Cited by 755Epigenetics and DNA MethylationBirth, Development, and HealthSperm and Testicular Function

The DOI matches its Crossref record; 48 of the 48 references it cites were found in a registry or an index.

Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress

Open access

Rodgers, Ali B., Morgan, Christopher P., Leu, N. Adrian, Bale, Tracy L.·2015·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1508347112PMC PMC4640733

Open this paper in CoChat — free account

Abstract

Significance: Studies examining paternal exposure to diverse environmental stimuli propose that epigenetic marks in germ cells, including small noncoding RNAs such as microRNA (miR), transmit experience-dependent information from parent to offspring. However, these nongenetic mechanisms of transgenerational inheritance are poorly understood, specifically how these germ-cell marks may act postfertilization to enact long-term changes in offspring behavior or physiology. In this study, through zygote microinjection of nine specific sperm miRs previously identified in our paternal stress mouse model, we demonstrate that sperm miRs function to reduce maternal mRNA stores in early zygotes, ultimately reprogramming gene expression in the offspring hypothalamus and recapitulating the offspring stress dysregulation phenotype.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1073/pnas.1508347112

Cites

48 of 48 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400
Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625
<tt>edgeR</tt> : a Bioconductor package for differential expression analysis of digital gene expression data
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190
Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108
PGC-1α-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes
Mootha, V. K., Lindgren, C. M., Eriksson, K.-F., Subramanian, A., Sihag, S., Lehar, J., Puigserver, P., Carlsson, E., Ridderstråle, M., Laurila, E., et al. (2003) · Nature Genetics · doi:10.1038/ng1180 · Cited by 10,197
miRWalk – Database: Prediction of possible miRNA binding sites by “walking” the genes of three genomes
Dweep, H., Sticht, C., Pandey, P., & Gretz, N. (2011) · Journal of Biomedical Informatics · doi:10.1016/j.jbi.2011.05.002 · Cited by 1,707
Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways
Grimm, D., Streetz, K. L., Jopling, C. L., Storm, T. A., Pandey, K., Davis, C. R., Marion, P., Salazar, F., & Kay, M. A. (2006) · Nature · doi:10.1038/nature04791 · Cited by 1,677
Autism genome-wide copy number variation reveals ubiquitin and neuronal genes
Glessner, J. T., Wang, K., Cai, G., Korvatska, O., Kim, C. E., Wood, S., Zhang, H., Estes, A., Brune, C. W., Bradfield, J. P., et al. (2009) · Nature · doi:10.1038/nature07953 · Cited by 1,421

