LYRM protein

Leucine-Tyrosine-Arginine motif-containing proteins, also known as LYRM proteins or simply LYRMs, are a superfamily of small (11–22 kDa), basic, predominantly mitochondrial proteins found exclusively in eukaryotes and named after their conserved LYR-like motif near the N-terminus.[1][2] They function as accessory subunits or assembly factors of OXPHOS complexes I, II, III and V and play essential roles in iron–sulfur (Fe–S) cluster biogenesis, mitochondrial translation, electron transfer flavoprotein (ETF) function, and acetate metabolism.[3][1] Most LYRM proteins depend on mitochondrial fatty acid synthesis (mtFAS) for their function, as they are allosterically activated by binding to acylated mitochondrial acyl carrier protein (acyl-mtACP).[4] It has been proposed that this mechanism evolved to protect cells from the toxic interaction of iron and oxygen.[5]

Characteristics

LYRM proteins constitute a conserved family of small mitochondrial proteins defined by sequence homology to the Complex1_LYR-like superfamily (Pfam clan CL0491), which was identified by bioinformatic analysis and curated by P. Coggill (EMBL-EBI).[2][6] The family was originally defined based on LYRM4, which stabilizes the cysteine desulfurase NFS1 within the mitochondrial iron–sulfur cluster (ISC) assembly machinery.[7] The presence of an LYR tripeptide alone is not sufficient to classify a protein as an LYRM, as additional conserved amino acid residues must also be present.[2] Members of this family share the following characteristic features:

  • Sequence features:
    • a conserved LYR-like motif near the N-terminus (e.g. LYR, LYK, LFK, TFR),[2]
    • additional conserved amino acid residues downstream of the motif:
  • Structural features:
    • structural homology characterized by a conserved three-α-helix bundle,[1]
    • a hydrophobic channel formed by the three-α-helix bundle, accommodating the fatty acyl chain of acylated mtACP (except FMC1),[1]
  • General properties:

These features distinguish LYRM proteins from the broader term "LYR proteins", which has been used by some authors in the past for proteins that contain an LYR tripeptide—a motif frequently found in mitochondrial proteins such as SDHB, NDUFAF3, or mitochondrial ribosomal proteins—but that lack the additional defining characteristics of the LYRM family.[2]

Occurrence and synthesis

LYRM proteins are found exclusively in eukaryotes, but they differ between species.[1] While LYRM proteins have been lost in anaerobic eukaryotes or are retained only in the form of LYRM4, twelve LYRM proteins occur in humans.[1] With the exception of LYRM3 and LYRM6, which are embedded within mitochondrial Complex I, LYRM proteins are soluble matrix-located proteins.[8] All LYRM proteins have in common that they are found in mitochondrial target complexes that contain iron–sulfur clusters, synthesize them, or are functionally linked to them, such as the electron transfer protein and the mitochondrial ribosome.[5] The only exception is FMC1, which acts at a target complex lacking iron–sulfur clusters, complex V, although this complex has been linked to mitochondrial iron uptake.[5]

They are synthesized in the cytosol by ribosomes after being transcribed from nuclear DNA, and are then imported into the mitochondria.[1] Some members have also been identified in the cytosol and nucleus.[2]

Interaction with mitochondrial acyl carrier protein

With the exception of FMC1, the function of LYRM proteins depends on their interaction with acylated mitochondrial acyl carrier protein (acyl-mtACP), which inserts its fatty acyl chain into a hydrophobic channel of the LYRM protein formed by three α-helices.[1] Upon binding, the fatty acyl chain attached to the flexible 4'-phosphopantetheine arm of mtACP flips from its hydrophobic cavity into that of the LYRM protein.[9] This interaction also requires the LYR-like motif and the highly conserved downstream phenylalanine residue, collectively referred to as the LYR–F motif.[1] While LYRM proteins can interact with 4'-phosphopantetheine-modified mtACP (holo-mtACP) in both its unacylated and acylated form, they exhibit a clear preference and higher affinity for the acylated form.[4] The acylated form of holo-mtACP is generated by mitochondrial fatty acid synthesis (mtFAS) in response to acetyl-CoA availability.[10][4] Fatty acyl chains of 10–16 carbons in length are required for effective binding to LYRM proteins.[11]

