Structural and physical determinants of complex virus assembly

Institution: Centro Nacional de Biotecnología (CNB)

Members (researchers): Pablo Herrera Nieto, Carmen San Martin

Home page: http://wwwuser.cnb.csic.es/~sanmartinlab
Contact email: carmen@cnb.csic.es

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Research topics:

Experimental structure determination, Structure prediction

Publications

Sandaa, R.-A., Wang, H., Meng, L., Otaegi-Ugartemendia, S., Condezo, G., Blanc-Mathieu, R., Stokke, R., Langvad, M., Brandt, D., Kalinowski, J., Dahle, H., Martín, C. S., & Ogata, H. (2025). Discovery from in-depth molecular analyses of giant viruses: Haptophyte-infecting viruses change the genome condensing proteins of dinoflagellates. https://doi.org/10.21203/rs.3.rs-3957437/v1

Perez-Illana, M., Schachner, A., Hernando-Perez, M., Condezo, G., Paradela, A., Martinez, M., Marabini, R., Hess, M., & San Martin, C. (2025). Aviadenovirus structure: a highly thermostable capsid in the absence of stabilizing proteins. https://doi.org/10.1101/2025.04.23.650237

Condezo, G. N., & San Martín, C. (2024). Maturation of Viruses. Structure and Physics of Viruses, 503–531. https://doi.org/10.1007/978-3-031-65187-8_14

San Martín, C. (2024). Architecture and Assembly of Structurally Complex Viruses. Structure and Physics of Viruses, 431–467. https://doi.org/10.1007/978-3-031-65187-8_12

Sanz Calderón, A., Cantero, M., Pérez, U., Ortega-González, P., San Martín, C., de Pablo, Pedro. J., Manso Silván, M., & Hernando-Pérez, M. (2023). Surface characterization of alkane viral anchoring films prepared by titanate-assisted organosilanization. Colloids and Surfaces B: Biointerfaces, 222, 113136. https://doi.org/10.1016/j.colsurfb.2023.113136

Martín-González, N., Gómez-González, A., Hernando-Pérez, M., Bauer, M., Greber, U. F., San Martín, C., & de Pablo, P. J. (2023). Adenovirus core protein V reinforces the capsid and enhances genome release from disrupted particles. Science Advances, 9(14). https://doi.org/10.1126/sciadv.ade9910

Reguera, D., de Pablo, P. J., Abrescia, N. G. A., Mateu, M. G., Hernández-Rojas, J., Castón, J. R., & San Martín, C. (2023). Physical Virology in Spain. Biophysica, 3(4), 598–619. https://doi.org/10.3390/biophysica3040041

de Pablo, P. J., & San Martín, C. (2022). Seeing and touching adenovirus: complementary approaches for understanding assembly and disassembly of a complex virion. Current Opinion in Virology, 52, 112–122. https://doi.org/10.1016/j.coviro.2021.11.006

Benkő, M., Aoki, K., Arnberg, N., Davison, A. J., Echavarría, M., Hess, M., Jones, M. S., Kaján, G. L., Kajon, A. E., Mittal, S. K., Podgorski, I. I., San Martín, C., Wadell, G., Watanabe, H., & Harrach, B. (2022). ICTV Virus Taxonomy Profile: Adenoviridae 2022. Journal of General Virology, 103(3). https://doi.org/10.1099/jgv.0.001721

Ismail, A. M., Saha, A., Lee, J. S., Painter, D. F., Chen, Y., Singh, G., Condezo, G. N., Chodosh, J., San Martín, C., & Rajaiya, J. (2022). RANBP2 and USP9x regulate nuclear import of adenovirus minor coat protein IIIa. PLOS Pathogens, 18(6), e1010588. https://doi.org/10.1371/journal.ppat.1010588

Condezo, G. N., Martín-González, N., Pérez-Illana, M., Hernando-Pérez, M., Gallardo, J., & San Martín, C. (2021). Adenoviruses (Adenoviridae) and Their Structural Relatives. Encyclopedia of Virology, 329–344. https://doi.org/10.1016/b978-0-12-814515-9.00035-7

