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LYRM protein

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Leu-Tyr-Arg motif-containing proteins (LYRMs) form a superfamily of small (<15kDa), positively charged and predominantly mitochondrial proteins with an N-terminal leucine–tyrosine–arginine motif.[1][2][3][4] However, the presence of this L–Y–R motif is not strictly required for LYRM classification, as membership is based on broader structural and functional criteria.[1][3] LYRMs play key roles in essential mitochondrial processes, including oxidative phosphorylation (OXPHOS), mitochondrial translation, iron–sulfur (Fe–S) cluster assembly, or also in acetate metabolism.[1][3] Their function is allosterically activated by acylated acyl carrier protein (acyl-ACP) provided by the mitochondrial fatty acid synthesis (mtFAS) pathway, in response to mitochondrial acetyl-CoA availability.[5] This mode of activation enables them to function as late-stage electron transport chain (ETC) assembly factors.[5]

Risk of confusion with LYR proteins

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To avoid confusion, it is important to note that the term “LYR proteins” has occasionally been used to describe mitochondrial proteins that contain the LYR sequence but do not share the defining structural or functional features of true LYRM family members.[3] An LYR tripeptide alone is insufficient for LYRM classification; proteins such as NDUFAF3, certain subunits of respiratory complexes II (e.g. SDHB), IV, and V, and several mitochondrial ribosomal proteins contain the motif but are not members of the LYRM superfamily.[3]

Occurrence and synthesis

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LYRMs are found exclusively in eukaryotes, but they differ between species.[1] While anaerobic eukaryotes have only LYRM4 or no LYRM proteins at all, twelve members have been characterized in humans.[1] With the exception of LYRM3 and LYRM6, which are embedded within mitochondrial Complex I, LYRM proteins are soluble matrix-located proteins.[6] 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.[3]

Structure

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LYRM proteins were classified based on LYRM4, which stabilizes the cysteine desulfurase NFS1 within the mitochondrial iron–sulfur cluster (ISC) assembly machinery.[4] A characteristic feature of LYRM proteins is their three-helix bundle fold.[7] In this antiparallel arrangement, helix α1 is tilted forward by approximately 20°, while helices α2 and α3 run parallel to each other. The LYR motif is located on helix α1, just behind its N-terminal start, and can be followed by an isoleucine or leucine and a phenylalanine.[4] Together, these helices create a hydrophobic tunnel in the interior that serves as a binding site for the acyl chain of acyl–ACP, which is linked via a 4’-phosphopantetheine group covalently attached to ACP.[1][5] Effective binding to LYRM proteins typically requires an acyl chain of about 10-16 carbons in length.[8] However, ACP is not dependent on acylation to bind to LYRM proteins, even though they have a higher affinity for acyl-ACP than for unacylated ACP (holo-ACP).[5]

FMC1 represents an exception, as it does not form a hydrophobic tunnel and generally behaves atypical behavior compared to other LYRM proteins.[1][5]

Function

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Iron–sulfur cluster biogensis

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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.[9] They are assembled on the ISCU scaffold protein, with iron donated by frataxin and sulfur provided by the NFS1–LYRM4 complex.[8] This complex binds acyl-ACP via LYRM4, and this interaction stabilizes the otherwise degradation-prone complex.[8] 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.[8]

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

Mitoribosome assembly

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The LYRM protein L0R8F8 and ACP function as assembly factors for the human mitoribosome.[10] 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.[11] In the late stages of human mitoribosome large subunit (mt-LSU) maturation, a complex composed of MALSU1, L0R8F8, and ACP associates with the mt-LSU.[10] This complex sterically prevents premature association with the small subunit (mt-SSU), thereby regulating the timing of mitoribosome subunit joining.[10] Structural analyses have shown that the interaction between L0R8F8 and ACP is mediated by the LYR motif of L0R8F8 and the 4′-phosphopantetheine moiety of ACP.[10] Notably, in this context, ACP is found in its unacylated form holo-ACP, and no acyl chain density is observed in the structural data.[10][12]

Electron transfer flavoprotein assembly

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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.[13] 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.[14] 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.[14] ETF:QO is thereby reduced and passes the electrons to ubiquinone (CoQ10) in the respiratory chain.[13] Unlike other LYRM family members, LYRM5 lacks the characteristic leucine–tyrosine–arginine motif and instead contains a leucine–tyrosine–lysine motif.[1]

Oxidative phosphorylation complex assembly

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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.[6]

NADH:ubiquinone oxidoreductase (Complex I)

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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.[15] Under certain conditions, the reaction can reverse, resulting in the reduction of NAD+.[15]

LYRM3 is an integral accessory subunit of Complex I, positioned in the distal proton-translocating module PD of the membrane arm.[6] It forms a stable heterodimer with the neighboring subunit SDAP1, an isoform of the mitochondrial ACP encoded by the gene NDUFAB1.[6] This interaction, mediated by LYR domain of LYRM3, plays a crucial role in the function and assembly of Complex I.[6]

