Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10
Abstract
The inner boundary and the cristae membrane are connected by pore-like structures termed crista junctions (CJs). The MICOS complex is required for CJ formation and enriched at CJs. Here, we address the roles of the MICOS subunits Mic27 and Mic10. We observe a positive genetic interaction between Mic27 and Mic60 and deletion of Mic27 results in impaired formation of CJs and altered cristae membrane curvature. Mic27 acts in an antagonistic manner to Mic60 as it promotes oligomerization of the F1FO-ATP synthase and partially restores CJ formation in cells lacking Mic60. Mic10 impairs oligomerization of the F1FO-ATP synthase similar to Mic60. Applying complexome profiling, we observed that deletion of Mic27 destabilizes the MICOS complex but does not impair formation of a high molecular weight Mic10 subcomplex. Moreover, this Mic10 subcomplex comigrates with the dimeric F1FO-ATP synthase in a Mic27-independent manner. Further, we observed a chemical crosslink of Mic10 to Mic27 and of Mic10 to the F1FO-ATP synthase subunit e. We corroborate the physical interaction of the MICOS complex and the F1FO-ATP synthase. We propose a model in which part of the F1FO-ATP synthase is linked to the MICOS complex via Mic10 and Mic27 and by that is regulating CJ formation.
- Authors:
-
- Goethe University, Frankfurt (Germany)
- Max Planck Inst. of Biophysics, Frankfurt am Main (Germany); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Heinrich Heine University, Dusseldorf (Germany)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division: German Research Foundation (DFG); Max Planck Society
- OSTI Identifier:
- 1629532
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbial Cell
- Additional Journal Information:
- Journal Volume: 4; Journal Issue: 8; Journal ID: ISSN 2311-2638
- Publisher:
- Shared Science Publishers OG
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; membrane structure; bioenergetics; mitochondria; cristae; membrane protein complex; crista junction
Citation Formats
Eydt, Katharina, Davis, Karen M., Behrendt, Christina, Wittig, Ilka, and Reichert, Andreas S. Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10. United States: N. p., 2017.
Web. doi:10.15698/mic2017.08.585.
Eydt, Katharina, Davis, Karen M., Behrendt, Christina, Wittig, Ilka, & Reichert, Andreas S. Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10. United States. https://doi.org/10.15698/mic2017.08.585
Eydt, Katharina, Davis, Karen M., Behrendt, Christina, Wittig, Ilka, and Reichert, Andreas S. Mon .
"Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10". United States. https://doi.org/10.15698/mic2017.08.585. https://www.osti.gov/servlets/purl/1629532.
@article{osti_1629532,
title = {Cristae architecture is determined by an interplay of the MICOS complex and the F1Fo ATP synthase via Mic27 and Mic10},
author = {Eydt, Katharina and Davis, Karen M. and Behrendt, Christina and Wittig, Ilka and Reichert, Andreas S.},
abstractNote = {The inner boundary and the cristae membrane are connected by pore-like structures termed crista junctions (CJs). The MICOS complex is required for CJ formation and enriched at CJs. Here, we address the roles of the MICOS subunits Mic27 and Mic10. We observe a positive genetic interaction between Mic27 and Mic60 and deletion of Mic27 results in impaired formation of CJs and altered cristae membrane curvature. Mic27 acts in an antagonistic manner to Mic60 as it promotes oligomerization of the F1FO-ATP synthase and partially restores CJ formation in cells lacking Mic60. Mic10 impairs oligomerization of the F1FO-ATP synthase similar to Mic60. Applying complexome profiling, we observed that deletion of Mic27 destabilizes the MICOS complex but does not impair formation of a high molecular weight Mic10 subcomplex. Moreover, this Mic10 subcomplex comigrates with the dimeric F1FO-ATP synthase in a Mic27-independent manner. Further, we observed a chemical crosslink of Mic10 to Mic27 and of Mic10 to the F1FO-ATP synthase subunit e. We corroborate the physical interaction of the MICOS complex and the F1FO-ATP synthase. We propose a model in which part of the F1FO-ATP synthase is linked to the MICOS complex via Mic10 and Mic27 and by that is regulating CJ formation.},
