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Annual Review of Biomedical Data Science

Volume 5, 2022

Cotranslational Mechanisms of Protein Biogenesis and Complex Assembly in Eukaryotes

Abstract

The formation of protein complexes is crucial to most biological functions. The cellular mechanisms governing protein complex biogenesis are not yet well understood, but some principles of cotranslational and posttranslational assembly are beginning to emerge. In bacteria, this process is favored by operons encoding subunits of protein complexes. Eukaryotic cells do not have polycistronic mRNAs, raising the question of how they orchestrate the encounter of unassembled subunits. Here we review the constraints and mechanisms governing eukaryotic co- and posttranslational protein folding and assembly, including the influence of elongation rate on nascent chain targeting, folding, and chaperone interactions. Recent evidence shows that mRNAs encoding subunits of oligomeric assemblies can undergo localized translation and form cytoplasmic condensates that might facilitate the assembly of protein complexes. Understanding the interplay between localized mRNA translation and cotranslational proteostasis will be critical to defining protein complex assembly in vivo.

Keyword(s): chaperones, cotranslational protein folding, Hsp70, nascent polypeptide, organelle targeting, protein complex assembly, RNA granules, translation elongation, TRiC/CCT
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2022-08-10
2024-05-28
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Literature Cited

  1. 1.
    Anfinsen CB. 1973. Principles that govern the folding of protein chains. Science 181:4096223–30
     [Google Scholar]
  2. 2.
    Netzer WJ, Hartl FU. 1997. Recombination of protein domains facilitated by co-translational folding in eukaryotes. Nature 388:6640343–49
     [Google Scholar]
  3. 3.
    Klaips CL, Jayaraj GG, Hartl FU. 2018. Pathways of cellular proteostasis in aging and disease. J. Cell Biol. 217:151–63
     [Google Scholar]
  4. 4.
    Sontag EM, Samant RS, Frydman J. 2017. Mechanisms and functions of spatial protein quality control. Annu. Rev. Biochem. 86:97–122
     [Google Scholar]
  5. 5.
    Balchin D, Hayer-Hartl M, Hartl FU. 2016. In vivo aspects of protein folding and quality control. Science 353:6294aac4354
     [Google Scholar]
  6. 6.
    Chiti F, Dobson CM. 2017. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu. Rev. Biochem. 86:27–68
     [Google Scholar]
  7. 7.
    Duncan CDS, Mata J. 2011. Widespread cotranslational formation of protein complexes. PLOS Genet. 7:12e1002398Shows for the first time that co-posttranslational assembly is widespread in eukaryotes.
     [Google Scholar]
  8. 8.
    Shiber A, Döring K, Friedrich U, Klann K, Merker D et al. 2018. Cotranslational assembly of protein complexes in eukaryotes revealed by ribosome profiling. Nature 561:7722268–72Uses C-terminally GFP-tagged subunits of preselected protein complexes to investigate co-posttranslational assembly in yeast using SeRP.
     [Google Scholar]
  9. 9.
    Cassaignau AME, Cabrita LD, Christodoulou J. 2020. How does the ribosome fold the proteome?. Annu. Rev. Biochem. 89:389–415
     [Google Scholar]
  10. 10.
    Kramer G, Shiber A, Bukau B. 2019. Mechanisms of cotranslational maturation of newly synthesized proteins. Annu. Rev. Biochem. 88:337–64
     [Google Scholar]
  11. 11.
    Aksnes H, Ree R, Arnesen T 2019. Co-translational, post-translational, and non-catalytic roles of N-terminal acetyltransferases. Mol. Cell 73:61097–114
     [Google Scholar]
  12. 12.
    Knorr AG, Schmidt C, Tesina P, Berninghausen O, Becker T et al. 2019. Ribosome–NatA architecture reveals that rRNA expansion segments coordinate N-terminal acetylation. Nat. Struct. Mol. Biol. 26:35–39
     [Google Scholar]
  13. 13.
    Yang C-I, Hsieh H-H, Shan S 2019. Timing and specificity of cotranslational nascent protein modification in bacteria. PNAS 116:4623050–60
     [Google Scholar]
  14. 14.
    Shemorry A, Hwang C-S, Varshavsky A. 2013. Control of protein quality and stoichiometries by N-terminal acetylation and the N-end rule pathway. Mol. Cell 50:4540–51
     [Google Scholar]
  15. 15.
    Friedrich UA, Zedan M, Hessling B, Fenzl K, Gillet L et al. 2021. Nα-terminal acetylation of proteins by NatA and NatB serves distinct physiological roles in Saccharomyces cerevisiae. Cell Rep. 34:5108711
     [Google Scholar]
  16. 16.
    Hartl FU, Bracher A, Hayer-Hartl M. 2011. Molecular chaperones in protein folding and proteostasis. Nature 475:7356324–32
     [Google Scholar]
  17. 17.
    Deuerling E, Gamerdinger M, Kreft SG. 2019. Chaperone interactions at the ribosome. Cold Spring Harb. Perspect. Biol. 11:11a033977
     [Google Scholar]
  18. 18.
