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AIFM2
Protein-coding gene in the species Homo sapiens

Apoptosis-inducing factor 2 (AIFM2), also called ferroptosis suppressor protein 1 (FSP1) or AMID, is a protein encoded by the AIFM2 gene on chromosome 10, also known as p53-responsive gene 3 (PRG3). This gene produces a flavoprotein oxidoreductase enzyme that plays a key role in cellular processes by reducing antioxidants such as coenzyme Q10, vitamin E, and vitamin K, thereby helping to regulate cell death mechanisms like apoptosis and ferroptosis.

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Function

The AIFM2 gene encodes the FSP1 protein encoded by this gene has significant homology to NADH oxidoreductases and the apoptosis-inducing factor PDCD8/AIF. Although it was originally proposed that this protein induce apoptosis due to its similarity with AIF, findings from James Olzmann's group at UC Berkeley 7 and Marcus Conrad's group at the Helmholtz Institute 8 demonstrated that the primary cellular function of FSP1 is to suppress lipid peroxidation and the induction of the regulated, non-apoptotic cell death pathway known as ferroptosis. Mechanistically, FSP1 reduces oxidized coenzyme Q10 (i.e., ubiquinone) to its reduced form (i.e., ubiquinol), which functions as an excellent lipophilic antioxidant to prevent the propagation of lipid peroxidation.910 FSP1 also may act through the reduction of other molecules, such as vitamin E and vitamin K.

Structure

AIFM2 can be found only both in prokaryotes and eukaryotes.11121314 Sequence analysis reveals that the AIFM2 gene promoter contains a consensus transcription initiator sequence instead of a TATA box.15 Though AIFM2 also lacks a recognizable mitochondrial localization sequence and cannot enter the mitochondria, it is found to adhere to the outer mitochondrial membrane (OMM), where it forms a ring-like structure.1617181920 Two deletion mutations at the N-terminal (aa 1–185 and 1–300) result in nuclear localization and failure to effect cell death, suggesting that AIFM2 must be associated with the mitochondria in order to induce apoptosis. Moreover, domain mapping experiments reveal that only the C-terminal 187 aa is required for apoptotic induction.21 Meanwhile, mutations in the N-terminal putative FAD- and ADP-binding domains, which are responsible for its oxidoreductase function, do not affect its apoptotic function, thus indicating that these two functions operate independently.2223 It assembles stoichiometrically and noncovalently with 6-hydroxy-FAD.24

The AIFM2 gene contains a putative p53-binding element in intron 5, suggesting that its gene expression can be activated by p53.252627

Function

This protein is a flavoprotein that functions as an NAD(P)H-dependent oxidoreductase and induces caspase- and p53-independent apoptosis.282930 The exact mechanisms remain unknown, but AIFM2 is found to localize to the cytosol and the OMM. Thus, it may carry out this function by disrupting mitochondrial morphology and releasing proapoptotic factors.31 Also, under conditions of stress which activate p53-mediated apoptosis, such as hypoxia, AIMF2 may stabilize p53 by inhibiting its degradation and accelerate the apoptotic process. Under normal conditions (i.e., undetectable p53 expression), the AIFM2 gene is highly expressed in the heart, followed by liver and skeletal muscle, with low levels detected in the placenta, lung, kidney, and pancreas and the lowest in the brain. However, in organs such as the heart, there may be additional regulatory mechanisms to suppress its proapoptotic function.32 For instance, AIFM2 may be able to directly bind nuclear DNA and effect chromatin condensation, as with AIF.33 Furthermore, AIMF2 expressed at low levels may function as an oxidoreductase involved in metabolism.34 Hence, under normal cellular conditions, AIFM2 may promote cell survival rather than death by metabolic processes such as generating reactive oxygen species (ROS) to maintain survival signaling.35

Clinical significance

AIFM2 has been implicated in tumorigenesis as a p53-inducible gene.36 AIFM2 mRNA levels are observed to be downregulated in many human cancer tissues, though a previous study reported that AIFM2 mRNA transcripts were only detected in colon cancer and B-cell lymphoma cell lines.3738 Furthermore, its DNA-binding ability contributes to its involvement in the apoptosis-inducing response to viral and bacterial infections, possibly through its role in ROS regulation.39

Inhibitors4041 of FSP1 have been identified to induce ferroptosis. icFSP1 has been shown to cause dissociation of FSP1 from the membrane and phase separation of FSP1 into droplets.