doi = {10.15698/mic2017.08.585},
journal = {Microbial Cell},
number = 8,
volume = 4,
place = {United States},
year = {Mon Aug 07 00:00:00 EDT 2017},
month = {Mon Aug 07 00:00:00 EDT 2017}
}
Works referenced in this record:
OPA1 functionally interacts with MIC60 but is dispensable for crista junction formation
journal, September 2016
- Barrera, Miguel; Koob, Sebastian; Dikov, Daniel
- FEBS Letters, Vol. 590, Issue 19
Mitochondrial myopathies
journal, June 1985
- DiMauro, Salvatore; Bonilla, Eduardo; Zeviani, Massimo
- Annals of Neurology, Vol. 17, Issue 6
Quantification of muscle mitochondrial oxidative phosphorylation enzymesvia histochemical staining of blue native polyacrylamide gels
journal, January 1997
- Zerbetto, Elisabetta; Vergani, Lodovica; Dabbeni-Sala, Federica
- Electrophoresis, Vol. 18, Issue 11
The internal compartmentation of rat-liver mitochondria: Tomographic study using the high-voltage transmission electron microscope
journal, March 1994
- Mannella, Carmen A.; Marko, Michael; Penczek, Pawel
- Microscopy Research and Technique, Vol. 27, Issue 4
Advantages and limitations of clear-native PAGE
journal, October 2005
- Wittig, Ilka; Schägger, Hermann
- PROTEOMICS, Vol. 5, Issue 17
Electron Tomography of Neuronal Mitochondria: Three-Dimensional Structure and Organization of Cristae and Membrane Contacts
journal, August 1997
- Perkins, G.; Renken, C.; Martone, M. E.
- Journal of Structural Biology, Vol. 119, Issue 3
The relevance of mitochondrial membrane topology to mitochondrial function
journal, February 2006
- Mannella, Carmen A.
- Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1762, Issue 2
Cristae formation—linking ultrastructure and function of mitochondria
journal, January 2009
- Zick, Michael; Rabl, Regina; Reichert, Andreas S.
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1793, Issue 1
The non-glycosylated isoform of MIC26 is a constituent of the mammalian MICOS complex and promotes formation of crista junctions
journal, July 2015
- Koob, Sebastian; Barrera, Miguel; Anand, Ruchika
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1853, Issue 7
Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex
journal, January 2016
- Huynen, Martijn A.; Mühlmeister, Mareike; Gotthardt, Katherina
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1863, Issue 1
Role of the mitochondrial contact site and cristae organizing system in membrane architecture and dynamics
journal, April 2017
- Rampelt, Heike; Zerbes, Ralf M.; van der Laan, Martin
- Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1864, Issue 4
Mitochondrial Rhomboid PARL Regulates Cytochrome c Release during Apoptosis via OPA1-Dependent Cristae Remodeling
journal, July 2006
- Cipolat, Sara; Rudka, Tomasz; Hartmann, Dieter
- Cell, Vol. 126, Issue 1
OPA1 Controls Apoptotic Cristae Remodeling Independently from Mitochondrial Fusion
journal, July 2006
- Frezza, Christian; Cipolat, Sara; Martins de Brito, Olga
- Cell, Vol. 126, Issue 1
Complexome Profiling Identifies TMEM126B as a Component of the Mitochondrial Complex I Assembly Complex
journal, October 2012
- Heide, Heinrich; Bleier, Lea; Steger, Mirco
- Cell Metabolism, Vol. 16, Issue 4
Mic10 Oligomerizes to Bend Mitochondrial Inner Membranes at Cristae Junctions
journal, May 2015
- Barbot, Mariam; Jans, Daniel C.; Schulz, Christian
- Cell Metabolism, Vol. 21, Issue 5
Central Role of Mic10 in the Mitochondrial Contact Site and Cristae Organizing System
journal, May 2015
- Bohnert, Maria; Zerbes, Ralf M.; Davies, Karen M.