Marabini, R., Condezo, G. N., Krupovic, M., Menéndez-Conejero, R., Gómez-Blanco, J., & San Martín, C. (2021). Near-atomic structure of an atadenovirus reveals a conserved capsid-binding motif and intergenera variations in cementing proteins. Science Advances, 7(14). https://doi.org/10.1126/sciadv.abe6008

Maksudov, F., Kononova, O., Llauró, A., Ortega-Esteban, A., Douglas, T., Condezo, G. N., Martín, C. S., Marx, K. A., Wuite, G. J. L., Roos, W. H., de Pablo, P. J., & Barsegov, V. (2021). Fluctuating nonlinear spring theory: Strength, deformability, and toughness of biological nanoparticles from theoretical reconstruction of force-deformation spectra. Acta Biomaterialia, 122, 263–277. https://doi.org/10.1016/j.actbio.2020.12.043

Martín-González, N., Ibáñez-Freire, P., Ortega-Esteban, Á., Laguna-Castro, M., San Martín, C., Valbuena, A., Delgado-Buscalioni, R., & de Pablo, P. J. (2021). Long-Range Cooperative Disassembly and Aging During Adenovirus Uncoating. Physical Review X, 11(2). https://doi.org/10.1103/physrevx.11.021025

Gallardo, J., Pérez-Illana, M., Martín-González, N., & San Martín, C. (2021). Adenovirus Structure: What Is New? International Journal of Molecular Sciences, 22(10), 5240. https://doi.org/10.3390/ijms22105240

Condezo, G. N., & San Martín, C. (2021). Bromodeoxyuridine Labelling to Determine Viral DNA Localization in Fluorescence and Electron Microscopy: The Case of Adenovirus. Viruses, 13(9), 1863. https://doi.org/10.3390/v13091863

Pérez-Illana, M., Martín-González, N., Hernando-Pérez, M., Condezo, G. N., Gallardo, J., Menéndez, M., San Martín, C., & de Pablo, P. J. (2021). Acidification induces condensation of the adenovirus core. Acta Biomaterialia, 135, 534–542. https://doi.org/10.1016/j.actbio.2021.08.019

Martín-González, N., Vieira Gonçalves, L., Condezo, G. N., San Martín, C., Rubiano, M., Fallis, I., Rubino, J. R., Ijaz, M. K., Maillard, J.-Y., & De Pablo, P. J. (2020). Virucidal Action Mechanism of Alcohol and Divalent Cations Against Human Adenovirus. Frontiers in Molecular Biosciences, 7. https://doi.org/10.3389/fmolb.2020.570914

Moya, A., Hernando-Pérez, M., Pérez-Illana, M., San Martín, C., Gómez-Herrero, J., Alemán, J., Mas-Ballesté, R., & de Pablo, P. J. (2020). Multifunctional carbon nanotubes covalently coated with imine-based covalent organic frameworks: exploring structure–property relationships through nanomechanics. Nanoscale, 12(2), 1128–1137. https://doi.org/10.1039/c9nr07716b

Hernando-Pérez, M., Martín-González, N., Pérez-Illana, M., Suomalainen, M., Condezo, G. N., Ostapchuk, P., Gallardo, J., Menéndez, M., Greber, U. F., Hearing, P., de Pablo, P. J., & San Martín, C. (2020). Dynamic competition for hexon binding between core protein VII and lytic protein VI promotes adenovirus maturation and entry. Proceedings of the National Academy of Sciences, 117(24), 13699–13707. https://doi.org/10.1073/pnas.1920896117

Pérez-Illana, M., Martínez, M., Condezo, G. N., Hernando-Pérez, M., Mangroo, C., Brown, M., Marabini, R., & Martín, C. S. (2020). Cryo-EM structure of enteric adenovirus HAdV-F41 highlights structural divergence among human adenoviruses. https://doi.org/10.1101/2020.07.01.177519

