191–1197 Varshavsky A (2008) Discovery of cellular regulation by protein degradation. J Biol Chem 283:34469–34489 Yewdell JW, Nicchitta CV (2006) The DRiP hypothesis decennial: support, controversy, refinement and extension. Trends Immunol 27:368–373 Grisolía S, Hernández-Yago J, Knecht E (1985) Regulation of mitochondrial protein concentration: a plausible model which may permit assessing protein turnover. Curr Topics Cell Regul 27:387–396 Yen HC, Xu Q, Chou DM, Zhao Z, Elledge SJ (2008) Global protein stability profiling in mammalian cells. Science 322:918–923 Fuertes G, Villarroya A, Knecht E (2003) Role of proteasomes in the degradation of short-lived proteins in human fibroblasts under various growth conditions. Int J Biochem Cell Biol 35:665–675 Vabulas RM, Hartl FU (2005) Protein synthesis upon acute nutrient restriction relies on proteasome function. Science 310:1960–1963 Quesada V, Ordoñez GR, Sánchez LM, Puente XS, López-Otín C (2009) The Degradome database: mammalian proteases and diseases of proteolysis. Nucl Acids Res 37:D239–D243 Esteban I, Aguado C, Sánchez M, Knecht E (2007) Regulation of various proteolytic pathways by insulin and amino acids in human fibroblasts. FEBS Lett 581:3415–3421 DeMartino GN, Gillette TG (2007) Proteasomes: machines for all reasons. Cell 129:659–662 Hanna J, Finley D (2007) A proteasome for all occasions. FEBS Lett 581:2854–2861 Raasi S, Wolf DH (2007) Ubiquitin receptors and ERAD: a network of pathways to the proteasome. Semin Cell Dev Biol 18:780–791 Takeuchi J, Chen H, Coffino P (2007) Proteasome substrate degradation requires association plus extended peptide. EMBO J 26:123–131 Kisselev AF, Callard A, Goldberg AL (2006) Importance of the different proteolytic sites of the proteasome and the efficacy of inhibitors varies with the protein substrate. J Biol Chem 281:8582–8590 Rosenzweig R, Glickman MH (2008) Chaperone-driven proteasome assembly. Biochem Soc Trans 36:807–812 Hutschenreiter S, Tinazli A, Model K, Tampé R (2004) Two-substrate association with the 20S proteasome at single-molecule level. EMBO J 23:2488–2497 Rechsteiner MC, Hill M (2005) Mobilizing the proteolytic machine: cell biological roles of proteasome activators and inhibitors. Trends Cell Biol 15:27–33 da Fonseca PC, Morris EP (2008) Structure of the human 26S proteasome: subunit radial displacements open the gate into the proteolytic core. J Biol Chem 283:23305–23314 Lee D, Ezhkova E, Li B, Pattenden SG, Tansey WP, Workman JL (2005) The proteasome regulatory particle alters the SAGA coactivator to enhance its interactions with transcriptional activators. Cell 123:423–436 Liu CW, Li X, Thompson D, Wooding K, Chang TL, Tang Z, Yu H, Thomas PJ, DeMartino GN (2006) ATP binding and ATP hydrolysis play distinct roles in the function of 26S proteasome. Mol Cell 24:39–50 Husnjak K, Elsasser S, Zhang N, Chen X, Randles L, Shi Y, Hofmann K, Walters KJ, Finley D, Dikic I (2008) Proteasome subunit Rpn13 is a novel ubiquitin receptor. Nature 453:481–488 Koulich E, Li X, DeMartino GN (2008) Relative structural and functional roles of multiple deubiquitinating proteins associated with mammalian 26S proteasome. Mol Biol Cell 19:1072–1082 Hanna J, Hathaway NA, Tone Y, Crosas B, Elsasser S, Kirkpatrick DS, Leggett DS, Gygi SP, King RW, Finley D (2006) Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell 127:99–111 Mao I, Liu J, Li X, Luo H (2008) REGgamma, a proteasome activator and beyond? Cell Mol Life Sci 65:3971–3980 Groettrup M, Pelzer C, Schmidtke G, Hofmann K (2008) Activating the ubiquitin family: UBA6 challenges the field. Trends Biochem Sci 33:230–237 Rodrigo-Brenni MC, Morgan DO (2007) Sequential E2s drive polyubiquitin chain assembly on APC targets. Cell 130:127–139 