The DOI matches its Crossref record; 160 of the 160 references it cites were found in a registry or an index.
Prions as adaptive conduits of memory and inheritance
Abstract
Changes in protein conformation drive most biological processes, but none have seized the imagination of scientists and the public alike as have the self-replicating conformations of prions. Prions transmit lethal neurodegenerative diseases by means of the food chain. However, self-replicating protein conformations can also constitute molecular memories that transmit genetic information. Here, we showcase definitive evidence for the prion hypothesis and discuss examples in which prion-encoded heritable information has been harnessed during evolution to confer selective advantages. We then describe situations in which prion-enciphered events might have essential roles in long-term memory formation, transcriptional memory and genome-wide expression patterns.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Moreover, the templated modification of protein structure also subserves the transfer and storage of useful biological information in systems ranging from microbes to mammals107-110.”
From Pathogenic protein seeding in Alzheimer disease and other neurodegenerative disorders (2011) · cites this paper as [107]
Citations
Cites
Novel Proteinaceous Infectious Particles Cause Scrapie
Prusiner, S. B. (1982) · Science · doi:10.1126/science.6801762 · Cited by 5,221
Protein folding and misfolding
Dobson, C. M. (2003) · Nature · doi:10.1038/nature02261 · Cited by 4,791
Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis
Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W., & Glabe, C. G. (2003) · Science · doi:10.1126/science.1079469 · Cited by 4,064
Functional Discovery via a Compendium of Expression Profiles
Hughes, T. R., Marton, M. J., Jones, A. R., Roberts, C. J., Stoughton, R. B., Armour, C. D., Bennett, H. A., Coffey, E. M., Dai, H. A., He, Y. D., et al. (2000) · Cell · doi:10.1016/s0092-8674(00)00015-5 · Cited by 2,534
Pan, K. M., Baldwin, M. A., Nguyen, J. T., Gasset, M., Serban, A. V., Groth, D., Mehlhorn, I., Huang, Z., Fletterick, R. J., & Cohen, F. E. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.23.10962 · Cited by 2,281
Impairment of the Ubiquitin-Proteasome System by Protein Aggregation
Bence, N., Sampat, R. M., & Kopito, R. R. (2001) · Science · doi:10.1126/science.292.5521.1552 · Cited by 2,209
Mice devoid of PrP are resistant to scrapie
Büeler, H., Aguzzi, A., Sailer, A. W., Greiner, R., Autenried, P., Aguet, M., & Weissmann, C. (1993) · Cell · doi:10.1016/0092-8674(93)90360-3 · Cited by 2,107
Why are ?natively unfolded? proteins unstructured under physiologic conditions?
Uversky, V. N., Gillespie, J. R., & Fink, A. L. (2000) · Proteins Structure Function and Bioinformatics · doi:10.1002/1097-0134(20001115)41:3 · Cited by 2,097
The molecular basis of CaMKII function in synaptic and behavioural memory
Lisman, J., Schulman, H., & Cline, H. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn753 · Cited by 1,860
AN UNSOLVED PROBLEM OF BIOLOGY
(1953) · The Medical Journal of Australia · doi:10.5694/j.1326-5377.1953.tb84985.x · Cited by 1,806
Flagged first, then by citations
Research works printed but not linked: 3
- Wickner, R. B., Liebman, S. W. & Saupe, S. J. in Prion Biology and Diseases (ed. Prusiner, S. B.) 305–372 (Cold Spring Harbor Laboratory Press New York, 2004).
- Kong, Q. et al. in Prion Biology and Diseases (ed. Prusiner, S. B.) 673–775 (Cold Spring Laboratory Press New York, 2004).
- Krishnan, R. & Lindquist, S. L. New structural insights on a yeast prion illuminate nucleation and strain diversity. Nature (in the press). This paper defines which regions of the Sup35 prion domain make intermolecular contacts in assembled prion fibres. It also describes how variations in these intermolecular contacts facilitate the construction of different prion variants.