Evolution

The phylogenetic studies indicates that the divergence of the AIFM1 and other AIFs occurred before the divergence of eukaryotes.42

Interactions

AIFM2 is shown to interact with p53.43

AIFM2 is not inhibited by Bcl-2.44

AIFM2 can also bind the following coenzymes:

Further reading

References

  1. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  2. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  3. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  4. "Entrez Gene: AIFM2 apoptosis-inducing factor, mitochondrion-associated, 2". https://www.ncbi.nlm.nih.gov/sites/entrez?Db=gene&Cmd=ShowDetailView&TermToSearch=84883 ↩

  5. Doll S, Freitas FP, Shah R, Aldrovandi M, da Silva MC, Ingold I, et al. (November 2019). "FSP1 is a glutathione-independent ferroptosis suppressor". Nature. 575 (7784): 693–698. Bibcode:2019Natur.575..693D. doi:10.1038/s41586-019-1707-0. hdl:10044/1/75345. PMID 31634899. S2CID 204833583. https://orca.cardiff.ac.uk/id/eprint/126674/ ↩

  6. Bersuker K, Hendricks JM, Li Z, Magtanong L, Ford B, Tang PH, et al. (November 2019). "The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis". Nature. 575 (7784): 688–692. Bibcode:2019Natur.575..688B. doi:10.1038/s41586-019-1705-2. PMC 6883167. PMID 31634900. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6883167 ↩

  7. Bersuker K, Hendricks JM, Li Z, Magtanong L, Ford B, Tang PH, et al. (November 2019). "The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis". Nature. 575 (7784): 688–692. Bibcode:2019Natur.575..688B. doi:10.1038/s41586-019-1705-2. PMC 6883167. PMID 31634900. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6883167 ↩

  8. Doll S, Freitas FP, Shah R, Aldrovandi M, da Silva MC, Ingold I, et al. (November 2019). "FSP1 is a glutathione-independent ferroptosis suppressor". Nature. 575 (7784): 693–698. Bibcode:2019Natur.575..693D. doi:10.1038/s41586-019-1707-0. hdl:10044/1/75345. PMID 31634899. S2CID 204833583. https://orca.cardiff.ac.uk/id/eprint/126674/ ↩

  9. Doll S, Freitas FP, Shah R, Aldrovandi M, da Silva MC, Ingold I, et al. (November 2019). "FSP1 is a glutathione-independent ferroptosis suppressor". Nature. 575 (7784): 693–698. Bibcode:2019Natur.575..693D. doi:10.1038/s41586-019-1707-0. hdl:10044/1/75345. PMID 31634899. S2CID 204833583. https://orca.cardiff.ac.uk/id/eprint/126674/ ↩

  10. Bersuker K, Hendricks JM, Li Z, Magtanong L, Ford B, Tang PH, et al. (November 2019). "The CoQ oxidoreductase FSP1 acts parallel to GPX4 to inhibit ferroptosis". Nature. 575 (7784): 688–692. Bibcode:2019Natur.575..688B. doi:10.1038/s41586-019-1705-2. PMC 6883167. PMID 31634900. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6883167 ↩

  11. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  12. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  13. Klim J, Gładki A, Kucharczyk R, Zielenkiewicz U, Kaczanowski S (May 2018). "Ancestral State Reconstruction of the Apoptosis Machinery in the Common Ancestor of Eukaryotes". G3. 8 (6): 2121–2134. doi:10.1534/g3.118.200295. PMC 5982838. PMID 29703784. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5982838 ↩