Ciechanover A (2005) N-terminal ubiquitination. Methods Mol Biol 301:255–270 Robinson PA, Ardley HC (2004) Ubiquitin-protein ligases. J Cell Sci 117:5191–5194 Li W, Ye Y (2008) Polyubiquitin chains: functions, structures, and mechanisms. Cell Mol Life Sci 65:2397–2406 Janse DM, Crosas B, Finley D, Church GM (2004) Localization to the proteasome is sufficient for degradation. J Biol Chem 279:21415–21420 Li W, Tu D, Brunger AT, Ye Y (2007) A ubiquitin ligase transfers preformed polyubiquitin chains from a conjugating enzyme to a substrate. Nature 446:333–337 Hoppe T (2005) Multiubiquitination by E4 enzymes: ‘one size’ doesn’t fit all. Trends Biochem Sci 30:183–187 Seaman MNJ (2008) Endosome protein sorting: motifs and machinery. Cell Mol Life Sci 65:2842–2858 Weake VM, Workman JL (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29:653–663 Millard SM, Wood SA (2006) Riding the DUBway: regulation of protein trafficking by deubiquitylating enzymes. J Cell Biol 173:463–468 Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180 Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10:538–546 Naujokat C, Fuchs D, Berges C (2007) Adaptive modification and flexibility of the proteasome system in response to proteasome inhibition. Biochim Biophys Acta 1773:1389–1397 Croall DE, Ersfeld K (2007) The calpains: modular designs and functional diversity. Genome Biol 28:218 Yi CH, Yuan J (2009) The Jekyll and Hyde functions of caspases. Dev Cell 16:21–34 Tatsuta T, Langer T (2008) Quality control of mitochondria: protection against neurodegeneration and ageing. EMBO J 27:306–314 Klionsky DJ, Cuervo AM, Dunn WA Jr, Levine B, van der Klei I, Seglen PO (2007) How shall I eat thee? Autophagy 3:413–416 Mizushima N (2007) Autophagy: process and function. Genes Dev 21:2861–2873 Sakai Y, Oku M, van der Klei IJ, Kiel JA (2006) Pexophagy: autophagic degradation of peroxisomes. Biochim Biophys Acta 1763:1767–1775 Kraft C, Deplazes A, Sohrmann M, Peter M (2008) Mature ribosomes are selectively degraded upon starvation by an autophagy pathway requiring the Ubp3p/Bre5p ubiquitin protease. Nat Cell Biol 10:602–610 Juhasz G, Neufeld TP (2006) Autophagy: a forty-year search for a missing membrane source. PLoS Biol 4:e36 Axe EL, Walker SA, Manifava M, Chandra P, Roderick HL, Habermann A, Griffiths G, Ktistakis NT (2008) Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J Cell Biol 182:685–701 Yoshimori T, Noda T (2008) Toward unraveling membrane biogenesis in mammalian autophagy. Curr Opin Cell Biol 20:401–407 Klionsky DJ, Cregg JM, Dunn WA Jr, Emr SD, Sakai Y, Sandoval IV, Sibirni A, Subramani S, Thumm M, Veenhuis M, Ohsumi Y (2003) A unified nomenclature for yeast autophagy-related genes. Dev Cell 5:539–545 Kawamata T, Kamada Y, Kabeya Y, Sekito T, Ohsumi Y (2008) Organization of the pre-autophagosomal structure responsible for autophagosome formation. Mol Biol Cell 19:2039–2050 Obara K, Sekito T, Niimi K, Ohsumi Y (2008) The Atg18-Atg2 complex is recruited to autophagic membranes via phosphatidylinositol 3-phosphate and exerts an essential function. J Biol Chem 283:23972–23980 Ohsumi Y, Mizushima N (2004) Two ubiquitin-like conjugation systems essential for autophagy. Semin Cell Dev Biol 15:231–236 Nakatogawa H, Ichimura Y, Ohsumi Y (2007) Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130:165–178 Fujita N, Itoh T, Omori H, Fukuda M, Noda T, Yoshimori T (2008) The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell 19:2092–2100 Wei Y, Pattingre S, Sinha S, Bassik M, Levine B (2008) JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell 30:678–688 Itakura E, Kishi C, Inoue K, Mizushima N (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol Biol Cell 19:5360–5372 Sun Q, Fan W, Chen K, Ding