    Bertolini M, Fenzl K, Kats I, Wruck F, Tippmann F et al. 2021. Interactions between nascent proteins translated by adjacent ribosomes drive homomer assembly. Science 371:652457–64Uses a new technique DiSP to show that some adjacent nascent proteins dimerize co-cotranslationally to favor homomer assembly.
     [Google Scholar]
  19. 19.
    Raue U, Oellerer S, Rospert S. 2007. Association of protein biogenesis factors at the yeast ribosomal tunnel exit is affected by the translational status and nascent polypeptide sequence. J. Biol. Chem. 282:117809–16
     [Google Scholar]
  20. 20.
    Gamerdinger M, Kobayashi K, Wallisch A, Kreft SG, Sailer C et al. 2019. Early scanning of nascent polypeptides inside the ribosomal tunnel by NAC. Mol. Cell 75:5996–1006.e8Describes an unexpected feature where NAC protrudes into the ribosome exit tunnel, implying early interaction between NAC and the nascent chain.
     [Google Scholar]
  21. 21.
    del Alamo M, Hogan DJ, Pechmann S, Albanese V, Brown PO, Frydman J. 2011. Defining the specificity of cotranslationally acting chaperones by systematic analysis of mRNAs associated with ribosome-nascent chain complexes. PLOS Biol. 9:7e1001100
     [Google Scholar]
  22. 22.
    Gamerdinger M, Hanebuth MA, Frickey T, Deuerling E. 2015. The principle of antagonism ensures protein targeting specificity at the endoplasmic reticulum. Science 348:6231201–7
     [Google Scholar]
  23. 23.
    Hsieh H-H, Lee JH, Chandrasekar S, Shan S. 2020. A ribosome-associated chaperone enables substrate triage in a cotranslational protein targeting complex. Nat. Commun. 11:5840
     [Google Scholar]
  24. 24.
    Singhal N, Sharma A, Kumari S, Garg A, Rai R et al. 2020. Biophysical and biochemical characterization of nascent polypeptide-associated complex of Picrophilus torridus and elucidation of its interacting partners. Front. Microbiol. 11:915
     [Google Scholar]
  25. 25.
    Koplin A, Preissler S, Llina Y, Koch M, Scior A et al. 2010. A dual function for chaperones SSB-RAC and the NAC nascent polypeptide-associated complex on ribosomes. J. Cell Biol. 189:157–68
     [Google Scholar]
  26. 26.
    Willmund F, Del Alamo M, Pechmann S, Chen T, Albanèse V et al. 2013. The cotranslational function of ribosome-associated Hsp70 in eukaryotic protein homeostasis. Cell 152:1–2196–209
     [Google Scholar]
  27. 27.
    Döring K, Ahmed N, Riemer T, Suresh HG, Vainshtein Y et al. 2017. Profiling Ssb-nascent chain interactions reveals principles of Hsp70-assisted folding. Cell 170:2298–311.e20
     [Google Scholar]
  28. 28.
    Zhang Y, Valentín Gesé G, Conz C, Lapouge K, Kopp J et al. 2020. The ribosome-associated complex RAC serves in a relay that directs nascent chains to Ssb. Nat. Commun. 11:1504
     [Google Scholar]
  29. 29.
    Galmozzi CV, Merker D, Friedrich UA, Döring K, Kramer G. 2019. Selective ribosome profiling to study interactions of translating ribosomes in yeast. Nat. Protoc. 14:2279–317
     [Google Scholar]
  30. 30.
    Stein KC, Kriel A, Frydman J. 2019. Nascent polypeptide domain topology and elongation rate direct the cotranslational hierarchy of Hsp70 and TRiC/CCT. Mol. Cell 75:61117–30Shows through SeRP how Hsp70 and TRiC/CCT cooperatively fold nascent proteins on the ribosome.
     [Google Scholar]
  31. 31.
    Lee K, Ziegelhoffer T, Delewski W, Berger SE, Sabat G, Craig EA. 2021. Pathway of Hsp70 interactions at the ribosome. Nat. Commun. 12:5666Identifies two modes of interactions between ribosome and Hsp70 that couples ATPase cycle of Hsp70 with ribosome interactions.
     [Google Scholar]
  32. 32.
    Yam AY-W, Albanèse V, Lin H-TJ, Frydman J. 2005. Hsp110 cooperates with different cytosolic HSP70 systems in a pathway for de novo folding. J. Biol. Chem. 280:5041252–61
     [Google Scholar]
  33. 33.
    Albanèse V, Yam AYW, Baughman J, Parnot C, Frydman J. 2006. Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells. Cell 124:75–88
     [Google Scholar]
  34. 34.
    Hansen WJ, Cowan NJ, Welch WJ. 1999. Prefoldin-nascent chain complexes in the folding of cytoskeletal proteins. J. Cell Biol. 145:2265–77
     [Google Scholar]
  35. 35.
