6xmt Citations

The endoplasmic reticulum P5A-ATPase is a transmembrane helix dislocase.

Science 369 (2020)
Related entries: 6xmp, 6xmq, 6xms, 6xmu

Cited: 56 times
EuropePMC logo PMID: 32973005

Abstract

Organelle identity depends on protein composition. How mistargeted proteins are selectively recognized and removed from organelles is incompletely understood. Here, we found that the orphan P5A-adenosine triphosphatase (ATPase) transporter ATP13A1 (Spf1 in yeast) directly interacted with the transmembrane segment (TM) of mitochondrial tail-anchored proteins. P5A-ATPase activity mediated the extraction of mistargeted proteins from the endoplasmic reticulum (ER). Cryo-electron microscopy structures of Saccharomyces cerevisiae Spf1 revealed a large, membrane-accessible substrate-binding pocket that alternately faced the ER lumen and cytosol and an endogenous substrate resembling an α-helical TM. Our results indicate that the P5A-ATPase could dislocate misinserted hydrophobic helices flanked by short basic segments from the ER. TM dislocation by the P5A-ATPase establishes an additional class of P-type ATPase substrates and may correct mistakes in protein targeting or topogenesis.

Articles - 6xmt mentioned but not cited (3)

  1. The endoplasmic reticulum P5A-ATPase is a transmembrane helix dislocase. McKenna MJ, Sim SI, Ordureau A, Wei L, Harper JW, Shao S, Park E. Science 369 eabc5809 (2020)
  2. Structure and transport mechanism of P5B-ATPases. Li P, Wang K, Salustros N, Grønberg C, Gourdon P. Nat Commun 12 3973 (2021)
  3. Cryo-EM reveals mechanistic insights into lipid-facilitated polyamine export by human ATP13A2. Tomita A, Daiho T, Kusakizako T, Yamashita K, Ogasawara S, Murata T, Nishizawa T, Nureki O. Mol Cell 81 4799-4809.e5 (2021)


Reviews citing this publication (14)

  1. The mechanisms of integral membrane protein biogenesis. Hegde RS, Keenan RJ. Nat Rev Mol Cell Biol 23 107-124 (2022)
  2. Order through destruction: how ER-associated protein degradation contributes to organelle homeostasis. Christianson JC, Carvalho P. EMBO J 41 e109845 (2022)
  3. Capture and delivery of tail-anchored proteins to the endoplasmic reticulum. Farkas Á, Bohnsack KE. J Cell Biol 220 e202105004 (2021)
  4. ER-SURF: Riding the Endoplasmic Reticulum Surface to Mitochondria. Koch C, Schuldiner M, Herrmann JM. Int J Mol Sci 22 9655 (2021)
  5. Fidelity of Cotranslational Protein Targeting to the Endoplasmic Reticulum. Hsieh HH, Shan SO. Int J Mol Sci 23 281 (2021)
  6. Membrane protein folding and quality control. Phillips BP, Miller EA. Curr Opin Struct Biol 69 50-54 (2021)
  7. Protein Quality Control at the Mitochondrial Surface. den Brave F, Gupta A, Becker T. Front Cell Dev Biol 9 795685 (2021)
  8. The Molecular Biodiversity of Protein Targeting and Protein Transport Related to the Endoplasmic Reticulum. Tirincsi A, Sicking M, Hadzibeganovic D, Haßdenteufel S, Lang S. Int J Mol Sci 23 143 (2021)
  9. The Roles of ATP13A2 Gene Mutations Leading to Abnormal Aggregation of α-Synuclein in Parkinson's Disease. Zhang F, Wu Z, Long F, Tan J, Gong N, Li X, Lin C. Front Cell Neurosci 16 927682 (2022)
  10. Cell death induction in Aspergillus fumigatus: accentuating drug toxicity through inhibition of the unfolded protein response (UPR). Guirao-Abad JP, Weichert M, Askew DS. Curr Res Microb Sci 3 100119 (2022)
  11. Cryo-EM structures of the endoplasmic reticulum membrane complex. Bai L, Li H. FEBS J 289 102-112 (2022)
  12. P-type ATPases: Many more enigmas left to solve. Palmgren M. J Biol Chem 299 105352 (2023)
  13. Spf1 and Ste24: quality controllers of transmembrane protein topology in the eukaryotic cell. Tipper DJ, Harley CA. Front Cell Dev Biol 11 1220441 (2023)
  14. MR1 antigen presentation to MAIT cells and other MR1-restricted T cells. McWilliam HEG, Villadangos JA. Nat Rev Immunol (2023)