Cited by
Sorted by citations
Items 501–555 of 555
PrionOme: A database of prions and other sequences relevant to prion phenomenaPreprint
Sowdhamini, R., Harrison, P. M., Harbi, D., Marimuthu, P., Gendoo, D. M. A., Ehsani, S., Kumar, M., & Schmitt‐Ulms, G. (2011) · Nature Precedings · doi:10.1038/npre.2011.6430.1
Nikhil, V., Jha, P., & Jha, M. (2013) · Dental Journal of Advance Studies · doi:10.1055/s-0038-1670587
Lewis, P. A., & Spillane, J. E. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-811069-0.00004-5
Susan Lee Lindquist (1949–2016)
Shorter, J. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2016.12.002
Self-citationKhan, F. A. (2014) · CRC Press eBooks · doi:10.1201/b16905-11
Hunting for Prions: Propagating Putative Prion States in Budding Yeast
Evarts, J. I., & Capage, M. (2021) · Oregon Undergraduate Research Journal · doi:10.5399/uo/ourj/18.1.4
Hugwil, A. V. (2021) · Open Access Journal of Cancer & Oncology · doi:10.23880/oajco-16000169
SOUS-CHAPITRE 8.4 Les maladies à prions
Lehmann, S. (2020) · EDP Sciences eBooks · doi:10.1051/978-2-7598-0154-1.c016
A Prion that regulates genome diversificationPreprint
Byers, J. S., Futia, R. A., Elgort, A. V., Lozanoski, T. M., Garcia, D. M., & Jarosz, D. F. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.23.465590
Uversky, V. N., & Breydo, L. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.717747972.793302833
Saupe, S. J., Jarosz, D. F., & True, H. L. (2017) · ASM Press eBooks · doi:10.1128/9781555819583.ch32
Schwarzbach, K. (2016) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-5852
(2009) · Wiley eBooks · doi:10.1002/9780470551455.biblio
van der Wel, P. C. A. (2021) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737535870.793582169
Essential Role of nSR100 and CPEB4 Proteins During the Development of the Nervous System
Venkata, S. G., & Rajagopal, S. (2022) · Nutritional neurosciences · doi:10.1007/978-981-15-9781-7_13
Clausen, T., & Suskiewicz, M. J. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.717980334.793471552
David, D. C. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.717968823.793468464
Reines, D. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737535870.793573000
Yeates, T. O. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737535870.793575865
Molecular and clinical determinants of pathogenic protein aggregation
de Mattos, E. P. (2022) · University of Groningen research database (University of Groningen / Centre for Information Technology) · doi:10.33612/diss.220760500
Investigation of Early Complex Formation of Huntingtin Protein With and Without Lipids
Stonebraker, A. R. (2023) · The Research Repository @ WVU (West Virginia University) · doi:10.33915/etd.11962
PRIONS AND AMYLOIDS AS SPATIAL TEMPLATES OF THE PROTEOME
Inge-Vechtomov, S. G., Galkin, A. P., Zhouravleva, G. A., Nizhnikov, A. A., & Zadorsky, S. P. (2023) · Вестник Российской академии наук · doi:10.31857/s0869587323090074
Gangopadhayya, A., Dharavath, M., Mhaske, S. T., & Bhukya, P. L. (2024) · Springer eBooks · doi:10.1007/978-981-97-4480-0_11
Our Ancient History with Microbes
Ramanathan, J. (2024) · Springer eBooks · doi:10.1007/978-3-031-70088-0_14
Thermo-primed cellular networks for plant stress management
Raturi, V., & Zinta, G. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-13490-6.00033-3
Receptor for Advanced Glycation End Products in Neuronal Pathophysiology
Malik, P., Rani, R., & Mukherjee, T. K. (2025) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/9789815322521125010012
Шкробот, С. І., Nasalyk, R. B., Duve, K. V., & SHALABAI, N. (2025) · Psychiatry Neurology and Medical Psychology · doi:10.26565/2312-5675-2025-27-10
Reversible amyloids encode biomolecular memory through hysteresisPreprint
Michaels, T. C. T., Dear, A. J., Pfizenmaier, D. M., Rüdiger, S., Коваленко, А., Lee, S. S., Arosio, P., & Peter, M. (2025) · Research Square · doi:10.21203/rs.3.rs-7754493/v1
Bhadra, A. K., Aggarwal, G., Jaysingh, M. A., Chen, D. C., Daw, J., Weihl, C. C., & True, H. L. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110945
Propagating Prions: An Essential Role for Molecular Chaperones
Guinan, E., Blumlein, A., Cusack, S. A., Moran, C., Loovers, H. M., & Jones, G. W. (2009) · Heat shock proteins · doi:10.1007/978-90-481-2976-8_2
A Role of Yeast Adhesin Amyloids in Force-Dependent Adhesion and Biofilm Formation
Chan, C. X. J. (2014) · CUNY Academic Works (City University of New York)