    Sahlan M, Zako T, Yohda M. 2018. Prefoldin, a jellyfish-like molecular chaperone: functional cooperation with a group II chaperonin and beyond. Biophys. Rev. 10:2339–45
     [Google Scholar]
  36. 36.
    Hartl FU, Hayer-Hartl M. 2002. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295:55611852–58
     [Google Scholar]
  37. 37.
    Gestaut D, Roh SH, Ma B, Pintilie G, Joachimiak LA et al. 2019. The chaperonin TRiC/CCT associates with prefoldin through a conserved electrostatic interface essential for cellular proteostasis. Cell 177:3751–65.e15
     [Google Scholar]
  38. 38.
    Yam AY, Xia Y, Lin H-TJ, Burlingame A, Gerstein M, Frydman J. 2008. Defining the TRiC/CCT interactome links chaperonin function to stabilization of newly made proteins with complex topologies. Nat. Struct. Mol. Biol. 15:121255–62
     [Google Scholar]
  39. 39.
    Hegde RS, Keenan RJ. 2021. The mechanisms of integral membrane protein biogenesis. Nat. Rev. Mol. Cell Biol. 23:107–24
     [Google Scholar]
  40. 40.
    Zhang X, Shan S. 2014. Fidelity of cotranslational protein targeting by the signal recognition particle. Annu. Rev. Biophys. 43:381–408
     [Google Scholar]
  41. 41.
    Aviram N, Ast T, Costa EA, Arakel EC, Chuartzman SG et al. 2016. The SND proteins constitute an alternative targeting route to the endoplasmic reticulum. Nature 540:7631134–38
     [Google Scholar]
  42. 42.
    Shan S. 2019. Guiding tail-anchored membrane proteins to the endoplasmic reticulum in a chaperone cascade. J. Biol. Chem. 294:4516577–86
     [Google Scholar]
  43. 43.
    Akopian D, Shen K, Zhang X, Shan S. 2013. Signal recognition particle: an essential protein-targeting machine. Annu. Rev. Biochem. 82:693–721
     [Google Scholar]
  44. 44.
    Chartron JW, Hunt KCL, Frydman J. 2016. Cotranslational signal-independent SRP preloading during membrane targeting. Nature 536:7615224–28
     [Google Scholar]
  45. 45.
    Lee JH, Chandrasekar S, Chung S, Hwang Fu Y-H, Liu D et al. 2018. Sequential activation of human signal recognition particle by the ribosome and signal sequence drives efficient protein targeting. PNAS 115:24E5487–96
     [Google Scholar]
  46. 46.
    Lee JH, Jomaa A, Chung S, Hwang Fu Y-H, Qian R et al. 2021. Receptor compaction and GTPase rearrangement drive SRP-mediated cotranslational protein translocation into the ER. Sci. Adv. 7:21eabg0942
     [Google Scholar]
  47. 47.
    Murayama E, Sarris M, Redd M, Le Guyader D, Vivier C et al. 2015. NACA deficiency reveals the crucial role of somite-derived stromal cells in haematopoietic niche formation. Nat. Commun. 6:8375
     [Google Scholar]
  48. 48.
    Jomaa A, Gamerdinger M, Hsieh H-H, Wallisch A, Chandrasekaran V et al. 2022. Mechanism of signal sequence handover from NAC to SRP on ribosomes during ER-protein targeting. Science 375:6583839–44Describes the first high-resolution structure of ribosome-bound NAC and shows substrate relay model from NAC to SRP.
     [Google Scholar]
  49. 49.
    Ariosa A, Lee JH, Wang S, Saraogi I, Shan S. 2015. Regulation by a chaperone improves substrate selectivity during cotranslational protein targeting. PNAS 112:25E3169–78
     [Google Scholar]
  50. 50.
    Zhang Y, De Laurentiis E, Bohnsack KE, Wahlig M, Ranjan N et al. 2021. Ribosome-bound Get4/5 facilitates the capture of tail-anchored proteins by Sgt2 in yeast. Nat. Commun. 12:782
     [Google Scholar]
  51. 51.
    Leznicki P, High S. 2020. SGTA associates with nascent membrane protein precursors. EMBO Rep. 21:5e48835
     [Google Scholar]
  52. 52.
    Couvillion MT, Soto IC, Shipkovenska G, Churchman LS. 2016. Synchronized mitochondrial and cytosolic translation programs. Nature 533:7604499–503
     [Google Scholar]
  53. 53.
    Kellems RE, Butow RA. 1972. Cytoplasmic-type 80 S ribosomes associated with yeast mitochondria. I. Evidence for ribosome binding sites on yeast mitochondria. J. Biol. Chem. 247:248043–50
     [Google Scholar]
  54. 54.
    Marc P, Margeot A, Devaux F, Blugeon C, Corral-Debrinski M, Jacq C. 2002. Genome-wide analysis of mRNAs targeted to yeast mitochondria. EMBO Rep. 3:2159–64
     [Google Scholar]
  55. 55.