Show all 48 references

Sorted by citations

Items 101–200 of 755

Paternal preconception alcohol exposure imparts intergenerational alcohol-related behaviors to male offspring on a pure C57BL/6J background
Rompala, G. R., Finegersh, A., Slater, M., & Homanics, G. E. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.11.001 · Cited by 86
Paternal epigenetics: Mammalian sperm provide much more than DNA at fertilization
Blévec, E. L., Muroňová, J., Ray, P. F., & Arnoult, C. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110964 · Cited by 86
Discovery of a Novel Seminal Fluid Microbiome and Influence of Estrogen Receptor Alpha Genetic Status
Javurek, A. B., Spollen, W. G., Ali, A. M. M., Johnson, S., Lubahn, D. B., Bivens, N. J., Bromert, K. H., Ellersieck, M. R., Givan, S. A., & Rosenfeld, C. S. (2016) · Scientific Reports · doi:10.1038/srep23027 · Cited by 83
Paternal epigenetic programming: evolving metabolic disease risk
Hur, S. S. J., Cropley, J. E., & Suter, C. M. (2017) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0236 · Cited by 81
Developmental programming of the HPA axis and related behaviours: epigenetic mechanisms
Matthews, S. G., & McGowan, P. O. (2019) · Journal of Endocrinology · doi:10.1530/joe-19-0057 · Cited by 85
Diet-Induced Modification of the Sperm Epigenome Programs Metabolism and Behavior
Bodden, C., Hannan, A. J., & Reichelt, A. C. (2019) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2019.10.005 · Cited by 81
Paternal phthalate exposure-elicited offspring metabolic disorders are associated with altered sperm small RNAs in mice
Liu, J., Shi, J., Hernandez, R., Li, X., Konchadi, P., Miyake, Y., Chen, Q., Zhou, T., & Zhou, C. (2023) · Environment International · doi:10.1016/j.envint.2023.107769 · Cited by 83
The Role of Epigenomics in Aquatic Toxicology
Brander, S. M., Biales, A. D., & Connon, R. E. (2017) · Environmental Toxicology and Chemistry · doi:10.1002/etc.3930 · Cited by 81
Embryonic environment and transgenerational effects in quail
Leroux, S., Gourichon, D., Leterrier, C., Labrune, Y., Coustham, V., Rivière, S., Zerjal, T., Coville, J., Morisson, M., Minvielle, F., et al. (2017) · Genetics Selection Evolution · doi:10.1186/s12711-017-0292-7 · Cited by 83
Can epigenetics translate environmental cues into phenotypes?
Norouzitallab, P., Baruah, K., Vanrompay, D. C. G., & Bossier, P. (2018) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2018.08.063 · Cited by 84
Periconceptional environment and the developmental origins of disease
Velazquez, M. A., Fleming, T. P., & Watkins, A. J. (2019) · Journal of Endocrinology · doi:10.1530/joe-18-0676 · Cited by 79
Single-molecule long-read sequencing reveals a conserved intact long RNA profile in sperm
Sun, Y. H., Wang, A., Song, C. W., Shankar, G., Srivastava, R. K., Au, K. F., & Li, X. Z. (2021) · Nature Communications · doi:10.1038/s41467-021-21524-6 · Cited by 80
Transgenerational transmission of aspartame-induced anxiety and changes in glutamate-GABA signaling and gene expression in the amygdala
Jones, S. K., McCarthy, D. M., Vied, C., Stanwood, G. D., Schatschneider, C. W., & Bhide, P. G. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2213120119 · Cited by 77
Transgenerational epigenetics: Integrating soma to germline communication with gametic inheritance
Sharma, A. (2017) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2016.12.015 · Cited by 80
Effect of stress on human biology: Epigenetics, adaptation, inheritance, and social significance
Denhardt, D. T. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.25837 · Cited by 76
Soma-to-germline RNA communication
Conine, C. C., & Rando, O. J. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00412-1 · Cited by 80
Driving the Next Generation: Paternal Lifetime Experiences Transmitted via Extracellular Vesicles and Their Small RNA Cargo
Morgan, C. P., Chan, J. C., & Bale, T. L. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.09.007 · Cited by 74
Self-citation
Maternal stress and fish reproduction: The role of cortisol revisited
Faught, E. L., & Vijayan, M. M. (2018) · Fish and Fisheries · doi:10.1111/faf.12309 · Cited by 73
Changes in miRNA levels of sperm and small extracellular vesicles of seminal plasma are associated with transient scrotal heat stress in bulls
Alves, M. B. R., de Arruda, R. P., Batissaco, L., Garcia‐Oliveros, L. N., Gonzaga, V. H. G., Nogueira, V. J. M., Almeida, F. D. S., Pinto, S. C. C., Andrade, G. M., Perecin, F., et al. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.11.015 · Cited by 76
Maternal gut microbiota mediate intergenerational effects of high-fat diet on descendant social behavior
Gesù, C. M. D., Matz, L. M., Bolding, I. J., Fultz, R., Hoffman, K. L., Marino, A., Petrosino, J. F., & Buffington, S. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111461 · Cited by 74