Marabini, R., Condezo, G. N., Gómez-Blanco, J., & Martín, C. S. (2020). Near Atomic Structure of an Atadenovirus Reveals a Conserved Capsid-Binding Motif and Intergenera Variations in Cementing Proteins. https://doi.org/10.1101/2020.07.24.220046

San Martín, C. (2019). Virus Maturation. Physical Virology, 129–158. https://doi.org/10.1007/978-3-030-14741-9_7

Martín-González, N., Hernando-Pérez, M., Condezo, G. N., Pérez-Illana, M., Šiber, A., Reguera, D., Ostapchuk, P., Hearing, P., San Martín, C., & de Pablo, P. J. (2019). Adenovirus major core protein condenses DNA in clusters and bundles, modulating genome release and capsid internal pressure. Nucleic Acids Research, 47(17), 9231–9242. https://doi.org/10.1093/nar/gkz687

Vidal, S., El Motiam, A., Seoane, R., Preitakaite, V., Bouzaher, Y. H., Gómez-Medina, S., San Martín, C., Rodríguez, D., Rejas, M. T., Baz-Martínez, M., Barrio, R., Sutherland, J. D., Rodríguez, M. S., Muñoz-Fontela, C., & Rivas, C. (2019). Regulation of the Ebola Virus VP24 Protein by SUMO. Journal of Virology, 94(1). https://doi.org/10.1128/jvi.01687-19

Ortega-Esteban, Á., Martín-González, N., Moreno-Madrid, F., Llauró, A., Hernando-Pérez, M., MartÚn, C. S., & de Pablo, P. J. (2018). Structural and Mechanical Characterization of Viruses with AFM. Atomic Force Microscopy, 259–278. https://doi.org/10.1007/978-1-4939-8894-5_15

Condezo, G. N., & San Martín, C. (2017). Localization of adenovirus morphogenesis players, together with visualization of assembly intermediates and failed products, favor a model where assembly and packaging occur concurrently at the periphery of the replication center. PLOS Pathogens, 13(4), e1006320. https://doi.org/10.1371/journal.ppat.1006320

Menéndez-Conejero, R., Nguyen, T. H., Singh, A. K., Condezo, G. N., Marschang, R. E., van Raaij, M. J., & San Martín, C. (2017). Structure of a Reptilian Adenovirus Reveals a Phage Tailspike Fold Stabilizing a Vertebrate Virus Capsid. Structure, 25(10), 1562-1573.e5. https://doi.org/10.1016/j.str.2017.08.007

Marion, S., San Martín, C., & Šiber, A. (2017). Role of Condensing Particles in Polymer Confinement: A Model for Virus-Packed “Minichromosomes.” Biophysical Journal, 113(8), 1643–1653. https://doi.org/10.1016/j.bpj.2017.08.035

Rojas, L. A., Condezo, G. N., Moreno, R., Fajardo, C. A., Arias-Badia, M., San Martín, C., & Alemany, R. (2016). Albumin-binding adenoviruses circumvent pre-existing neutralizing antibodies upon systemic delivery. Journal of Controlled Release, 237, 78–88. https://doi.org/10.1016/j.jconrel.2016.07.004

Condezo, G. N., Marabini, R., Ayora, S., Carazo, J. M., Alba, R., Chillón, M., & San Martín, C. (2015). Structures of Adenovirus Incomplete Particles Clarify Capsid Architecture and Show Maturation Changes of Packaging Protein L1 52/55k. Journal of Virology, 89(18), 9653–9664. https://doi.org/10.1128/jvi.01453-15

Ortega-Esteban, A., Bodensiek, K., San Martín, C., Suomalainen, M., Greber, U. F., de Pablo, P. J., & Schaap, I. A. T. (2015). Fluorescence Tracking of Genome Release during Mechanical Unpacking of Single Viruses. ACS Nano, 9(11), 10571–10579. https://doi.org/10.1021/acsnano.5b03020

Pérez-Berná, A. J., Marion, S., Chichón, F. J., Fernández, J. J., Winkler, D. C., Carrascosa, J. L., Steven, A. C., Šiber, A., & San Martín, C. (2015). Distribution of DNA-condensing protein complexes in the adenovirus core. Nucleic Acids Research, 43(8), 4274–4283. https://doi.org/10.1093/nar/gkv187