Acylation of mtACP is an acetyl-CoA-dependent post-translational modification that is sensitive to perturbations in mitochondrial acetyl-CoA synthesis and allosterically activates those LYRM proteins that function as assembly factors for OXPHOS complexes.[4] It is proposed that this mechanism forms a feedback loop in which acetyl-CoA availability regulates mtACP acylation and LYRM-mediated OXPHOS assembly, thereby increasing NADH and FADH2 oxidation and citric acid cycle activity, which in turn promotes acetyl-CoA consumption.[10] This would allow cells to increase oxidative capacity when substrate is abundant while preventing electron transport chain activity under substrate-limited conditions, thereby reducing reactive oxygen species (ROS) formation.[10]

In addition to their role in OXPHOS assembly, mtACP and LYRM proteins have also been implicated in mitochondrial translation.[1] Although the role of mtFAS in mammalian mitoribosome assembly and mitochondrial translation has not been experimentally studied, structural analyses revealed the LYRM protein L0R8F8 and unacylated mtACP bound to the mitoribosomal assembly factor MALSU1.[12] This finding suggests a distinct mtACP–LYRM binding mode in which mtACP acylation may promote release of the complex, allowing mitoribosome assembly to proceed.[12] Furthermore, LYRM1 is predicted to interact with the mitochondrial translational release factor 1-like (MTRF1L), while LYRM9 is predicted to interact with mitochondrial ribosomal protein L57 (MRPL57).[1]

Overview of members

At least 12 LYRM proteins have been identified in humans (2019):[9]

Overview of human LYRM proteins
LYRM protein LYR-like motif m (kDa) pI Target location Function Interaction partner
LYRM1[9] LYR[2] 14[2] 10[2] Mitoribosome (predicted)[1] Insulin signaling[2] Acyl-mtACP[1], MTRF1L (predicted)[1]
LYRM2[9] LYR[2] 11[2] 11[2] Complex I Associates with Complex I activity[9] Acyl-mtACP[9]
LYRM3/NDUFB9[9] LYK[2] 22[2] 9[2] Complex I Structural subunit[9] Acyl-mtACP[9]
LYRM4/ISD11[9] LYR[2] 11[2] 11[2] Cysteine desulfurase NFS1 Iron-sulfur cluster biogenesis[2] Acyl-mtACP,[9] NFS1[2]
LYRM5[9] LYK[2] 11[2] 10[2] Electron transfer flavoprotein (ETF) Accessory factor Acyl-mtACP[9]
LYRM6/NDUFA6[9] LYR[2] 18[2] 10[2] Complex I Structural subunit[9] Acyl-mtACP,[9] NDUFS3[2]
LYRM7/MZM1L[9] LFK[2] 12[2] 10[2] Complex III Assembly factor[13] Acyl-mtACP,[9] UQCRFS1, HSC20[2]
LYRM8/SDHAF1[9] LYR[2] 13[2] 11[2] Complex II Assembly factor[9] Acyl-mtACP,[9] SDHB, HSC20[2]
LYRM9/C17orf108[9] LYR[2] 10[2] 9[2] Mitoribosome (predicted)[1] Unknown[14] Acyl-mtACP[1], MRPL57 (predicted)[1]
LYRM10[15]/ACN9/SDHAF3/[9] LYK[2] 15[2] 9[2] Complex II Assembly factor[9] Acyl-mtACP,[9] SDHB[2]
FMC1/C7orf55[9] TFR[2] 13[2] 10[2] Complex V Assembly factor[2] Unacylated holo-mtACP[1], ATP12[2]
L0R8F8[9]/AltMiD51[16]/MIEF1-MP[1] Mitoribosome[16] Assembly factor[17] Unacylated holo-mtACP[9]

Function

Iron–sulfur cluster biogensis

In eukaryotes, iron–sulfur (Fe–S) clusters serve as versatile cofactors in redox reactions, electron transport, enzyme catalysis, regulation of gene expression, and DNA repair.[18] They are assembled on the ISCU scaffold protein, with iron donated by frataxin and sulfur provided by the NFS1–LYRM4 complex.[11] This complex binds acyl-mtACP via LYRM4, and this interaction stabilizes the otherwise degradation-prone complex.[11] Once formed, Fe–S clusters are transferred to target proteins by a Fe–S transfer complex composed of ISCU, the co-chaperone HSC20, and the chaperone HSPA9.[11]

The incorporation of iron–sulfur clusters into OXPHOS complexes II and III with the help of other LYRM proteins is covered below under "OXPHOS complex assembly".