Exercise and epigenetic inheritance of disease risk
Denham, J. (2017) · Acta Physiologica · doi:10.1111/apha.12881 · Cited by 79
Paternal programming of offspring cardiometabolic diseases in later life
Li, J., Tsuprykov, O., Yang, X., & Hocher, B. (2016) · Journal of Hypertension · doi:10.1097/hjh.0000000000001051 · Cited by 76
How do lifestyle and environmental factors influence the sperm epigenome? Effects on sperm fertilising ability, embryo development, and offspring health
Akhatova, A., Jones, C., Coward, K., & Yeste, M. (2025) · Clinical Epigenetics · doi:10.1186/s13148-025-01815-1 · Cited by 87
Repression in Residential Youth Care: A Scoping Review
de Valk, S., Kuiper, C. H. Z., van der Helm, P. G., Maas, A. J. J., & Stams, G. J. J. M. (2016) · Adolescent Research Review · doi:10.1007/s40894-016-0029-9 · Cited by 80
Prenatal Ethanol Exposure and Neocortical Development: A Transgenerational Model of FASD
Abbott, C. W., Rohac, D. J., Bottom, R. T., Patadia, S., & Huffman, K. J. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx168 · Cited by 72
Frequency, morbidity and equity — the case for increased research on male fertility
Kimmins, S., Anderson, R. A., Barratt, C. L. R., Behre, H. M., Catford, S. R., Jonge, C. J. D., Delbès, G., Eisenberg, M. L., Garrido, N., Houston, B. J., et al. (2023) · Nature Reviews Urology · doi:10.1038/s41585-023-00820-4 · Cited by 71
Paternal cocaine taking elicits epigenetic remodeling and memory deficits in male progeny
Wimmer, M. E., Briand, L. A., Fant, B., Guercio, L. A., Arreola, A. C., Schmidt, H. D., Sidoli, S., Han, Y., Garcia, B. A., & Pierce, R. C. (2017) · Molecular Psychiatry · doi:10.1038/mp.2017.8 · Cited by 70
Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications
Evans, J. P., Wilson, A. J., Pilastro, A., & García–González, F. (2019) · Reproduction · doi:10.1530/rep-18-0524 · Cited by 72
Learning of Signaling Networks: Molecular Mechanisms
Csermely, P., Kunšič, N., Mendik, P., Kerestély, M., Faragó, T., Veres, D. V., & Tompa, P. (2020) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2019.12.005 · Cited by 73
Paternal high-fat diet and exercise regulate sperm miRNA and histone methylation to modify placental inflammation, nutrient transporter mRNA expression and fetal weight in a sex-dependent manner
Larson, K., Bundy, A. N., & Roemmich, J. N. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108373 · Cited by 75
Epigenetics in fibrosis
O’Reilly, S. (2016) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2016.10.001 · Cited by 71
A comprehensive overview of bull sperm-borne small non-coding RNAs and their diversity across breeds
Sellem, E., Marthey, S., Rau, A., Jouneau, L., Allais‐Bonnet, A., Perrier, J., Fritz, S., Danvic, C. L., Boussaha, M., Kiefer, H., et al. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00340-0 · Cited by 70
Heritable variation in circulating glucocorticoids and endocrine flexibility in a free‐living songbird
Stedman, J. M., Hallinger, K. K., Winkler, D. W., & Vitousek, M. N. (2017) · Journal of Evolutionary Biology · doi:10.1111/jeb.13135 · Cited by 67
Epigenetic germline inheritance in mammals: looking to the past to understand the future
Gapp, K., & Bohacek, J. (2017) · Genes Brain & Behavior · doi:10.1111/gbb.12407 · Cited by 72
Protection from DNA re-methylation by transcription factors in primordial germ cells and pre-implantation embryos can explain trans-generational epigenetic inheritance
Kremsky, I., & Corces, V. G. (2020) · Genome biology · doi:10.1186/s13059-020-02036-w · Cited by 73
All Roads Lead to the miRNome: miRNAs Have a Central Role in the Molecular Pathophysiology of Psychiatric Disorders
O’Connor, R. M., Gururajan, A., Dinan, T. G., Kenny, P. J., & Cryan, J. F. (2016) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2016.10.004 · Cited by 69
Noncoding RNAs: Stress, Glucocorticoids, and Posttraumatic Stress Disorder
Daskalakis, N. P., Provost, A. C., Hunter, R. G., & Guffanti, G. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.01.009 · Cited by 69
FK506 binding protein 51 integrates pathways of adaptation
Rein, T. (2016) · BioEssays · doi:10.1002/bies.201600050 · Cited by 67
Transgenerational effects of polychlorinated biphenyls: 1. Development and physiology across 3 generations of rats
Mennigen, J. A., Thompson, L. M., Bell, M., Santos, M. T., & Gore, A. C. (2018) · Environmental Health · doi:10.1186/s12940-018-0362-5 · Cited by 65
Intergenerational Effects of Alcohol: A Review of Paternal Preconception Ethanol Exposure Studies and Epigenetic Mechanisms in the Male Germline
Rompala, G. R., & Homanics, G. E. (2019) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.14029 · Cited by 70
Stress and the Emerging Roles of Chromatin Remodeling in Signal Integration and Stable Transmission of Reversible Phenotypes