    Saint-Georges Y, Garcia M, Delaveau T, Jourdren L, Le Crom S et al. 2008. Yeast mitochondrial biogenesis: a role for the PUF RNA-binding protein Puf3p in mRNA localization. PLOS ONE 3:6e2293
     [Google Scholar]
  56. 56.
    Fazal FM, Han S, Parker KR, Kaewsapsak P, Xu J et al. 2019. Atlas of subcellular RNA localization revealed by APEX-Seq. Cell 178:2473–90
     [Google Scholar]
  57. 57.
    Williams CC, Jan CH, Weissman JS. 2014. Targeting and plasticity of mitochondrial proteins revealed by proximity-specific ribosome profiling. Science 346:6210748–51
     [Google Scholar]
  58. 58.
    Tsuboi T, Viana MP, Xu F, Yu J, Chanchani R et al. 2020. Mitochondrial volume fraction and translation duration impact mitochondrial mRNA localization and protein synthesis. eLife 9:e57814
     [Google Scholar]
  59. 59.
    Eliyahu E, Pnueli L, Melamed D, Scherrer T, Gerber AP et al. 2010. Tom20 mediates localization of mRNAs to mitochondria in a translation-dependent manner. Mol. Cell. Biol. 30:1284–94
     [Google Scholar]
  60. 60.
    Wiedmann B, Sakai H, Davis TA, Wiedmann M. 1994. A protein complex required for signal-sequence-specific sorting and translocation. Nature 370:6489434–40
     [Google Scholar]
  61. 61.
    Lesnik C, Cohen Y, Atir-Lande A, Schuldiner M, Arava Y. 2014. OM14 is a mitochondrial receptor for cytosolic ribosomes that supports co-translational import into mitochondria. Nat. Commun. 5:5711
     [Google Scholar]
  62. 62.
    Young JC, Hoogenraad NJ, Hartl FU. 2003. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112:141–50
     [Google Scholar]
  63. 63.
    Cabrita LD, Dobson CM, Christodoulou J. 2010. Protein folding on the ribosome. Curr. Opin. Struct. Biol. 20:133–45
     [Google Scholar]
  64. 64.
    Lu J, Deutsch C. 2005. Folding zones inside the ribosomal exit tunnel. Nat. Struct. Mol. Biol. 12:121123–29
     [Google Scholar]
  65. 65.
    Kaiser CM, Liu K. 2018. Folding up and moving on-nascent protein folding on the ribosome. J. Mol. Biol. 430:224580–91
     [Google Scholar]
  66. 66.
    Chaney JL, Clark PL. 2015. Roles for synonymous codon usage in protein biogenesis. Annu. Rev. Biophys. 44:143–66
     [Google Scholar]
  67. 67.
    Letzring DP, Dean KM, Grayhack EJ. 2010. Control of translation efficiency in yeast by codon-anticodon interactions. RNA 16:122516–28
     [Google Scholar]
  68. 68.
    Hanson G, Coller J. 2018. Codon optimality, bias and usage in translation and mRNA decay. Nat. Rev. Mol. Cell Biol. 19:20–30
     [Google Scholar]
  69. 69.
    Tsai CJ, Sauna ZE, Kimchi-Sarfaty C, Ambudkar SV, Gottesman MM, Nussinov R. 2008. Synonymous mutations and ribosome stalling can lead to altered folding pathways and distinct minima. J. Mol. Biol. 383:2281–91
     [Google Scholar]
  70. 70.
    Brule CE, Grayhack EJ. 2017. Synonymous codons: choose wisely for expression. Trends Genet. 33:4283–97
     [Google Scholar]
  71. 71.
    Seidelt B, Innis CA, Wilson DN, Gartmann M, Armache J-P et al. 2009. Structural insight into nascent polypeptide chain-mediated translational stalling. Science 326:59581412–15
     [Google Scholar]
  72. 72.
    Huter P, Arenz S, Bock LV, Graf M, Frister JO et al. 2017. Structural basis for polyproline-mediated ribosome stalling and rescue by the translation elongation factor EF-P. Mol. Cell 68:3515–27.e6
     [Google Scholar]
  73. 73.
    Gutierrez E, Shin BS, Woolstenhulme CJ, Kim JR, Saini P et al. 2013. eif5A promotes translation of polyproline motifs. Mol. Cell 51:135–45
     [Google Scholar]
  74. 74.
    Doerfel LK, Wohlgemuth I, Kothe C, Peske F, Urlaub H, Rodnina MV. 2013. EF-P is essential for rapid synthesis of proteins containing consecutive proline residues. Science 339:611585–88
     [Google Scholar]
  75. 75.
    Schuller AP, Wu CCC, Dever TE, Buskirk AR, Green R. 2017. eIF5A functions globally in translation elongation and termination. Mol. Cell 66:2194–205.e5
     [Google Scholar]
  76. 76.
    Pechmann S, Frydman J. 2013. Evolutionary conservation of codon optimality reveals hidden signatures of cotranslational folding. Nat. Struct. Mol. Biol. 20:2237–43
     [Google Scholar]
  77. 77.