OXPHOS complex assembly

The assembly of these complexes depends on a tightly regulated and coordinated process involving transcription and translation of both nuclear- and mitochondrial-encoded subunits, import and assembly of individual subunits, and maturation through the insertion of essential cofactors such as iron–sulfur clusters.[8] OXPHOS complexes can further assemble into higher-order structures known as supercomplexes, whose formation and stability are influenced by interactions between acylated mtACP and LYRM proteins.[5]

Complex I (NADH:ubiquinone oxidoreductase)

Three LYRM proteins—LYRM3, LYRM6, and LYRM2—are known to be associated with Complex I. The first complex of the respiratory chain couples NADH oxidation and ubiquinone reduction to proton pumping across the inner mitochondrial membrane and constitutes the largest single contributor to the proton motive force driving ATP synthesis.[19] Under certain conditions, the reaction can reverse, resulting in the reduction of NAD+.[19]

LYRM3 is an integral accessory subunit of Complex I, positioned in the distal proton-translocating module PD of the membrane arm.[8] It forms a stable heterodimer with the neighboring mtACP, contributing to the stability and assembly of Complex I.[8]

LYRM6 is also an integral accessory subunit of Complex I.[20] It binds near the critical interface between the matrix arm (Q module) and the membrane arm (P module) of Complex I, forming a heterodimer with mtACP.[20] Two adjacent loops of LYRM6 interact directly with central subunits of Complex I, helping stabilize this interface.[20] In particular, LYRM6 plays a key role in stabilizing the TMH1-2 loop of subunit ND3, a structural element essential for the proton pumping mechanism.[20]

LYRM2 is located in mitochondria, directly interacts with Complex I and increases its activity.[13]

Complex II (Succinate dehydrogenase)

LYRM8 and ACN9 are required for the assembly of the Fe–S cluster–containing subunit SDHB in Complex II.[2] As part of the citric acid cycle, Complex II couples the oxidation of succinate to fumarate to the reduction of ubiquinone.[21] The functions of LYRM8 and ACN9 involve interactions with acyl-mtACP.[9]

LYRM8 functions as an assembly factor for Complex II, acting as a bridge between HSC20, as part of the Fe–S cluster transfer complex, and the SDHB subunit.[22] As one of four subunits of Complex II, SDHB plays a central role in transferring electrons from subunit SDHA to ubiquinone via its three iron–sulfur clusters. HSC20 recognizes and binds with high affinity to LYR motifs; however, SDHB itself contains only two L(I)YR motifs, an IYR motif near the N-terminus and a LYR motif closer to the C-terminus.[22][23][21] However, SDHB is not one of the LYRM proteins.[2] Additionally, several aromatic amino acid regions within SDHB enable the transient binding of a LYRM8 protein through its arginine-rich C-terminal domain, thereby providing a LYRM site for HSC20 and thus contributing to Fe–S cluster incorporation into SDHB.[22] Notably, LYRM8 itself also contains two LYR motifs, located at the N-terminus and in the central region, but HSC20 binds exclusively to the N-terminal motif.[22]

ACN9 functions as an assembly factor involved in the maturation of Complex II.[21] Specifically, it contributes to the incorporation of iron–sulfur (Fe–S) clusters into the SDHB subunit, which is essential for Complex II activity.[21] However, its exact molecular role remains to be fully defined.[21] Yeast data indicate that ACN9 plays a role in gluconeogenesis and in converting ethanol or acetate into carbohydrates.[24]

Complex III (Coenzyme Q : cytochrome c – oxidoreductase)