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  1. MTCH2 is a mitochondrial outer membrane protein insertase. Guna A, Stevens TA, Inglis AJ, Replogle JM, Esantsi TK, Muthukumar G, Shaffer KCL, Wang ML, Pogson AN, Jones JJ, Lomenick B, Chou TF, Weissman JS, Voorhees RM. Science 378 317-322 (2022)
  2. A unified evolutionary origin for the ubiquitous protein transporters SecY and YidC. Lewis AJO, Hegde RS. BMC Biol 19 266 (2021)
  3. ER targeting of non-imported mitochondrial carrier proteins is dependent on the GET pathway. Xiao T, Shakya VP, Hughes AL. Life Sci Alliance 4 e202000918 (2021)
  4. ATP2, The essential P4-ATPase of malaria parasites, catalyzes lipid-stimulated ATP hydrolysis in complex with a Cdc50 β-subunit. Lamy A, Macarini-Bruzaferro E, Dieudonné T, Perálvarez-Marín A, Lenoir G, Montigny C, le Maire M, Vázquez-Ibar JL. Emerg Microbes Infect 10 132-147 (2021)
  5. Structural basis of polyamine transport by human ATP13A2 (PARK9). Sim SI, von Bülow S, Hummer G, Park E. Mol Cell 81 4635-4649.e8 (2021)
  6. The ER protein Ema19 facilitates the degradation of nonimported mitochondrial precursor proteins. Laborenz J, Bykov YS, Knöringer K, Räschle M, Filker S, Prescianotto-Baschong C, Spang A, Tatsuta T, Langer T, Storchová Z, Schuldiner M, Herrmann JM. Mol Biol Cell 32 664-674 (2021)
  7. Dynamic membranes: the multiple roles of P4 and P5 ATPases. López-Marqués RL, Davis JA, Harper JF, Palmgren M. Plant Physiol 185 619-631 (2021)
  8. Structural insights into the activation of autoinhibited human lipid flippase ATP8B1 upon substrate binding. Cheng MT, Chen Y, Chen ZP, Liu X, Zhang Z, Chen Y, Hou WT, Zhou CZ. Proc Natl Acad Sci U S A 119 e2118656119 (2022)
  9. ATP13A1 prevents ERAD of folding-competent mislocalized and misoriented proteins. McKenna MJ, Adams BM, Chu V, Paulo JA, Shao S. Mol Cell 82 4277-4289.e10 (2022)
  10. Structural basis of the P4B ATPase lipid flippase activity. Bai L, Jain BK, You Q, Duan HD, Takar M, Graham TR, Li H. Nat Commun 12 5963 (2021)
  11. Cryo-EM structures and transport mechanism of human P5B type ATPase ATP13A2. Chen X, Zhou M, Zhang S, Yin J, Zhang P, Xuan X, Wang P, Liu Z, Zhou B, Yang M. Cell Discov 7 106 (2021)
  12. Conformational cycle of human polyamine transporter ATP13A2. Mu J, Xue C, Fu L, Yu Z, Nie M, Wu M, Chen X, Liu K, Bu R, Huang Y, Yang B, Han J, Jiang Q, Chan KC, Zhou R, Li H, Huang A, Wang Y, Liu Z. Nat Commun 14 1978 (2023)
  13. Structural insights into metazoan pretargeting GET complexes. Keszei AFA, Yip MCJ, Hsieh TC, Shao S. Nat Struct Mol Biol 28 1029-1037 (2021)
  14. The Endoplasmic Reticulum ATP13A1 is Essential for MAVS-Mediated Antiviral Innate Immunity. Zhang R, Hou X, Wang C, Li J, Zhu J, Jiang Y, Hou F. Adv Sci (Weinh) 9 e2203831 (2022)
  15. A genome-wide optical pooled screen reveals regulators of cellular antiviral responses. Carlson RJ, Leiken MD, Guna A, Hacohen N, Blainey PC. Proc Natl Acad Sci U S A 120 e2210623120 (2023)
  16. Intramembrane client recognition potentiates the chaperone functions of calnexin. Bloemeke N, Meighen-Berger K, Hitzenberger M, Bach NC, Parr M, Coelho JP, Frishman D, Zacharias M, Sieber SA, Feige MJ. EMBO J 41 e110959 (2022)
  17. Endoplasmic reticulum calnexins participate in the primary root growth response to phosphate deficiency. Montpetit J, Clúa J, Hsieh YF, Vogiatzaki E, Müller J, Abel S, Strasser R, Poirier Y. Plant Physiol 191 1719-1733 (2023)
  18. GET pathway mediates transfer of mislocalized tail-anchored proteins from mitochondria to the ER. Matsumoto S, Ono S, Shinoda S, Kakuta C, Okada S, Ito T, Numata T, Endo T. J Cell Biol 221 e202104076 (2022)
  19. Mechanism of signal-anchor triage during early steps of membrane protein insertion. Wu H, Hegde RS. Mol Cell 83 961-973.e7 (2023)
  20. Pleiotropic Effects of the P5-Type ATPase SpfA on Stress Response Networks Contribute to Virulence in the Pathogenic Mold Aspergillus fumigatus. Guirao-Abad JP, Weichert M, Luengo-Gil G, Sze Wah Wong S, Aimanianda V, Grisham C, Malev N, Reddy S, Woollett L, Askew DS. mBio 12 e0273521 (2021)