    Pechmann S, Chartron JW, Frydman J. 2014. Local slowdown of translation by nonoptimal codons promotes nascent-chain recognition by SRP in vivo. Nat. Struct. Mol. Biol. 21:121100–105
     [Google Scholar]
  78. 78.
    Lyu X, Yang Q, Li L, Dang Y, Zhou Z et al. 2020. Adaptation of codon usage to tRNA I34 modification controls translation kinetics and proteome landscape. PLOS Genet. 16:6e1008836
     [Google Scholar]
  79. 79.
    Rapino F, Zhou Z, Roncero Sanchez AM, Joiret M, Seca C et al. 2021. Wobble tRNA modification and hydrophilic amino acid patterns dictate protein fate. Nat. Commun. 12:2170
     [Google Scholar]
  80. 80.
    Geller R, Pechmann S, Acevedo A, Andino R, Frydman J. 2018. Hsp90 shapes protein and RNA evolution to balance trade-offs between protein stability and aggregation. Nat. Commun. 9:1781
     [Google Scholar]
  81. 81.
    Pechmann S, Willmund F, Frydman J. 2013. The ribosome as a hub for protein quality control. Mol. Cell 49:3411–21
     [Google Scholar]
  82. 82.
    Joazeiro CAP. 2017. Ribosomal stalling during translation: providing substrates for ribosome-associated protein quality control. Annu. Rev. Cell Dev. Biol. 33:343–68
     [Google Scholar]
  83. 83.
    Simms CL, Yan LL, Zaher HS. 2017. Ribosome collision is critical for quality control during no-go decay. Mol. Cell 68:2361–73.e5
     [Google Scholar]
  84. 84.
    Brandman O, Hegde RS. 2016. Ribosome-associated protein quality control. Nat. Struct. Mol. Biol. 23:7–15
     [Google Scholar]
  85. 85.
    Yonashiro R, Tahara EB, Bengtson MH, Khokhrina M, Lorenz H et al. 2016. The Rqc2/Tae2 subunit of the ribosome-associated quality control(RQC) complex marks ribosome-stalled nascent polypeptide chains for aggregation. eLife 5:e11794
     [Google Scholar]
  86. 86.
    Izawa T, Park SH, Zhao L, Hartl FU, Neupert W. 2017. Cytosolic protein Vms1 links ribosome quality control to mitochondrial and cellular homeostasis. Cell 171:4890–903.e18
     [Google Scholar]
  87. 87.
    Stein KC, Morales-Polanco F, van der Lienden J, Rainbolt TK, Frydman J. 2022. Ageing exacerbates ribosome pausing to disrupt cotranslational proteostasis. Nature 601:637–42
     [Google Scholar]
  88. 88.
    Zhao T, Chen Y-M, Li Y, Wang J, Chen S et al. 2021. Disome-seq reveals widespread ribosome collisions that promote cotranslational protein folding. Genome Biol. 22:16
     [Google Scholar]
  89. 89.
    Arpat AB, Liechti A, De Matos M, Dreos R, Janich P, Gatfield D. 2020. Transcriptome-wide sites of collided ribosomes reveal principles of translational pausing. Genome Res. 30:7985–99
     [Google Scholar]
  90. 90.
    Han P, Shichino Y, Schneider-Poetsch T, Mito M, Hashimoto S et al. 2020. Genome-wide survey of ribosome collision. Cell Rep. 31:5107610
     [Google Scholar]
  91. 91.
    Meydan S, Guydosh NR. 2020. Disome and trisome profiling reveal genome-wide targets of ribosome quality control. Mol. Cell 79:4588–602Profiles disomes and trisomes to show widespread ribosome collisions on endogenous mRNAs in normal conditions, which may play functional roles in cotranslational protein folding without inducing RQC.
     [Google Scholar]
  92. 92.
    Taggart JC, Li G-W. 2018. Production of protein-complex components is stoichiometric and lacks general feedback regulation in eukaryotes. Cell Syst. 7:6580–89
     [Google Scholar]
  93. 93.
    Marsh JA, Hernández H, Hall Z, Ahnert SE, Perica T et al. 2013. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell 153:2461–70
     [Google Scholar]
  94. 94.
    Hemmingsen SM, Woolford C, van der Vies SM, Tilly K, Dennis DT et al. 1988. Homologous plant and bacterial proteins chaperone oligomeric protein assembly. Nature 333:6171330–34
     [Google Scholar]
  95. 95.
    Minton AP. 2000. Implications of macromolecular crowding for protein assembly. Curr. Opin. Struct. Biol. 10:134–39
     [Google Scholar]
  96. 96.
    Schwarz A, Beck M. 2019. The benefits of cotranslational assembly: a structural perspective. Trends Cell Biol. 29:10791–803
     [Google Scholar]
  97. 97.
    Kihara HK, Hu ASL, Halvorson HO. 1961. The identification of a ribosomal-bound β-glucosidase. PNAS 47:4489
     [Google Scholar]
  98. 98.