  14. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  15. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  16. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  17. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  18. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  19. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  20. Gong M, Hay S, Marshall KR, Munro AW, Scrutton NS (October 2007). "DNA binding suppresses human AIF-M2 activity and provides a connection between redox chemistry, reactive oxygen species, and apoptosis". The Journal of Biological Chemistry. 282 (41): 30331–40. doi:10.1074/jbc.m703713200. PMID 17711848. https://doi.org/10.1074%2Fjbc.m703713200 ↩

  21. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  22. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  23. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  24. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  25. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  26. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  27. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  28. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  29. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  30. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  31. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  32. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  33. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  34. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  35. Gong M, Hay S, Marshall KR, Munro AW, Scrutton NS (October 2007). "DNA binding suppresses human AIF-M2 activity and provides a connection between redox chemistry, reactive oxygen species, and apoptosis". The Journal of Biological Chemistry. 282 (41): 30331–40. doi:10.1074/jbc.m703713200. PMID 17711848. https://doi.org/10.1074%2Fjbc.m703713200 ↩

  36. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  37. Wu M, Xu LG, Li X, Zhai Z, Shu HB (July 2002). "AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis". The Journal of Biological Chemistry. 277 (28): 25617–23. doi:10.1074/jbc.M202285200. PMID 11980907. https://doi.org/10.1074%2Fjbc.M202285200 ↩

  38. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  39. Wu M, Xu LG, Su T, Tian Y, Zhai Z, Shu HB (September 2004). "AMID is a p53-inducible gene downregulated in tumors". Oncogene. 23 (40): 6815–9. doi:10.1038/sj.onc.1207909. PMID 15273740. S2CID 8541615. /wiki/Doi_(identifier) ↩

  40. Doll S, Freitas FP, Shah R, Aldrovandi M, da Silva MC, Ingold I, et al. (November 2019). "FSP1 is a glutathione-independent ferroptosis suppressor". Nature. 575 (7784): 693–698. Bibcode:2019Natur.575..693D. doi:10.1038/s41586-019-1707-0. hdl:10044/1/75345. PMID 31634899. S2CID 204833583. https://orca.cardiff.ac.uk/id/eprint/126674/ ↩

  41. Nakamura T, Hipp C, Santos Dias Mourão A, Borggräfe J, Aldrovandi M, Henkelmann B, Wanninger J, Mishima E, Lytton E, Emler D, Proneth B, Sattler M, Conrad M (July 2023). "Phase separation of FSP1 promotes ferroptosis". Nature. 619 (7969): 371–377. Bibcode:2023Natur.619..371N. doi:10.1038/s41586-023-06255-6. ISSN 1476-4687. PMC 10338336. PMID 37380771. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10338336 ↩

  42. Klim J, Gładki A, Kucharczyk R, Zielenkiewicz U, Kaczanowski S (May 2018). "Ancestral State Reconstruction of the Apoptosis Machinery in the Common Ancestor of Eukaryotes". G3. 8 (6): 2121–2134. doi:10.1534/g3.118.200295. PMC 5982838. PMID 29703784. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5982838 ↩

  43. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  44. Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N, Horikoshi N (July 2002). "A novel p53-inducible apoptogenic gene, PRG3, encodes a homologue of the apoptosis-inducing factor (AIF)". FEBS Letters. 524 (1–3): 163–71. Bibcode:2002FEBSL.524..163O. doi:10.1016/S0014-5793(02)03049-1. PMID 12135761. S2CID 6972218. https://doi.org/10.1016%2FS0014-5793%2802%2903049-1 ↩

  45. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  46. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  47. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  48. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩

  49. Marshall KR, Gong M, Wodke L, Lamb JH, Jones DJ, Farmer PB, Scrutton NS, Munro AW (September 2005). "The human apoptosis-inducing protein AMID is an oxidoreductase with a modified flavin cofactor and DNA binding activity". The Journal of Biological Chemistry. 280 (35): 30735–40. doi:10.1074/jbc.M414018200. PMID 15958387. https://doi.org/10.1074%2Fjbc.M414018200 ↩