Invited Talk 21st International Conference on Biological Inorganic Chemistry 2025

The function of Mak16 in ribosome biogenesis depends on its [4Fe-4S] cluster (122167)

Nadine Duppe 1 , Marc Hageboelling 1 , Martin Stuempfig 2 , Larissa Heimann 3 , Volker Schuenemann 3 , Antonio J. Pierik 1 , Daili J. Netz 1
  1. Dept. of Chemistry, RPTU University Kaiserslautern-Landau, Kaiserslautern, Germany
  2. Inst. für Zytobiologie & Zytopathologie and Synmikro, Philipps University, Marburg, Germany
  3. Dept. of Physics, RPTU University Kaiserslautern-Landau, Kaiserslautern, Germany

Mak16 and its interacting partner Rpf1 play a critical role at an early step in the maturation of the ribosomal 60S subunit, as revealed by recent cryo-EM structures.1 While most studies suggested no metal participation or the presence of a Zn2+ ion in Mak16, we identify a bona fide Fe/S cluster in yeast Mak16 through both in vivo and in vitro methods. We demonstrate a functional link between the mitochondrial and cytosolic Fe/S protein biogenesis and ribosome assembly, highlighting a previously unexplored aspect of 60S ribosomal biogenesis. Interestingly, 17 % of all Mak16 proteins, including those from pathogens like Trypanosoma and Leishmania, have a C-terminal tryptophan residue as likely CIA targetting complex motif.2 Characterization of human and yeast Mak16 by EPR and Mössbauer spectroscopy revealed a redox-active [4Fe-4S]2+/1+ cluster with a midpoint potential below -450 mV. Yeast cells in which the endogenous Mak16 is substituted by its Fe/S-deficient C38A variant exhibited heightened sensitivity to redox stressors, including DTT, H₂O₂, and menadione. Our findings also reveal that upon binding to rRNA expansion segment 7a (ES7a) the redox properties of the nearby Fe/S cluster largely remain unchanged. However, disruption of Fe/S cluster coordination destabilized Mak16, impaired the Mak16-Rpf1 complex formation and decreased the 25S rRNA level. The critical role of Fe/S proteins in eukaryotic DNA replication and repair—through their involvement in DNA polymerases, primase, helicases, and glycosylase—has now been extended to ribosomal assembly. However, relying on such a vulnerable cofactor comes at a cost, as cluster loss can severely disrupt essential cellular processes. The inherent biosynthetic complexity and instability of Fe/S clusters allows a function as sensor for redox imbalance, creating new possibilities for Fe/S proteins to regulate cellular homeostasis.

  1. Kater, L.; Thoms, M.; Barrio-Garcia, C.; Cheng, J.; Ismail, S.; Luqman Ahmed, Y.; Bange, G.; Kressler, D.; Berninghausen, O.; Sinning, I.; Hurt, E.; Beckmann, R. Cell, 2017, 171, 1599-1610.
  2. Marquez, M.D.; Greth, C.; Buzuk, A.; Liu, X.; Blinn, C.M.; Beller, S.; Leiskau, L.; Hushka, A.; Wu, K.; Nur, K.; Netz, D.J.A.; Perlstein, D.L.; Pierik, A.J. Proc. Natl. Acad. Sci. USA, 2023, 120, e2311057120.