LYRM6 is also an integral accessory subunit of Complex I.[16] 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 mitochondrial ACP.[16] Two adjacent loops of LYRM6 interact directly with central subunits of Complex I, helping stabilize this interface.[16] 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.[16]

LYRM2 is located in mitochondria, directly interacts with Complex I and increases its activity.[17]

Succinate dehydrogenase (Complex II)

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LYRM8 and ACN9 are required for the assembly of the Fe–S cluster–containing subunit SDHB in Complex II.[3] As part of the citric acid cycle, Complex II couples the oxidation of succinate to fumarate to the reduction of ubiquinone.[18] The functions of LYRM8 and ACN9 involve interactions with acyl-ACP.[19]

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.[20] 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.[20][21][18] However, SDHB is not one of the LYRM proteins.[3] 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.[20] 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.[20]

ACN9 functions as an assembly factor involved in the maturation of Complex II.[18] Specifically, it contributes to the incorporation of iron–sulfur (Fe–S) clusters into the SDHB subunit, which is essential for Complex II activity.[18] However, its exact molecular role remains to be fully defined.[18] Yeast data indicate that ACN9 plays a role in gluconeogenesis and in converting ethanol or acetate into carbohydrates.[22]

Coenzyme Q : cytochrome c – oxidoreductase (Complex III)

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LYRM7 functions as an assembly factor for Complex III, acting as a chaperone for the Rieske iron-sulfur protein.[23] 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).[24] 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.[24] 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.[23] This prevents the Rieske iron-sulfur protein from proteolytic degradation or temperature‑induced aggregation.[25] 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.[26][24]

ATP synthase (Complex V)

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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.[27] 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.[27] 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.[28] Although FMC1 belongs to the LYRM protein family, it lacks key residues of the LYRM motif, including leucine and phenylalanine, and cannot bind acylated ACP due to the missing hydrophobic tunnel.[1] Nevertheless, it interacts with non-acylated ACP, 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]

Regulation

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While the network of LYRM proteins can bind with unacylated ACP (holo-ACP), they are only allosterically activated upon binding to the acylated form (acyl-ACP), to which they exhibit a higher affinity.[5][29] Only upon this activation can they functionally interact with specific target proteins.[5][29] ACP acylation is driven by the mitochondrial fatty acid synthesis (mtFAS) pathway in response to mitochondrial acetyl-CoA availability and is sensitive to perturbations in acetyl-CoA synthesis.[5][29] When acyl-ACP levels are limited, the following prioritization is observed: mitochondrial translation is maintained, lipoic acid biosynthesis is reduced, and activation of LYRM proteins for ETC complex assembly is halted, establishing them as late-stage ETC assembly factors.[5][29] ACP and mtFAS thus coordinate the activation of mitochondrial respiration in response to substrate availability.[5][29] This enables the cells to increase their oxidative capacity when there is an excess of substrate and prevents the electron transport chain from running empty and subsequent formation of reactive oxygen species when there is a lack of substrate.[29][19]

Overview of members

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At least 12 LYRM proteins have been identified in humans (2019):[19]

LYRM protein LYR motif Target location Function Interaction partner
LYRM1[19] LYR Insulin signaling[19] Acyl-ACP[19]
LYRM2[19] LYR Complex I Associates with Complex I activity[19] Acyl-ACP[19]
LYRM3/NDUFB9[19] LYR Complex I Structual subunit[19] Acyl-ACP[19]
LYRM4/ISD11[19] LYR Cysteine desulfurase NFS1 Assembly factor Acyl-ACP,[19] NFS1[3]
LYRM5[19] LYK Electron transfer flavoprotein (ETF) Accessory factor Acyl-ACP[19]
LYRM6/NDUFA6[19] Complex I Structual subunit[19] Acyl-ACP,[19] NDUFS3[3]
LYRM7/MZM1L[19] AYR or other Complex III Assembly factor[17] Acyl-ACP,[19] UQCRFS1, HSC20[3]
LYRM8/SDHAF1[19] IYR & LYR Complex II Assembly factor[19] Acyl-ACP,[19] SDHB, HSC20[3]
LYRM9/C17orf108[19] Unknown[19] Unkown[19]
ACN9/SDHAF3/[19] LYRM10[30] Complex II Assembly factor[19] Acyl-ACP,[19] SDHB[3]
FMC1/C7orf55[19] no LYR motif Complex V Assembly factor[3] Acyl-ACP,[19] ATP12[3]
L0R8F8[19] Mitoribosome Assembly factor[10] Holo-ACP[19]

Clinical significance

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

References

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  2. ^ 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.
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  29. ^ a b c d e f 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.
  30. ^ "SDHAF3 succinate dehydrogenase complex assembly factor 3 [Homo sapiens (human)] - Gene - NCBI". www.ncbi.nlm.nih.gov. Retrieved 2025-05-26.
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