    Duerksen JD, O'Connor ML 1963. The demonstration of ribosome-bound penicillinase in Bacillus cereus. Biochem. Biophys. Res. Commun. 10:134–39
     [Google Scholar]
  99. 99.
    Zipser D. 1963. Studies on the ribosome-bound β-galactosidase of Escherichia coli. J. Mol. Biol. 7:6739–51
     [Google Scholar]
  100. 100.
    Fulton AB, Wan KM, Penman S. 1980. The spatial distribution of polyribosomes in 3T3 cells and the associated assembly of proteins into the skeletal framework. Cell 20:3849–57
     [Google Scholar]
  101. 101.
    Isaacs WB, Fulton AB. 1987. Cotranslational assembly of myosin heavy chain in developing cultured skeletal muscle. PNAS 84:176174–78
     [Google Scholar]
  102. 102.
    Gilmore R, Coffey MC, Leone G, McLure K, Lee PW. 1996. Co-translational trimerization of the reovirus cell attachment protein. EMBO J. 15:112651–58
     [Google Scholar]
  103. 103.
    Shieh Y-W, Minguez P, Bork P, Auburger JJ, Guilbride DL et al. 2015. Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science 350:6261678–80
     [Google Scholar]
  104. 104.
    Wells JN, Bergendahl LT, Marsh JA. 2016. Operon gene order is optimized for ordered protein complex assembly. Cell Rep. 14:4679–85
     [Google Scholar]
  105. 105.
    Cassaignau AME, Włodarski T, Chan SHS, Woodburn LF, Bukvin IV et al. 2021. Interactions between nascent proteins and the ribosome surface inhibit co-translational folding. Nat. Chem. 13:1214–20
     [Google Scholar]
  106. 106.
    Marino J, Buholzer KJ, Zosel F, Nettels D, Schuler B. 2018. Charge interactions can dominate coupled folding and binding on the ribosome. Biophys. J. 115:6996–1006
     [Google Scholar]
  107. 107.
    Zhang L, Paakkarinen V, van Wijk KJ, Aro E-M. 1999. Co-translational assembly of the D1 protein into photosystem II. J. Biol. Chem. 274:2316062–67
     [Google Scholar]
  108. 108.
    Zhang L, Paakkarinen V, van Wijk KJ, Aro E-M. 2000. Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12:91769–81
     [Google Scholar]
  109. 109.
    Panasenko OO, Somasekharan SP, Villanyi Z, Zagatti M, Bezrukov F et al. 2019. Co-translational assembly of proteasome subunits in NOT1-containing assemblysomes. Nat. Struct. Mol. Biol. 26:2110–20Shows the proteasomal subunits Rpt1 and Rpt2 assemble co-cotranslationally in trans within cytoplasmic granules termed assemblysomes.
     [Google Scholar]
  110. 110.
    Wagner S, Herrmannová A, Hronová V, Gunišová S, Sen ND et al. 2020. Selective translation complex profiling reveals staged initiation and co-translational assembly of initiation factor complexes. Mol. Cell 79:4546–60
     [Google Scholar]
  111. 111.
    Halbach A, Zhang H, Wengi A, Jablonska Z, Gruber IML et al. 2009. Cotranslational assembly of the yeast SET1C histone methyltransferase complex. EMBO J. 28:192959–70
     [Google Scholar]
  112. 112.
    Kamenova I, Mukherjee P, Conic S, Mueller F, El-Saafin F et al. 2019. Co-translational assembly of mammalian nuclear multisubunit complexes. Nat. Commun. 10:1740
     [Google Scholar]
  113. 113.
    Umlauf D, Bonnet J, Waharte F, Fournier M, Stierle M et al. 2013. The human TREX-2 complex is stably associated with the nuclear pore basket. J. Cell Sci. 126:122656–67
     [Google Scholar]
  114. 114.
    Lautier O, Penzo A, Rouvière JO, Chevreux G, Collet L et al. 2021. Co-translational assembly and localized translation of nucleoporins in nuclear pore complex biogenesis. Mol. Cell 81:112417–27
     [Google Scholar]
  115. 115.
    Seidel M, Becker A, Pereira F, Landry JJM, de Azevedo NTD et al. 2021. Co-translational assembly counteracts promiscuous interactions. bioRxiv 10.1101/2021.07.13.452229. https://doi.org/10.1101/2021.07.13.452229
    [Crossref]
  116. 116.
    Morales-Polanco F, Bates C, Lui J, Casson J, Solari CA et al. 2021. Core fermentation (CoFe) granules focus coordinated glycolytic mRNA localization and translation to fuel glucose fermentation. iScience 24:2102069Shows that mRNAs encoding glycolitic enzymes can colocalize in translationally active RNA granules as translation factories for the effective production of highly expressed proteins.
     [Google Scholar]
  117. 117.
    Heidenreich M, Georgeson JM, Locatelli E, Rovigatti L, Nandi SK et al. 2020. Designer protein assemblies with tunable phase diagrams in living cells. Nat. Chem. Biol. 16:9939–45
     [Google Scholar]
  118. 118.