- Cell Metabolism, Vol. 21, Issue 5
Ancient Homology of the Mitochondrial Contact Site and Cristae Organizing System Points to an Endosymbiotic Origin of Mitochondrial Cristae
journal, June 2015
- Muñoz-Gómez, Sergio A.; Slamovits, Claudio H.; Dacks, Joel B.
- Current Biology, Vol. 25, Issue 11
Dual Role of Mitofilin in Mitochondrial Membrane Organization and Protein Biogenesis
journal, October 2011
- von der Malsburg, Karina; Müller, Judith M.; Bohnert, Maria
- Developmental Cell, Vol. 21, Issue 4
Data supporting the role of the non-glycosylated isoform of MIC26 in determining cristae morphology
journal, September 2015
- Koob, Sebastian; Barrera, Miguel; Anand, Ruchika
- Data in Brief, Vol. 4
Differential protein distributions define two sub-compartments of the mitochondrial inner membrane in yeast
journal, September 2006
- Wurm, Christian A.; Jakobs, Stefan
- FEBS Letters, Vol. 580, Issue 24
The mitochondrial inner membrane protein Mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled-coil-helix coiled-coil-helix domain-containing protein 3 and 6 and DnaJC11
journal, June 2007
- Xie, Jing; Marusich, Michael F.; Souda, Puneet
- FEBS Letters, Vol. 581, Issue 18
Distinct Roles of Mic12 and Mic27 in the Mitochondrial Contact Site and Cristae Organizing System
journal, April 2016
- Zerbes, Ralf M.; Höß, Philipp; Pfanner, Nikolaus
- Journal of Molecular Biology, Vol. 428, Issue 8
Mic10, a Core Subunit of the Mitochondrial Contact Site and Cristae Organizing System, Interacts with the Dimeric F 1 F o -ATP Synthase
journal, April 2017
- Rampelt, Heike; Bohnert, Maria; Zerbes, Ralf M.
- Journal of Molecular Biology, Vol. 429, Issue 8
Role of MINOS in mitochondrial membrane architecture and biogenesis
journal, April 2012
- van der Laan, Martin; Bohnert, Maria; Wiedemann, Nils
- Trends in Cell Biology, Vol. 22, Issue 4
The cristal membrane of mitochondria is the principal site of oxidative phosphorylation
journal, June 2003
- Gilkerson, Robert W.; Selker, Jeanne M. L.; Capaldi, Roderick A.
- FEBS Letters, Vol. 546, Issue 2-3
The internal structure of mitochondria
journal, July 2000
- Frey, Terrence G.; Mannella, Carmen A.
- Trends in Biochemical Sciences, Vol. 25, Issue 7
A thermodynamic model describing the nature of the crista junction: a structural motif in the mitochondrion
journal, April 2002
- Renken, Christian; Siragusa, Gino; Perkins, Guy
- Journal of Structural Biology, Vol. 138, Issue 1-2
A Distinct Pathway Remodels Mitochondrial Cristae and Mobilizes Cytochrome c during Apoptosis
journal, January 2002
- Scorrano, Luca; Ashiya, Mona; Buttle, Karolyn
- Developmental Cell, Vol. 2, Issue 1
Dimer ribbons of ATP synthase shape the inner mitochondrial membrane
journal, March 2008
- Strauss, Mike; Hofhaus, Götz; Schröder, Rasmus R.