LYRM7 functions as an assembly factor for Complex III, acting as a chaperone for the Rieske iron-sulfur protein.[25] Complex III's task is to transfer electrons from the two-electron carrier ubiquinone to the one-electron carrier cytochrome c via the Q cycle, while pumping protons to build a gradient. It functions as a dimer (CIII2), with each monomer composed of 11 subunits. Among these, three are catalytic: cytochrome b, cytochrome c1, and the Rieske iron-sulfur protein, which contains a [2Fe–2S] cluster (Rieske center).[26] During the assembly process, a stable but non-functional "late core" pre-Complex III forms, containing all subunits except the Rieske iron-sulfur protein and subunit Qcr10.[26] To complete the assembly, LYRM7 binds to and stabilizes the Rieske iron-sulfur protein in the mitochondrial matrix before its translocation to the inner membrane and subsequent integration into the pre-complex.[25] This prevents the Rieske iron-sulfur protein from proteolytic degradation or temperature‑induced aggregation.[27] Final incorporation of both the Rieske iron-sulfur protein and Qcr10 into pre-Complex III is then driven by the AAA-ATPase BCS1L, completing the assembly of complex III.[28][26]

Complex V (ATP synthase)

FMC1 acts as an assembly factor for Complex V by stabilizing ATP12, a chaperone required for proper F1 assembly, particularly under elevated temperatures.[1] Complex V synthesizes ATP from ADP and inorganic phosphate by harnessing the proton motive force generated by the electron transport chain through a rotary catalytic mechanism.[29] It consists of an Fo domain embedded in the inner mitochondrial membrane that translocates protons, and a matrix-exposed F₁ domain where ATP synthesis occurs.[29] Within the F₁ domain, the catalytic hexameric ring of alternating α- and β-subunits requires ATP12 for assembly, with FMC1 supporting ATP12 at elevated temperatures; without this, subunits are not incorporated properly and aggregate in the mitochondrial matrix.[30] Although FMC1 belongs to the LYRM protein family, its function is independent of acylated mtACP, consistent with the absence of key residues of the LYR motif and a channel formed by its three α-helices that is not sufficiently hydrophobic.[1] Nevertheless, FMC1interacts with unacylated mtACP, enabling F1 domain assembly even when acetyl-CoA is limited.[1] This ensures that Complex V remains functional during metabolic stress, allowing it to operate in reverse and hydrolyze ATP to maintain the proton gradient required for protein import and other transport processes.[1]

Electron transfer flavoprotein function

LYRM5 interacts with the two subunits ETFA and ETFB of electron transfer flavoprotein (ETF), which destabilizes the FAD binding site, leading to the release of FAD and thereby to an interruption of normal electron transfer.[31] ETF functions as an electron carrier, transiently docking with mitochondrial flavoproteins involved in fatty acid and amino acid oxidation (e.g., acyl-CoA dehydrogenases, isovaleryl-CoA dehydrogenase), accepting electrons as its own FAD is reduced to FADH2.[32] The reduced ETF then dissociates and transfers the electrons to ETF:ubiquinone oxidoreductase (ETF:QO), an enzyme embedded in the inner mitochondrial membrane that also contains FAD.[32] ETF:QO is thereby reduced and passes the electrons to ubiquinone (CoQ10) in the respiratory chain.[31] Unlike other LYRM family members, LYRM5 lacks the characteristic leucine–tyrosine–arginine motif and instead contains a leucine–tyrosine–lysine motif.[1]

Mitoribosome assembly

The LYRM protein L0R8F8 and mtACP function as assembly factors for the human mitoribosome.[17] Mitoribosomes translate mitochondrial mRNAs into 13 specific proteins, which are exclusively incorporated as structural subunits into Complexes I, III, IV, and V of the mitochondrial respiratory chain.[33] In the late stages of human mitoribosome large subunit (mt-LSU) maturation, a complex composed of MALSU1, L0R8F8, and mtACP associates with the mt-LSU.[17] This complex sterically prevents premature association with the small subunit (mt-SSU), thereby regulating the timing of mitoribosome subunit joining.[17] Structural analyses have shown that the interaction between L0R8F8 and mtACP is mediated by the LYR motif of L0R8F8 and the 4'-phosphopantetheine moiety of mtACP.[17] Notably, in this context, mtACP is found in its unacylated form holo-mtACP, and no acyl chain density is observed in the structural data.[17][12]