Peña‐Díaz, S., Zhang, Z., Mittal, C., Jiang, Y., Ferreira, P., Hernández, M. L., Daugberg, A. O. H., Dueholm, M. S., Ramos, M. J., Pedersen, J. S., et al. (2026) · Elsevier eBooks · doi:10.1016/b978-0-323-99507-8.00052-4
N6-methyldeoxyadenosine is a transgenerational epigenetic mark protecting DNA from deletionPreprint
Li, X., Allen, S., Lyu, L., Bechara, S. T., Cristina, E., Hendrick, A. G., & Nowacki, M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.13.705781
Bio-inspired protein nanowire : electrical conductivity and use as redox mediator for enzyme wiring
Altamura, L. (2015) · theses.fr (ABES) · doi:10.70675/98fc4371z3d35z4b3az9e8bz77e61cef5d70
Malabirade, A. (2017) · theses.fr (ABES) · doi:10.70675/fe1363f1z38f6z41e3za6c0z45558d9d4ec4
Recent cryo-EM structures redefine the functional amyloid landscape
Ventura, S., Bartolomé-Nafría, A., & García‐Pardo, J. (2026) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2026.03.008
Role of the Prion-like domain of Imp in neuronal RNP granule regulation
Vijayakumar, J. (2018) · theses.fr (ABES) · doi:10.70675/ca5e1883z42fbz4d34z93f6zaf2f3d1a3e60
Analyse de l’assemblage de peptides amyloïdes bactériens
Partouche, D. M. (2018) · theses.fr (ABES) · doi:10.70675/02bec91cz773dz4dfbzb6a9z26cb75eb69a8
Castelot, R. (2024) · theses.fr (ABES) · doi:10.70675/c2a7ce1ez8caaz4593zbb3azae8add8055b5
Programming Biomimetic Self-Assembly through Solvent-Encoded Pathway SelectionPreprint
Yang, S. (2026) · Research Square · doi:10.21203/rs.3.rs-9380005/v1
De-Darwinizing the proteome: the genome as the original germ linePreprint
Ratcliff, W. C., & Burnetti, A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.06.723269
N6-methyldeoxyadenosine is a transgenerational epigenetic mark protecting DNA from deletionPreprint
Nowacki, M., Li, X., Allen, S., Bechara, S. T., Hoehener, C., & Hendrick, A. G. (2026) · Research Square · doi:10.21203/rs.3.rs-9235884/v1
A Phosphorylation‐Induced Micellization Switch in the Low‐Complexity Domain of TDP‐43
Dillenburg, R. F., Anastasia, L., Ruan, H., Scheidt, T., Mosna, S., Pekbilir, E., Hesselbarth, J., Schafer-Depoix, F., Landfester, K., Schmidt, C., et al. (2026) · Advanced Science · doi:10.1002/advs.76625
A DNA-barcoded Luria-Delbrück assay resolves mechanisms of adaptationPreprint
Husain, K. B., Flagg, L., Pincus, D., & Murugan, A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.03.742544
Lin, J., Banwait, J. K., Saurabh, A., Sharp, K. A., Southworth, D. R., Pressé, S., Lucius, A. L., Goldman, Y. E., & Shorter, J. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.08.09.743785
Self-citationPrion-like proteins as facilitators of molecular memory in plants
Johnson, J. J., & Meyer, H. M. (2026) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2026.08.005
Prion-induced heritable states in Caenorhabditis elegansPreprint
Ilbay, O., Zabinsky, R. A., Lozanoski, T. M., Jarosz, D. F., & Fire, A. Z. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.27.753494
Fundamentals of protein structure and function
Chaki, S., & Dasgupta, S. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-44536-1.00021-3
Dagestad, G. (2010) · NORA - Norwegian Open Research Archives
Metadata
- Authors
- Shorter, J., & Lindquist, S.
- Affiliations
- Whitehead Institute for Biomedical Research (US)
- Corresponding author
- Shorter, James
- Lindquist, Susan
- ORCID
- Shorter, James
- Venue
- Nature Reviews Genetics
- Published
- 2005-06
- Volume
- 6
- Issue
- 6
- Pages
- 435-450
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2141566674
- Cited by
- 555
- References
- 160
- Citations by year
- 2026: 15 · 2025: 15 · 2024: 15 · 2023: 16 · 2022: 15 · 2021: 28 · 2020: 27 · 2019: 18 · 2018: 23 · 2017: 26 · 2016: 27 · 2015: 30 · 2014: 21 · 2013: 33 · 2012: 38
- FWCI
- 2.42
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Charles A. King Trust
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Prion Diseases and Protein Misfolding
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Keywords
- prions, protein conformation, prion hypothesis, molecular memory, evolution, neurodegenerative diseases, long-term memory, transcriptional memory, gene expression patterns
- MeSH terms
- Amyloid, Animals, Biological Evolution, Humans, Memory, Peptide Termination Factors, Prions, Protein Structure, Tertiary, Saccharomyces cerevisiae Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review