- The EMBO Journal, Vol. 27, Issue 7
The mitochondrial contact site complex, a determinant of mitochondrial architecture: Molecular architecture of mitochondria
journal, October 2011
- Harner, Max; Körner, Christian; Walther, Dirk
- The EMBO Journal, Vol. 30, Issue 21
Blue native PAGE
journal, June 2006
- Wittig, Ilka; Braun, Hans-Peter; Schägger, Hermann
- Nature Protocols, Vol. 1, Issue 1
Hepatitis C virus enhances Rubicon expression, leading to autophagy inhibition and intracellular innate immune activation
journal, September 2020
- Shiode, Yuto; Hikita, Hayato; Tanaka, Satoshi
- Scientific Reports, Vol. 10, Issue 1
Disrupted-in-schizophrenia
1 (DISC1) plays essential roles in mitochondria in collaboration with Mitofilin
journal, September 2010
- Park, Young-Un; Jeong, Jaehoon; Lee, Haeryun
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 41
Macromolecular organization of ATP synthase and complex I in whole mitochondria
journal, August 2011
- Davies, K. M.; Strauss, M.; Daum, B.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 34
Structure of the yeast F1Fo-ATP synthase dimer and its role in shaping the mitochondrial cristae
journal, August 2012
- Davies, K. M.; Anselmi, C.; Wittig, I.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 34
ChChd3, an Inner Mitochondrial Membrane Protein, Is Essential for Maintaining Crista Integrity and Mitochondrial Function
journal, January 2011
- Darshi, Manjula; Mendiola, Vincent L.; Mackey, Mason R.
- Journal of Biological Chemistry, Vol. 286, Issue 4
CHCM1/CHCHD6, Novel Mitochondrial Protein Linked to Regulation of Mitofilin and Mitochondrial Cristae Morphology
journal, March 2012
- An, Jie; Shi, Jingxue; He, Qin
- Journal of Biological Chemistry, Vol. 287, Issue 10
In the Absence of the First Membrane-spanning Segment of Subunit4(b), the Yeast ATP Synthase Is Functional but Does Not Dimerize or Oligomerize
journal, March 2002
- Soubannier, Vincent; Vaillier, Jacques; Paumard, Patrick
- Journal of Biological Chemistry, Vol. 277, Issue 12
Su e of the Yeast F1Fo-ATP Synthase Forms Homodimers
journal, December 2002
- Brunner, Susanne; Everard-Gigot, Valerie; Stuart, Rosemary A.
- Journal of Biological Chemistry, Vol. 277, Issue 50
Mitochondrial Membrane Potential Is Dependent on the Oligomeric State of F1F0-ATP Synthase Supracomplexes
journal, May 2006
- Bornhövd, Carsten; Vogel, Frank; Neupert, Walter
- Journal of Biological Chemistry, Vol. 281, Issue 20
Topology of the Mitochondrial Inner Membrane: Dynamics and Bioenergetic Implications
journal, September 2001
- Mannella, Carmen A.; Pfeiffer, Douglas R.; Bradshaw, Patrick C.
- IUBMB Life (International Union of Biochemistry and Molecular Biology: Life), Vol. 52, Issue 3-5
Alternative topogenesis of Mgm1 and mitochondrial morphology depend on ATP and a functional import motor
journal, April 2004
- Herlan, Mark; Bornhövd, Carsten; Hell, Kai
- Journal of Cell Biology, Vol. 165, Issue 2
Dynamic subcompartmentalization of the mitochondrial inner membrane
journal, October 2006
- Vogel, Frank; Bornhövd, Carsten; Neupert, Walter
- Journal of Cell Biology, Vol. 175, Issue 2
Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj1 and Su e/g
journal, June 2009
- Rabl, Regina; Soubannier, Vincent; Scholz, Roland
- Journal of Cell Biology, Vol. 185, Issue 6
A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria
journal, October 2011
- Hoppins, Suzanne; Collins, Sean R.; Cassidy-Stone, Ann
- Journal of Cell Biology, Vol. 195, Issue 2
Uniform nomenclature for the mitochondrial contact site and cristae organizing system
journal, March 2014
- Pfanner, Nikolaus; van der Laan, Martin; Amati, Paolo
- Journal of Cell Biology, Vol. 204, Issue 7
The Mitochondrial Inner Membrane Protein Mitofilin Controls Cristae Morphology
journal, March 2005
- John, George B.; Shang, Yonglei; Li, Li
- Molecular Biology of the Cell, Vol. 16, Issue 3
MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization
journal, January 2012
- Alkhaja, Alwaleed K.; Jans, Daniel C.; Nikolov, Miroslav
- Molecular Biology of the Cell, Vol. 23, Issue 2
The C-terminal domain of Fcj1 is required for formation of crista junctions and interacts with the TOB/SAM complex in mitochondria
journal, June 2012
- Körner, Christian; Barrera, Miguel; Dukanovic, Jovana
- Molecular Biology of the Cell, Vol. 23, Issue 11
NOVA: a software to analyze complexome profiling data
journal, October 2014
- Giese, Heiko; Ackermann, Jörg; Heide, Heinrich
- Bioinformatics, Vol. 31, Issue 3
Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits
journal, December 1998
- Arnold, I.