    Liu F, Jones DK, de Lange WJ, Robertson GA. 2016. Cotranslational association of mRNA encoding subunits of heteromeric ion channels. PNAS 113:174859–64
     [Google Scholar]
  119. 119.
    Zhao N, Kamijo K, Fox PD, Oda H, Morisaki T et al. 2019. A genetically encoded probe for imaging nascent and mature HA-tagged proteins in vivo. Nat. Commun. 10:2947
     [Google Scholar]
  120. 120.
    Pizzinga M, Bates C, Lui J, Forte G, Morales-Polanco F et al. 2019. Translation factor mRNA granules direct protein synthetic capacity to regions of polarized growth. J. Cell Biol. 218:51564–81
     [Google Scholar]
  121. 121.
    Chen X, Mayr C. 2021. A working model for condensate RNA-binding proteins as matchmakers for protein complex assembly. RNA 28:76–87
     [Google Scholar]
  122. 122.
    Redick SD, Schwarzbauer JE. 1995. Rapid intracellular assembly of tenascin hexabrachions suggests a novel cotranslational process. J. Cell Sci. 108:41761–69
     [Google Scholar]
  123. 123.
    Mrazek J, Toso D, Ryazantsev S, Zhang X, Zhou ZH et al. 2014. Polyribosomes are molecular 3D nanoprinters that orchestrate the assembly of vault particles. ACS Nano 8:1111552–59
     [Google Scholar]
  124. 124.
    Veitia RA. 2007. Exploring the molecular etiology of dominant-negative mutations. Plant Cell 19:123843–51
     [Google Scholar]
  125. 125.
    Natan E, Wells JN, Teichmann SA, Marsh JA. 2017. Regulation, evolution and consequences of cotranslational protein complex assembly. Curr. Opin. Struct. Biol. 42:90–97
     [Google Scholar]
  126. 126.
    Niazi S, Purohit M, Niazi JH. 2018. Role of p53 circuitry in tumorigenesis: a brief review. Eur. J. Med. Chem. 158:7–24
     [Google Scholar]
  127. 127.
    Nicholls CD, McLure KG, Shields MA, Lee PWK. 2002. Biogenesis of p53 involves cotranslational dimerization of monomers and posttranslational dimerization of dimers: implications on the dominant negative effect. J. Biol. Chem. 277:1512937–45
     [Google Scholar]
  128. 128.
    Lin L, DeMartino GN, Greene WC. 1998. Cotranslational biogenesis of NF-κB p50 by the 26S proteasome. Cell 92:6819–28
     [Google Scholar]
  129. 129.
    Lin L, DeMartino GN, Greene WC. 2000. Cotranslational dimerization of the Rel homology domain of NF-κB1 generates p50-p105 heterodimers and is required for effective p50 production. EMBO J. 19:174712–22
     [Google Scholar]
  130. 130.
    Das S, Vera M, Gandin V, Singer RH, Tutucci E. 2021. Intracellular mRNA transport and localized translation. Nat. Rev. Mol. Cell Biol. 22:7483–504
     [Google Scholar]
  131. 131.
    Sil A, Herskowitz I. 1996. Identification of an asymmetrically localized determinant, Ash1p, required for lineage-specific transcription of the yeast HO gene. Cell 84:5711–22
     [Google Scholar]
  132. 132.
    Böhl F, Kruse C, Frank A, Ferring D, Jansen R. 2000. She2p, a novel RNA-binding protein tethers ASH1 mRNA to the Myo4p myosin motor via She3p. EMBO J. 19:205514–24
     [Google Scholar]
  133. 133.
    Chartrand P, Meng XH, Huttelmaier S, Donato D, Singer RH. 2002. Asymmetric sorting of Ash1p in yeast results from inhibition of translation by localization elements in the mRNA. Mol. Cell 10:61319–30
     [Google Scholar]
  134. 134.
    Paquin N, Ménade M, Poirier G, Donato D, Drouet E, Chartrand P. 2007. Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1p by the casein kinase Yck1p. Mol. Cell 26:6795–809
     [Google Scholar]
  135. 135.
    Yoon YJ, Wu B, Buxbaum AR, Das S, Tsai A et al. 2016. Glutamate-induced RNA localization and translation in neurons. PNAS 113:44E6877–86
     [Google Scholar]
  136. 136.
    Buxbaum AR, Wu B, Singer RH. 2014. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343:6169419–22
     [Google Scholar]
  137. 137.
    Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G. 2005. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 118:112425–33
     [Google Scholar]
  138. 138.
    Shurtleff MJ, Itzhak DN, Hussmann JA, Oakdale NTS, Costa EA et al. 2018. The ER membrane protein complex interacts cotranslationally to enable biogenesis of multipass membrane proteins. eLife 7:e37018
     [Google Scholar]
  139. 139.
    Lu J, Robinson JM, Edwards D, Deutsch C. 2001. T1–T1 interactions occur in ER membranes while nascent Kv peptides are still attached to ribosomes. Biochemistry 40:3710934–46
     [Google Scholar]
  140. 140.