San Martín, C. (2015). Transmission electron microscopy and the molecular structure of icosahedral viruses. Archives of Biochemistry and Biophysics, 581, 59–67. https://doi.org/10.1016/j.abb.2015.06.001

Hernando-Pérez, M., Cartagena-Rivera, A. X., Lošdorfer Božič, A., Carrillo, P. J. P., San Martín, C., Mateu, M. G., Raman, A., Podgornik, R., & de Pablo, P. J. (2015). Quantitative nanoscale electrostatics of viruses. Nanoscale, 7(41), 17289–17298. https://doi.org/10.1039/c5nr04274g

Ortega-Esteban, A., Condezo, G. N., Pérez-Berná, A. J., Chillón, M., Flint, S. J., Reguera, D., San Martín, C., & de Pablo, P. J. (2015). Mechanics of Viral Chromatin Reveals the Pressurization of Human Adenovirus. ACS Nano, 9(11), 10826–10833. https://doi.org/10.1021/acsnano.5b03417

Mangel, W., & San Martín, C. (2014). Structure, Function and Dynamics in Adenovirus Maturation. Viruses, 6(11), 4536–4570. https://doi.org/10.3390/v6114536

Pérez-Berná, A. J., Mangel, W. F., McGrath, W. J., Graziano, V., Flint, J., & San Martín, C. (2014). Processing of the L1 52/55k Protein by the Adenovirus Protease: a New Substrate and New Insights into Virion Maturation. Journal of Virology, 88(3), 1513–1524. https://doi.org/10.1128/jvi.02884-13

Singh, A. K., Menéndez-Conejero, R., San Martín, C., & van Raaij, M. J. (2014). Crystal Structure of the Fibre Head Domain of the Atadenovirus Snake Adenovirus 1. PLoS ONE, 9(12), e114373. https://doi.org/10.1371/journal.pone.0114373

San Martín, C. (2013). Structure and Assembly of Complex Viruses. Structure and Physics of Viruses, 329–360. https://doi.org/10.1007/978-94-007-6552-8_11

Graziano, V., Luo, G., Blainey, P. C., Pérez-Berná, A. J., McGrath, W. J., Flint, S. J., San Martín, C., Xie, X. S., & Mangel, W. F. (2013). Regulation of a Viral Proteinase by a Peptide and DNA in One-dimensional Space. Journal of Biological Chemistry, 288(3), 2068–2080. https://doi.org/10.1074/jbc.m112.407312

Ortega-Esteban, A., Pérez-Berná, A. J., Menéndez-Conejero, R., Flint, S. J., Martín, C. S., & de Pablo, P. J. (2013). Monitoring dynamics of human adenovirus disassembly induced by mechanical fatigue. Scientific Reports, 3(1). https://doi.org/10.1038/srep01434

Singh, A. K., Menéndez-Conejero, R., San Martín, C., & van Raaij, M. J. (2013). Crystallization of the C-terminal domain of the fibre protein from snake adenovirus 1, an atadenovirus. Acta Crystallographica Section F Structural Biology and Crystallization Communications, 69(12), 1374–1379. https://doi.org/10.1107/s1744309113029308

Menéndez-Conejero, R., Pérez-Berná, A. J., Condezo, G. N., Ortega-Esteban, A., del Alamo, M., de Pablo, P. J., & Martín, C. S. (2013). Biophysical Methods to Monitor Structural Aspects of the Adenovirus Infectious Cycle. Adenovirus, 1–24. https://doi.org/10.1007/978-1-62703-679-5_1

Pérez-Berná, A. J., Ortega-Esteban, A., Menéndez-Conejero, R., Winkler, D. C., Menéndez, M., Steven, A. C., Flint, S. J., de Pablo, P. J., & San Martín, C. (2012). The Role of Capsid Maturation on Adenovirus Priming for Sequential Uncoating. Journal of Biological Chemistry, 287(37), 31582–31595. https://doi.org/10.1074/jbc.m112.389957