Clinical significance

Defects in human LYRMs, due to their critical role in mitochondrial function, have been linked to severe diseases:[1]

References

  1. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z aa ab ac Dohnálek, Vít; Doležal, Pavel (May 2024). "Installation of LYRM proteins in early eukaryotes to regulate the metabolic capacity of the emerging mitochondrion". Open Biology. 14 (5). doi:10.1098/rsob.240021. ISSN 2046-2441. PMC 11293456. PMID 38772414.
  2. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z aa ab ac ad ae af ag ah ai aj ak al am an ao ap aq ar as at au av aw ax ay az ba bb bc bd be bf bg bh bi Angerer, Heike (2015-02-12). "Eukaryotic LYR Proteins Interact with Mitochondrial Protein Complexes". Biology. 4 (1): 133–150. doi:10.3390/biology4010133. ISSN 2079-7737. PMC 4381221. PMID 25686363.
  3. ^ Angerer, Heike (2013-10-01). "The superfamily of mitochondrial Complex1_LYR motif-containing (LYRM) proteins". Biochemical Society Transactions. 41 (5): 1335–1341. doi:10.1042/BST20130116. ISSN 0300-5127. PMID 24059529.
  4. ^ a b c d Van Vranken, Jonathan G.; Nowinski, Sara M.; Clowers, Katie J.; Jeong, Mi-Young; Ouyang, Yeyun; Berg, Jordan A.; Gygi, Jeremy P.; Gygi, Steven P.; Winge, Dennis R.; Rutter, Jared (August 2018). "ACP Acylation Is an Acetyl-CoA-Dependent Modification Required for Electron Transport Chain Assembly". Molecular Cell. 71 (4): 567–580.e4. doi:10.1016/j.molcel.2018.06.039. PMC 6104058. PMID 30118679.
  5. ^ a b c d e Murdock, Deborah G.; Janssen, Kevin A.; Keller, Kierstin; Mitchell, Katherine L.; Beauplan, Maina; O’Brien, William T.; D’Alessandro, Lia; Haltom, Jeffrey A.; Wallace, Douglas C. (2025-10-07). "A mouse model of MEPAN demonstrates a role for mitochondrial fatty acid synthesis in iron–sulfur cluster and supercomplex formation". Proceedings of the National Academy of Sciences. 122 (40). doi:10.1073/pnas.2506761122. ISSN 0027-8424. PMC 12519216. PMID 41021813.
  6. ^ Maio, Nunziata; Rouault, Tracey A. (July 2022). "Mammalian iron sulfur cluster biogenesis: From assembly to delivery to recipient proteins with a focus on novel targets of the chaperone and co‐chaperone proteins". IUBMB Life. 74 (7): 684–704. doi:10.1002/iub.2593. ISSN 1521-6543. PMC 10118776. PMID 35080107.
  7. ^ Ivanova, Aneta; Gill-Hille, Mabel; Huang, Shaobai; Branca, Rui M.; Kmiec, Beata; Teixeira, Pedro F.; Lehtiö, Janne; Whelan, James; Murcha, Monika W. (December 2019). "A Mitochondrial LYR Protein Is Required for Complex I Assembly". Plant Physiology. 181 (4): 1632–1650. doi:10.1104/pp.19.00822. ISSN 0032-0889. PMC 6878026. PMID 31601645.
  8. ^ a b c d Saha, Saurabh; Parlar, Simge; Meyer, Etienne H.; Murcha, Monika W. (February 2025). "The complex I subunit B22 contains a LYR domain that is crucial for an interaction with the mitochondrial acyl carrier protein SDAP1". The Plant Journal. 121 (4): 1534. Bibcode:2025PlJ...121.1534S. doi:10.1111/tpj.70028. ISSN 0960-7412. PMC 11843852. PMID 39981882.