    Pleiner T, Hazu M, Tomaleri GP, Januszyk K, Oania RS et al. 2021. WNK1 is an assembly factor for the human ER membrane protein complex. Mol. Cell 81:132693–704.e12
     [Google Scholar]
  141. 141.
    Ivanov P, Kedersha N, Anderson P 2019. Stress granules and processing bodies in translational control. Cold Spring Harb. Perspect. Biol. 11:5a032813
     [Google Scholar]
  142. 142.
    Batada NN, Shepp LA, Siegmund DO. 2004. Stochastic model of protein-protein interaction: Why signaling proteins need to be colocalized. PNAS 101:176445–49
     [Google Scholar]
  143. 143.
    Chouaib R, Safieddine A, Pichon X, Imbert A, Kwon OS et al. 2020. A dual protein-mRNA localization screen reveals compartmentalized translation and widespread co-translational RNA targeting. Dev. Cell 54:6773–91
     [Google Scholar]
  144. 144.
    Lui J, Castelli LM, Pizzinga M, Simpson CE, Hoyle NP et al. 2014. Granules harboring translationally active mRNAs provide a platform for P-body formation following stress. Cell Rep. 9:3944–54
     [Google Scholar]
  145. 145.
    Dufourt J, Bellec M, Trullo A, Dejean M, De Rossi S et al. 2021. Imaging translation dynamics in live embryos reveals spatial heterogeneities. Science 372:6544840–44
     [Google Scholar]
  146. 146.
    Trcek T, Douglas TE, Grosch M, Yin Y, Eagle WVI et al. 2020. Sequence-independent self-assembly of germ granule mRNAs into homotypic clusters. Mol. Cell 78:5941–50
     [Google Scholar]
  147. 147.
    Hyjek-Składanowska M, Bajczyk M, Gołębiewski M, Nuc P, Kołowerzo-Lubnau A et al. 2020. Core spliceosomal Sm proteins as constituents of cytoplasmic mRNPs in plants. Plant J. 103:31155–73
     [Google Scholar]
  148. 148.
    Ma W, Mayr C. 2018. A membraneless organelle associated with the endoplasmic reticulum enables 3′ UTR-mediated protein-protein interactions. Cell 175:61492–506Shows RBP TIS11B forms a condensate that facilitates protein complex assembly.
     [Google Scholar]
  149. 149.
    Chang L, Shav-Tal Y, Trcek T, Singer RH, Goldman RD. 2006. Assembling an intermediate filament network by dynamic cotranslation. J. Cell Biol. 172:5747–58
     [Google Scholar]
  150. 150.
    Hampoelz B, Schwarz A, Ronchi P, Bragulat-Teixidor H, Tischer C et al. 2019. Nuclear pores assemble from nucleoporin condensates during oogenesis. Cell 179:3671–86
     [Google Scholar]
  151. 151.
    Nair RR, Zabezhinsky D, Gelin-Licht R, Haas BJ, Dyhr MCA et al. 2021. Multiplexed mRNA assembly into ribonucleoprotein particles plays an operon-like role in the control of yeast cell physiology. eLife 10:e66050Shows functionally related mRNAs can arrange in condensates from the moment they are being transcribed.
     [Google Scholar]
  152. 152.
    Tarbier M, Mackowiak SD, Frade J, Catuara-Solarz S, Biryukova I et al. 2020. Nuclear gene proximity and protein interactions shape transcript covariations in mammalian single cells. Nat. Commun. 11:5445
     [Google Scholar]
  153. 153.
    Keene JD. 2007. RNA regulons: coordination of post-transcriptional events. Nat. Rev. Genet. 8:7533–43
     [Google Scholar]
  154. 154.
    Hieronymus H, Silver PA. 2003. Genome-wide analysis of RNA–protein interactions illustrates specificity of the mRNA export machinery. Nat. Genet. 33:2155–61
     [Google Scholar]
  155. 155.
    Gama-Carvalho M, Barbosa-Morais NL, Brodsky AS, Silver PA, Carmo-Fonseca M. 2006. Genome-wide identification of functionally distinct subsets of cellular mRNAs associated with two nucleocytoplasmic-shuttling mammalian splicing factors. Genome Biol. 7:11R113
     [Google Scholar]
  156. 156.
    Juszkiewicz S, Hegde RS. 2018. Quality control of orphaned proteins. Mol. Cell 71:3443–57
     [Google Scholar]
  157. 157.
    Herhaus L, Dikic I. 2018. Dimerization quality control via ubiquitylation. Science 362:6411151–52
     [Google Scholar]
/content/journals/10.1146/annurev-biodatasci-121721-095858
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Cotranslational Mechanisms of Protein Biogenesis and Complex Assembly in Eukaryotes
Annual Review of Biomedical Data Science 5, 67 (2022); https://doi.org/10.1146/annurev-biodatasci-121721-095858
/content/journals/10.1146/annurev-biodatasci-121721-095858
/content/journals/10.1146/annurev-biodatasci-121721-095858
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