  21. Positively charged amino acids at the N terminus of select mitochondrial proteins mediate early recognition by import proteins αβ'-NAC and Sam37. Avendaño-Monsalve MC, Mendoza-Martínez AE, Ponce-Rojas JC, Poot-Hernández AC, Rincón-Heredia R, Funes S. J Biol Chem 298 101984 (2022)
  22. Protein biosynthesis at the ER: finding the right accessories. Shao S. Mol Biol Cell 34 (2023)
  23. The CATP-8/P5A-type ATPase functions in multiple pathways during neuronal patterning. Tang LTH, Trivedi M, Freund J, Salazar CJ, Rahman M, Ramirez-Suarez NJ, Lee G, Wang Y, Grant BD, Bülow HE. PLoS Genet 17 e1009475 (2021)
  24. The P5-type ATPase ATP13A1 modulates major histocompatibility complex I-related protein 1 (MR1)-mediated antigen presentation. Kulicke CA, De Zan E, Hein Z, Gonzalez-Lopez C, Ghanwat S, Veerapen N, Besra GS, Klenerman P, Christianson JC, Springer S, Nijman SM, Cerundolo V, Salio M. J Biol Chem 298 101542 (2022)
  25. A selectivity filter in the ER membrane protein complex limits protein misinsertion at the ER. Pleiner T, Hazu M, Pinton Tomaleri G, Nguyen VN, Januszyk K, Voorhees RM. J Cell Biol 222 e202212007 (2023)
  26. ATP hydrolytic activity of purified Spf1p correlate with micellar lipid fluidity and is dependent on conserved residues in transmembrane helix M1. Ipsen JØ, Sørensen DM. PLoS One 17 e0274908 (2022)
  27. Adding New Chemistries to the Central Dogma of Molecular Biology. Diercks CS, Dik DA, Schultz PG. Chem 7 2883-2895 (2021)
  28. Cryo-EM of the ATP11C flippase reconstituted in Nanodiscs shows a distended phospholipid bilayer inner membrane around transmembrane helix 2. Nakanishi H, Hayashida K, Nishizawa T, Oshima A, Abe K. J Biol Chem 298 101498 (2022)
  29. Evolution of Plant Na+-P-Type ATPases: From Saline Environments to Land Colonization. Dabravolski SA, Isayenkov SV. Plants (Basel) 10 221 (2021)
  30. Highly exposed segment of the Spf1p P5A-ATPase near transmembrane M5 detected by limited proteolysis. Petrovich GD, Corradi GR, Pavan CH, Noli Truant S, Adamo HP. PLoS One 16 e0245679 (2021)
  31. Mitochondrial antiviral-signalling protein is a client of the BAG6 protein quality control complex. Roboti P, Lawless C, High S. J Cell Sci 135 jcs259596 (2022)
  32. Structural basis of ion uptake in copper-transporting P1B-type ATPases. Salustros N, Grønberg C, Abeyrathna NS, Lyu P, Orädd F, Wang K, Andersson M, Meloni G, Gourdon P. Nat Commun 13 5121 (2022)
  33. The ER membrane protein complex restricts mitophagy by controlling BNIP3 turnover. Delgado JM, Shepard LW, Lamson SW, Liu SL, Shoemaker CJ. EMBO J 43 32-60 (2024)
  34. The unfolded protein response of the endoplasmic reticulum supports mitochondrial biogenesis by buffering nonimported proteins. Knöringer K, Groh C, Krämer L, Stein KC, Hansen KG, Zimmermann J, Morgan B, Herrmann JM, Frydman J, Boos F. Mol Biol Cell 34 ar95 (2023)
  35. ATP13A2 modifies mitochondrial localization of overexpressed TOM20 to autolysosomal pathway. Hatori Y, Kanda Y, Nonaka S, Nakanishi H, Kitazawa T. PLoS One 17 e0276823 (2022)
  36. Activation and substrate specificity of the human P4-ATPase ATP8B1. Dieudonné T, Kümmerer F, Laursen MJ, Stock C, Flygaard RK, Khalid S, Lenoir G, Lyons JA, Lindorff-Larsen K, Nissen P. Nat Commun 14 7492 (2023)
  37. Proteomic screens of SEL1L-HRD1 ER-associated degradation substrates reveal its role in glycosylphosphatidylinositol-anchored protein biogenesis. Wei X, Lu Y, Lin LL, Zhang C, Chen X, Wang S, Wu SA, Li ZJ, Quan Y, Sun S, Qi L. Nat Commun 15 659 (2024)
  38. Reconstitution of Msp1 Extraction Activity with Fully Purified Components. Fresenius HL, Wohlever ML. J Vis Exp (2021)
  39. Yeast as a tool for membrane protein production and structure determination. Carlesso A, Delgado R, Ruiz Isant O, Uwangue O, Valli D, Bill RM, Hedfalk K. FEMS Yeast Res 22 foac047 (2022)