  9. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z aa ab ac Masud, Ali J.; Kastaniotis, Alexander J.; Rahman, M. Tanvir; Autio, Kaija J.; Hiltunen, J. Kalervo (2019-12-01). "Mitochondrial acyl carrier protein (ACP) at the interface of metabolic state sensing and mitochondrial function". Biochimica et Biophysica Acta (BBA) - Molecular Cell Research. 1866 (12) 118540. doi:10.1016/j.bbamcr.2019.118540. ISSN 0167-4889.
  10. ^ a b c Nowinski, Sara M; Solmonson, Ashley; Rusin, Scott F; Maschek, J Alan; Bensard, Claire L; Fogarty, Sarah; Jeong, Mi-Young; Lettlova, Sandra; Berg, Jordan A; Morgan, Jeffrey T; Ouyang, Yeyun; Naylor, Bradley C; Paulo, Joao A; Funai, Katsuhiko; Cox, James E (2020-08-17). "Mitochondrial fatty acid synthesis coordinates oxidative metabolism in mammalian mitochondria". eLife. 9. doi:10.7554/eLife.58041. ISSN 2050-084X. PMC 7470841. PMID 32804083.
  11. ^ a b c d Tang, Jia Xin; Thompson, Kyle; Taylor, Robert W.; Oláhová, Monika (2020-05-28). "Mitochondrial OXPHOS Biogenesis: Co-Regulation of Protein Synthesis, Import, and Assembly Pathways". International Journal of Molecular Sciences. 21 (11): 3820. doi:10.3390/ijms21113820. ISSN 1422-0067. PMC 7312649. PMID 32481479.
  12. ^ a b c Wedan, Riley J.; Longenecker, Jacob Z.; Nowinski, Sara M. (January 2024). "Mitochondrial fatty acid synthesis is an emergent central regulator of mammalian oxidative metabolism". Cell Metabolism. 36 (1): 36–47. doi:10.1016/j.cmet.2023.11.017. PMC 10843818. PMID 38128528.
  13. ^ a b Huang, Qi; Chen, Zhigang; Cheng, Pu; Jiang, Zhou; Wang, Zhen; Huang, Yucheng; Yang, Chenghui; Pan, Jun; Qiu, Fuming; Huang, Jian (2019-07-28). "LYRM2 directly regulates complex I activity to support tumor growth in colorectal cancer by oxidative phosphorylation". Cancer Letters. 455: 36–47. doi:10.1016/j.canlet.2019.04.021. ISSN 0304-3835.
  14. ^ Pei, Jimin; Zhang, Jing; Cong, Qian (2022-09-15). "Human mitochondrial protein complexes revealed by large-scale coevolution analysis and deep learning-based structure modeling". Bioinformatics. 38 (18): 4301–4311. doi:10.1093/bioinformatics/btac527. ISSN 1367-4803.
  15. ^ "SDHAF3 succinate dehydrogenase complex assembly factor 3 [Homo sapiens (human)] - Gene - NCBI". www.ncbi.nlm.nih.gov. Retrieved 2025-05-26.
  16. ^ a b Dibley, Marris G.; Formosa, Luke E.; Lyu, Baobei; Reljic, Boris; McGann, Dylan; Muellner-Wong, Linden; Kraus, Felix; Sharpe, Alice J.; Stroud, David A.; Ryan, Michael T. (January 2020). "The Mitochondrial Acyl-carrier Protein Interaction Network Highlights Important Roles for LYRM Family Members in Complex I and Mitoribosome Assembly". Molecular & Cellular Proteomics. 19 (1): 65–77. doi:10.1074/mcp.RA119.001784. PMC 6944232. PMID 31666358.
  17. ^ a b c d e f Brown, Alan; Rathore, Sorbhi; Kimanius, Dari; Aibara, Shintaro; Bai, Xiao-chen; Rorbach, Joanna; Amunts, Alexey; Ramakrishnan, V (October 2017). "Structures of the human mitochondrial ribosome in native states of assembly". Nature Structural & Molecular Biology. 24 (10): 866–869. doi:10.1038/nsmb.3464. ISSN 1545-9993. PMC 5633077. PMID 28892042.