Ortega-Esteban, A., Horcas, I., Hernando-Pérez, M., Ares, P., Pérez-Berná, A. J., San Martín, C., Carrascosa, J. L., de Pablo, P. J., & Gómez-Herrero, J. (2012). Minimizing tip–sample forces in jumping mode atomic force microscopy in liquid. Ultramicroscopy, 114, 56–61. https://doi.org/10.1016/j.ultramic.2012.01.007

San Martín, C. (2012). Latest Insights on Adenovirus Structure and Assembly. Viruses, 4(5), 847–877. https://doi.org/10.3390/v4050847

Seto, D., Chodosh, J., Brister, J. R., & Jones, M. S. (2011). Using the Whole-Genome Sequence To Characterize and Name Human Adenoviruses. Journal of Virology, 85(11), 5701–5702. https://doi.org/10.1128/jvi.00354-11

Gonzalez-Aparicio, M., Mauleon, I., Alzuguren, P., Bunuales, M., Gonzalez-Aseguinolaza, G., San Martín, C., Prieto, J., & Hernandez-Alcoceba, R. (2011). Self-inactivating helper virus for the production of high-capacity adenoviral vectors. Gene Therapy, 18(11), 1025–1033. https://doi.org/10.1038/gt.2011.58

Pérez-Berná, A. J., Marabini, R., Scheres, S. H. W., Menéndez-Conejero, R., Dmitriev, I. P., Curiel, D. T., Mangel, W. F., Flint, S. J., & Martín, C. S. (2009). Structure and Uncoating of Immature Adenovirus. Journal of Molecular Biology, 392(2), 547–557. https://doi.org/10.1016/j.jmb.2009.06.057

Sorzano, C. O. S., Recarte, E., Alcorlo, M., Bilbao-Castro, J. R., San-Martín, C., Marabini, R., & Carazo, J. M. (2009). Automatic particle selection from electron micrographs using machine learning techniques. Journal of Structural Biology, 167(3), 252–260. https://doi.org/10.1016/j.jsb.2009.06.011

San Martín, C., Glasgow, J. N., Borovjagin, A., Beatty, M. S., Kashentseva, E. A., Curiel, D. T., Marabini, R., & Dmitriev, I. P. (2008). Localization of the N-Terminus of Minor Coat Protein IIIa in the Adenovirus Capsid. Journal of Molecular Biology, 383(4), 923–934. https://doi.org/10.1016/j.jmb.2008.08.054

Luque, D., Saugar, I., Rodríguez, J. F., Verdaguer, N., Garriga, D., Martín, C. S., Velázquez-Muriel, J. A., Trus, B. L., Carrascosa, J. L., & Castón, J. R. (2007). Infectious Bursal Disease Virus Capsid Assembly and Maturation by Structural Rearrangements of a Transient Molecular Switch. Journal of Virology, 81(13), 6869–6878. https://doi.org/10.1128/jvi.00077-07

Gómez-Llorente, Y., Fletcher, R. J., Chen, X. S., Carazo, J. M., & Martín, C. S. (2005). Polymorphism and Double Hexamer Structure in the Archaeal Minichromosome Maintenance (MCM) Helicase from Methanobacterium thermoautotrophicum. Journal of Biological Chemistry, 280(49), 40909–40915. https://doi.org/10.1074/jbc.m509760200

Fletcher, R. J., Shen, J., Gómez-Llorente, Y., Martín, C. S., Carazo, J. M., & Chen, X. S. (2005). Double Hexamer Disruption and Biochemical Activities of Methanobacterium thermoautotrophicum MCM. Journal of Biological Chemistry, 280(51), 42405–42410. https://doi.org/10.1074/jbc.m509773200

Scheres, S. H. W., Marabini, R., Lanzavecchia, S., Cantele, F., Rutten, T., Fuller, S. D., Carazo, J. M., Burnett, R. M., & San Martín, C. (2005). Classification of single-projection reconstructions for cryo-electron microscopy data of icosahedral viruses. Journal of Structural Biology, 151(1), 79–91. https://doi.org/10.1016/j.jsb.2005.04.003