- The EMBO Journal, Vol. 17, Issue 24
The ATP synthase is involved in generating mitochondrial cristae morphology
journal, February 2002
- Paumard, Patrick; Vaillier, Jacques; Coulary, Bénédicte
- The EMBO Journal, Vol. 21, Issue 3
The origin of mitochondrial cristae from alphaproteobacteria
journal, January 2017
- Muñoz-Gómez, Sergio A.; Wideman, Jeremy G.; Roger, Andrew J.
- Molecular Biology and Evolution
The Oxidation Status of Mic19 Regulates MICOS Assembly
journal, December 2015
- Sakowska, Paulina; Jans, Daniel C.; Mohanraj, Karthik
- Molecular and Cellular Biology, Vol. 35, Issue 24
A Mitochondrial Paradigm of Metabolic and Degenerative Diseases, Aging, and Cancer: A Dawn for Evolutionary Medicine
journal, December 2005
- Wallace, Douglas C.
- Annual Review of Genetics, Vol. 39, Issue 1
APOOL Is a Cardiolipin-Binding Constituent of the Mitofilin/MINOS Protein Complex Determining Cristae Morphology in Mammalian Mitochondria
journal, May 2013
- Weber, Tobias A.; Koob, Sebastian; Heide, Heinrich
- PLoS ONE, Vol. 8, Issue 5
Mic13 Is Essential for Formation of Crista Junctions in Mammalian Cells
journal, August 2016
- Anand, Ruchika; Strecker, Valentina; Urbach, Jennifer
- PLOS ONE, Vol. 11, Issue 8
Mitofilin complexes: conserved organizers of mitochondrial membrane architecture
journal, October 2012
- Zerbes, Ralf M.; van der Klei, Ida J.; Veenhuis, Marten
- bchm, Vol. 393, Issue 11
CHCHD
10
mutations promote loss of mitochondrial cristae junctions with impaired mitochondrial genome maintenance and inhibition of apoptosis
journal, December 2015
- Genin, Emmanuelle C.; Plutino, Morgane; Bannwarth, Sylvie
- EMBO Molecular Medicine, Vol. 8, Issue 1
QIL1 mutation causes MICOS disassembly and early onset fatal mitochondrial encephalopathy with liver disease
journal, September 2016
- Guarani, Virginia; Jardel, Claude; Chrétien, Dominique
- eLife, Vol. 5
Works referencing / citing this record:
Single amino acid mutations in the Saccharomyces cerevisiae rhomboid peptidase, Pcp1p, alter mitochondrial morphology
journal, August 2019
- Huddleston, Mary Elizabeth; Xiao, Ningyu; Both, Andries Pieter
- Cell Biology International, Vol. 44, Issue 1
Listeria monocytogenes Exploits Mitochondrial Contact Site and Cristae Organizing System Complex Subunit Mic10 To Promote Mitochondrial Fragmentation and Cellular Infection
journal, February 2020
- Carvalho, Filipe; Spier, Anna; Chaze, Thibault
- mBio, Vol. 11, Issue 1
QIL1-dependent assembly of MICOS complex–lethal mutation in C19ORF70 resulting in liver disease and severe neurological retardation
journal, April 2018
- Gödiker, J.; Grüneberg, M.; DuChesne, I.