  18. ^ Vanlander, A. V.; Van Coster, R. (June 2018). "Clinical and genetic aspects of defects in the mitochondrial iron–sulfur cluster synthesis pathway". Journal of Biological Inorganic Chemistry. 23 (4): 495–506. doi:10.1007/s00775-018-1550-z. ISSN 0949-8257. PMC 6006192. PMID 29623423.
  19. ^ a b Kampjut, Domen; Sazanov, Leonid A. (June 2022). "Structure of respiratory complex I – An emerging blueprint for the mechanism". Current Opinion in Structural Biology. 74 102350. doi:10.1016/j.sbi.2022.102350. PMC 7613608. PMID 35316665.
  20. ^ a b c d Galemou Yoga, Etienne; Parey, Kristian; Djurabekova, Amina; Haapanen, Outi; Siegmund, Karin; Zwicker, Klaus; Sharma, Vivek; Zickermann, Volker; Angerer, Heike (2020-11-26). "Essential role of accessory subunit LYRM6 in the mechanism of mitochondrial complex I". Nature Communications. 11 (1): 6008. Bibcode:2020NatCo..11.6008G. doi:10.1038/s41467-020-19778-7. ISSN 2041-1723. PMC 7693276. PMID 33243981.
  21. ^ a b c d e Dwight, Trisha; Na, Un; Kim, Edward; Zhu, Ying; Richardson, Anne Louise; Robinson, Bruce G.; Tucker, Katherine M.; Gill, Anthony J.; Benn, Diana E.; Clifton-Bligh, Roderick J.; Winge, Dennis R. (December 2017). "Analysis of SDHAF3 in familial and sporadic pheochromocytoma and paraganglioma". BMC Cancer. 17 (1). doi:10.1186/s12885-017-3486-z. ISSN 1471-2407. PMC 5525311. PMID 28738844.
  22. ^ a b c d Maio, Nunziata; Ghezzi, Daniele; Verrigni, Daniela; Rizza, Teresa; Bertini, Enrico; Martinelli, Diego; Zeviani, Massimo; Singh, Anamika; Carrozzo, Rosalba; Rouault, Tracey A. (February 2016). "Disease-Causing SDHAF1 Mutations Impair Transfer of Fe-S Clusters to SDHB". Cell Metabolism. 23 (2): 292–302. doi:10.1016/j.cmet.2015.12.005. PMC 4749439. PMID 26749241.
  23. ^ Rouault, Tracey A.; Maio, Nunziata (August 2017). "Biogenesis and functions of mammalian iron-sulfur proteins in the regulation of iron homeostasis and pivotal metabolic pathways". Journal of Biological Chemistry. 292 (31): 12744–12753. doi:10.1074/jbc.R117.789537. PMC 5546015. PMID 28615439.
  24. ^ a b Dick, Danielle M.; Aliev, Fazil; Wang, Jen C.; Saccone, Scott; Hinrichs, Anthony; Bertelsen, Sarah; Budde, John; Saccone, Nancy; Foroud, Tatiana; Nurnberger, John; Xuei, Xiaoling; Conneally, P. M.; Schuckit, Marc; Almasy, Laura; Crowe, Raymond (2008-06-01). "A Systematic Single Nucleotide Polymorphism Screen to Fine-Map Alcohol Dependence Genes on Chromosome 7 Identifies Association With a Novel Susceptibility Gene ACN9". Biological Psychiatry. 63 (11): 1047–1053. doi:10.1016/j.biopsych.2007.11.005. ISSN 0006-3223. PMC 3823371. PMID 18163977.
  25. ^ a b Hempel, Maja; Kremer, Laura S.; Tsiakas, Konstantinos; Alhaddad, Bader; Haack, Tobias B.; Löbel, Ulrike; Feichtinger, René G.; Sperl, Wolfgang; Prokisch, Holger; Mayr, Johannes A.; Santer, René (November 2017). "LYRM7 - associated complex III deficiency: A clinical, molecular genetic, MR tomographic, and biochemical study". Mitochondrion. 37: 55–61. doi:10.1016/j.mito.2017.07.001. PMID 28694194.