Abrescia, N. G. A., Cockburn, J. J. B., Grimes, J. M., Sutton, G. C., Diprose, J. M., Butcher, S. J., Fuller, S. D., San Martín, C., Burnett, R. M., Stuart, D. I., Bamford, D. H., & Bamford, J. K. H. (2004). Insights into assembly from structural analysis of bacteriophage PRD1. Nature, 432(7013), 68–74. https://doi.org/10.1038/nature03056

Bárcena, M., San Martı́n, C., Weise, F., Ayora, S., Alonso, J. C., & Carazo, J. M. (1998). Polymorphic quaternary organization of the Bacillus subtilis bacteriophage SPP1 replicative helicase (G 40 P) 1 1Edited by W. Baumeister. Journal of Molecular Biology, 283(4), 809–819. https://doi.org/10.1006/jmbi.1998.2128

San Martı́n, M. C., Gruss, C., & Carazo, J. M. (1997). Six molecules of SV40 large T antigen assemble in a propeller-shaped particle around a channel. Journal of Molecular Biology, 268(1), 15–20. https://doi.org/10.1006/jmbi.1997.0952

Marabini Roberto, San Martin M. Carmen, & Carazo Jose M. (1997). ELECTRON TOMOGRAPHY OF BIOLOGICAL SPECIMENS. Contemporary Perspectives in Three-Dimensional Biomedical Imaging. https://doi.org/10.3233/978-1-60750-874-8-53

Marabini, R., Masegosa, I. M., San Martı́n, M. C., Marco, S., Fernández, J. J., de la Fraga, L. G., Vaquerizo, C., & Carazo, J. M. (1996). Xmipp: An Image Processing Package for Electron Microscopy. Journal of Structural Biology, 116(1), 237–240. https://doi.org/10.1006/jsbi.1996.0036

Martín, C. S., Flores, A. I., & Cuezva, J. M. (1995). Cpn60 is exclusively localized into mitochondria of rat liver and embryonic Drosophila cells. Journal of Cellular Biochemistry, 59(2), 235–245. Portico. https://doi.org/10.1002/jcb.240590212

Sanchez-Fauquier, A., Carrascosa, A. L., Carrascosa, J. L., Otero, A., Glass, R. I., Lopez, J. A., San Martin, C., & Melero, J. A. (1994). Characterization of a Human Astrovirus Serotype 2 Structural Protein (VP26) That Contains an Epitope Involved in Virus Neutralization. Virology, 201(2), 312–320. https://doi.org/10.1006/viro.1994.1296

Cortes, E., Martin, C. S., Langeveld, J., Meloen, R., Dalsgaard, K., Vela, C., & Casal, I. (1993). Topographical analysis of canine parvovirus virions and recombinant VP2 capsids. Journal of General Virology, 74(9), 2005–2010. https://doi.org/10.1099/0022-1317-74-9-2005

Carmona, M. J., Hern�ndez-Lucas, C., San Martin, C., Gonz�lez, P., & Garc�a-Olmedo, F. (1993). Subcellular localization of type I thionins in the endosperms of wheat and barley. Protoplasma, 173(1–2), 1–7. https://doi.org/10.1007/bf01378856

Marco, S., Valpuesta, J., Rivas, G., Andrés, G., San Martín, C., & Carrascosa, J. (1993). A structural model for the GroEL chaperonin. FEMS Microbiology Letters, 106(3), 301–308. https://doi.org/10.1111/j.1574-6968.1993.tb05980.x

Ortiz, A., Aranda, F. J., Villalaín, J., San Martin, C., Micol, V., & Gómez-Fernandez, J. C. (1992). 1,2-Dioleoylglycerol promotes calcium-induced fusion in phospholipid vesicles. Chemistry and Physics of Lipids, 62(3), 215–224. https://doi.org/10.1016/0009-3084(92)90058-w

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