- Journal of Human Genetics, Vol. 63, Issue 6
Digging Deeper Into the Pyriproxyfen-Response of the Amphipod Gammarus fossarum With a Next-Generation Ultra-High-Field Orbitrap Analyser: New Perspectives for Environmental Toxicoproteomics
journal, June 2018
- Trapp, Judith; Gouveia, Duarte; Almunia, Christine
- Frontiers in Environmental Science, Vol. 6
Transport o proteins into mitochondria
journal, August 1989
- Pfanner, N.; Neupert, W.
- Current Opinion in Cell Biology, Vol. 1, Issue 4
Transport of Proteins into Mitochondria
journal, March 2019
- Hansen, Katja G.; Herrmann, Johannes M.
- The Protein Journal, Vol. 38, Issue 3
Mitochondrial proteins: from biogenesis to functional networks
journal, January 2019
- Pfanner, Nikolaus; Warscheid, Bettina; Wiedemann, Nils
- Nature Reviews Molecular Cell Biology, Vol. 20, Issue 5
Functional Interplay between Cristae Biogenesis, Mitochondrial Dynamics and Mitochondrial DNA Integrity
journal, September 2019
- Kondadi, Arun Kumar; Anand, Ruchika; Reichert, Andreas S.
- International Journal of Molecular Sciences, Vol. 20, Issue 17
Single amino acid mutations in the Saccharomyces cerevisiae rhomboid peptidase, Pcp1p, alter mitochondrial morphology
journal, August 2019
- Huddleston, Mary Elizabeth; Xiao, Ningyu; Both, Andries Pieter
- Cell Biology International, Vol. 44, Issue 1
The spatio-temporal organization of mitochondrial F1FO ATP synthase in cristae depends on its activity mode
journal, January 2020
- Salewskij, Kirill; Rieger, Bettina; Hager, Frances
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1861, Issue 1
Listeria monocytogenes Exploits Mitochondrial Contact Site and Cristae Organizing System Complex Subunit Mic10 To Promote Mitochondrial Fragmentation and Cellular Infection
journal, February 2020
- Carvalho, Filipe; Spier, Anna; Chaze, Thibault
- mBio, Vol. 11, Issue 1
BANFF:bending of bilayer membranes byamphiphilic α-helices isnecessary forform andfunction of organelles
journal, June 2019
- Könnel, Anne; Bugaeva, Wassilina; Gügel, Irene L.
- Biochemistry and Cell Biology, Vol. 97, Issue 3
The Yin & Yang of Mitochondrial Architecture - Interplay of MICOS and F1Fo-ATP synthase in cristae formation
journal, August 2017
- Rampelt, Heike; van der Laan, Martin
- Microbial Cell, Vol. 4, Issue 8
Impact of F1Fo-ATP-synthase dimer assembly factors on mitochondrial function and organismic aging
journal, April 2018
- Rampello, Nadia G.; Stenger, Maria; Westermann, Benedikt
- Microbial Cell, Vol. 5, Issue 4
Potential Role of Mic60/Mitofilin in Parkinson’s Disease
journal, January 2019
- Van Laar, Victor S.; Otero, P. Anthony; Hastings, Teresa G.
- Frontiers in Neuroscience, Vol. 12
Consequences of Folding the Mitochondrial Inner Membrane
journal, June 2020
- Mannella, Carmen A.
- Frontiers in Physiology, Vol. 11
Functional Interplay between Cristae Biogenesis, Mitochondrial Dynamics and Mitochondrial DNA Integrity
journal, September 2019
- Kondadi, Arun Kumar; Anand, Ruchika; Reichert, Andreas S.
- International Journal of Molecular Sciences, Vol. 20, Issue 17