X, Chen S, Zhong Q (2008) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc Natl Acad Sci USA 105:19211–19216 Maria Fimia G, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F (2007) Ambra1 regulates autophagy and development of the nervous system. Nature 447:1121–1125 Krick R, Muehe Y, Prick T, Bremer S, Schlotterhose P, Eskelinen EL, Millen J, Goldfarb DS, Thumm M (2008) Piecemeal microautophagy of the nucleus requires the core macroautophagy genes. Mol Biol Cell 19:4492–4505 Scarlatti F, Maffei R, Beau I, Codogno P, Ghidoni R (2008) Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human cancer cells. Cell Death Differ 15:1318–1329 Meijer AJ, Codogno P (2006) Signalling and autophagy regulation in health, aging and disease. Mol Aspects Med 27:411–425 Nicklin P, Bergman P, Zhang B, Triantafellow E, Wang H, Nyfeler B, Yang H, Hild M, Kung C, Wilson C, Myer VE, MacKeigan JP, Porter JA, Wang YK, Cantley LC, Finan PM, Murphy LO (2009) Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136:521–534 Meléndez A, Neufeld TP (2008) The cell biology of autophagy in metazoans: a developing story. Development 135:2347–2360 Kadowaki M, Razaul Karim M, Carpi A, Miotto G (2006) Nutrient control of macroautophagy in mammalian cells. Mol Aspects Med 27:426–443 Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 282:5641–5652 Abraham RT (2009) Regulation of the mTOR signalling pathway: from laboratory bench to bedside and back again. F1000 Biol Rep 1:8 Meley D, Bauvy C, Houben-Weerts JH, Dubbelhuis PF, Helmond MT, Codogno P, Meijer AJ (2006) AMP-activated protein kinase and the regulation of autophagic proteolysis. J Biol Chem 281:34870–34879 Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jaattela M (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25:193–205 Sadiq F, Hazlerigg DG, Lomax MA (2007) Amino acids and insulin act additively to regulate components of the ubiquitin-proteasome pathway in C2C12 myotubes. BMC Mol Biol 8:23 Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6:472–483 Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069–1075 Sun XM, Butterworth M, MacFarlane M, Dubiel W, Ciechanover A, Cohen GM (2004) Caspase activation inhibits proteasome function during apoptosis. Mol Cell 14:81–93 Levine B, Kroemer G (2009) Autophagy in aging, disease and death: the true identity of a cell death impostor. Cell Death Differ 16:1–2 Bennett EJ, Shaler TA, Woodman B, Ryu KY, Zaitseva TS, Becker CH, Bates GP, Schulman H, Kopito RR (2007) Global changes to the ubiquitin system in Huntington’s disease. Nature 448:704–708 Nedelsky NB, Todd PK, Taylor JP (2008) Autophagy and the ubiquitin-proteasome system: collaborators in neuroprotection. Biochim Biophys Acta 1782:691–699 Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T (2008) The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest 118:2190–2199 Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D, de Pablo R, Tacchetti C, Rubinsztein DC, Ballabio A (2008) A block of autophagy in lysosomal storage disorders. Hum Mol Genet 17:119–129 Perrin AJ, Jiang X, Birmingham CL, So NS, Brumell JH (2004) Recognition of bacteria in the cytosol of mammalian cells by the ubiquitin system. Curr Biol 14:806–811 Levine B (2005) Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120:159–162 Shackelford J, Pagano JS (2007) Role of the ubiquitin system and tumor viruses in AIDS-related cancer. BMC Biochem 8(Suppl 1):S8 Petroski MD (2008) The ubiquitin system, disease, and drug discovery. BMC Biochem 9(Suppl 1):S7 Levine BB, Kroemer G (2008) Autophagy in the pathogenesis of disease. Cell 132:27–42 Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441:880–884 Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441:885–889