  26. ^ a b c Sánchez, Ester; Lobo, Teresa; Fox, Jennifer L.; Zeviani, Massimo; Winge, Dennis R.; Fernández-Vizarra, Erika (2013-03-01). "LYRM7/MZM1L is a UQCRFS1 chaperone involved in the last steps of mitochondrial Complex III assembly in human cells". Biochimica et Biophysica Acta (BBA) - Bioenergetics. 1827 (3): 285–293. doi:10.1016/j.bbabio.2012.11.003. ISSN 0005-2728. PMC 3570683. PMID 23168492.
  27. ^ Cui, Tie-Zhong; Smith, Pamela M.; Fox, Jennifer L.; Khalimonchuk, Oleh; Winge, Dennis R. (2012-11-01). "Late-Stage Maturation of the Rieske Fe/S Protein: Mzm1 Stabilizes Rip1 but Does Not Facilitate Its Translocation by the AAA ATPase Bcs1". Molecular and Cellular Biology. 32 (21): 4400–4409. doi:10.1128/MCB.00441-12. ISSN 1098-5549. PMC 3486142. PMID 22927643.
  28. ^ Fernández-Vizarra, Erika; Zeviani, Massimo (2015-04-09). "Nuclear gene mutations as the cause of mitochondrial complex III deficiency". Frontiers in Genetics. 6. doi:10.3389/fgene.2015.00134. ISSN 1664-8021. PMC 4391031. PMID 25914718.
  29. ^ a b Lai, Yuezheng; Zhang, Yuying; Zhou, Shan; Xu, Jinxu; Du, Zhanqiang; Feng, Ziyan; Yu, Long; Zhao, Ziqing; Wang, Weiwei; Tang, Yanting; Yang, Xiuna; Guddat, Luke W.; Liu, Fengjiang; Gao, Yan; Rao, Zihe (June 2023). "Structure of the human ATP synthase". Molecular Cell. 83 (12): 2137–2147.e4. doi:10.1016/j.molcel.2023.04.029. PMID 37244256.
  30. ^ Lefebvre-Legendre, Linnka; Vaillier, Jacques; Benabdelhak, Houssain; Velours, Jean; Slonimski, Piotr P.; di Rago, Jean-Paul (March 2001). "Identification of a Nuclear Gene (FMC1) Required for the Assembly/Stability of Yeast Mitochondrial F1-ATPase in Heat Stress Conditions". Journal of Biological Chemistry. 276 (9): 6789–6796. doi:10.1074/jbc.M009557200. PMID 11096112.
  31. ^ a b Floyd, Brendan J.; Wilkerson, Emily M.; Veling, Mike T.; Minogue, Catie E.; Xia, Chuanwu; Beebe, Emily T.; Wrobel, Russell L.; Cho, Holly; Kremer, Laura S.; Alston, Charlotte L.; Gromek, Katarzyna A.; Dolan, Brendan K.; Ulbrich, Arne; Stefely, Jonathan A.; Bohl, Sarah L. (August 2016). "Mitochondrial Protein Interaction Mapping Identifies Regulators of Respiratory Chain Function". Molecular Cell. 63 (4): 621–632. doi:10.1016/j.molcel.2016.06.033. ISSN 1097-2765. PMC 4992456.
  32. ^ a b Roberts, David L.; Frerman, Frank E.; Kim, Jung-Ja P. (1996-12-10). "Three-dimensional structure of human electron transfer flavoprotein to 2.1-Å resolution". Proceedings of the National Academy of Sciences. 93 (25): 14355–14360. doi:10.1073/pnas.93.25.14355. ISSN 0027-8424. PMC 26136. PMID 8962055.
  33. ^ Hilander, Taru; Jackson, Christopher B.; Robciuc, Marius; Bashir, Tanzeela; Zhao, Hongxia (2021-09-01). "The roles of assembly factors in mammalian mitoribosome biogenesis". Mitochondrion. 60: 70–84. doi:10.1016/j.mito.2021.07.008. ISSN 1567-7249. PMID 34339868.
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