Weaver, I. C. G., Korgan, A. C., Lee, K., Wheeler, R. V., Hundert, A. S., & Goguen, D. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00041 · Cited by 69
Multigenerational epigenetic inheritance: One step forward, two generations back
Tuscher, J. J., & Day, J. J. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104591 · Cited by 63
What Is a Genome?
Goldman, A. D., & Landweber, L. F. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006181 · Cited by 67
MicroRNAs and psychiatric disorders: From aetiology to treatment
Luoni, A., & Riva, M. A. (2016) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2016.07.006 · Cited by 62
Role of epigenetic mechanisms in transmitting the effects of neonatal sevoflurane exposure to the next generation of male, but not female, rats
Ju, L.-S., Yang, J., Morey, T. E., Gravenstein, N. L., Seubert, C. N., Resnick, J. L., Zhang, J.-Q., & Martynyuk, A. E. (2018) · British Journal of Anaesthesia · doi:10.1016/j.bja.2018.04.034 · Cited by 63
Paternal malnutrition programs breast cancer risk and tumor metabolism in offspring
da Cruz, R. S., Carney, E., Clarke, J., Cao, H., Cruz, M. I., Benitez, C., Lu, J., Fu, Y., Cheng, Z., Wang, Y., et al. (2018) · Breast Cancer Research · doi:10.1186/s13058-018-1034-7 · Cited by 67
Contribution of epididymal epithelial cell functions to sperm epigenetic changes and the health of progeny
Chen, H., Alves, M. B. R., & Belleannée, C. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab029 · Cited by 63
The influence of paternal diet on sncRNA-mediated epigenetic inheritance
Klastrup, L. K., Bak, S. T., & Nielsen, A. L. (2018) · Molecular Genetics and Genomics · doi:10.1007/s00438-018-1492-8 · Cited by 66
Transgenerational paternal transmission of acquired traits: stress-induced modification of the sperm regulatory transcriptome and offspring phenotypes
Pang, T. Y., Short, A. K., Bredy, T. W., & Hannan, A. J. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.02.007 · Cited by 61
Acrylamide modulates the mouse epididymal proteome to drive alterations in the sperm small non-coding RNA profile and dysregulate embryo development
Trigg, N. A., Skerrett-Byrne, D. A., Xavier, M. J., Zhou, W., Anderson, A. L., Stanger, S. J., Katen, A. L., Iuliis, G. N. D., Dun, M. D., Roman, S. D., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109787 · Cited by 62
Recruitment of CTCF to an Fto enhancer is responsible for transgenerational inheritance of BPA-induced obesity
Jung, Y. H., Wang, H. V., Ruíz, D., Bixler, B. J., Linsenbaum, H., Xiang, J., Forestier, S., Shafik, A. M., Jin, P., & Corces, V. G. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2214988119 · Cited by 71
Mother or Father: Who Is in the Front Line? Mechanisms Underlying the Non-Genomic Transmission of Obesity/Diabetes via the Maternal or the Paternal Line
Portha, B., Grandjean, V., & Movassat, J. (2019) · Nutrients · doi:10.3390/nu11020233 · Cited by 64
Intergenerational transmission of the positive effects of physical exercise on brain and cognition
McGreevy, K. R., Tezanos, P., Ferreiro‐Villar, I., Pallé, A., Moreno-Serrano, M., Esteve‐Codina, A., Lamas‐Toranzo, I., Bermejo‐Álvarez, P., Fernández-Punzano, J., Martín‐Montalvo, A., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1816781116 · Cited by 63
Association of Maternal Prepregnancy Dyslipidemia With Adult Offspring Dyslipidemia in Excess of Anthropometric, Lifestyle, and Genetic Factors in the Framingham Heart Study
Mendelson, M. M., Lyass, A., O’Donnell, C. J., D’Agostino, R. B., & Levy, D. (2016) · JAMA Cardiology · doi:10.1001/jamacardio.2015.0304 · Cited by 60
A Novel Class of tRNA-Derived Small Non-Coding RNAs Respond to Myocardial Hypertrophy and Contribute to Intergenerational Inheritance
Shen, L., Gan, M., Tan, Z., Jiang, D., Jiang, Y., Li, M., Wang, J., Li, X., Zhang, S., & Zhu, L. (2018) · Biomolecules · doi:10.3390/biom8030054 · Cited by 61
Altered sperm tsRNAs in aged male contribute to anxiety‐like behavior in offspring
Guo, Y., Bai, D., Liu, W., Liu, Y., Zhang, Y., Kou, X., Chen, J., Wang, H., Teng, X., Zuo, J., et al. (2021) · Aging Cell · doi:10.1111/acel.13466 · Cited by 61
Transgenerational attenuation of opioid self-administration as a consequence of adolescent morphine exposure
Vassoler, F. M., Oliver, D. J., Wyse, C., Blau, A., Shtutman, M. S., Turner, J. R., & Byrnes, E. M. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.10.006 · Cited by 59
Small RNAs in epigenetic inheritance: from mechanisms to trait transmission
Cecere, G. (2021) · FEBS Letters · doi:10.1002/1873-3468.14210 · Cited by 61
Prenatal programming of stress responsiveness and behaviours: Progress and perspectives
Hamada, H., & Matthews, S. G. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12674 · Cited by 65
Biological Embedding of Early-Life Adversity and a Scoping Review of the Evidence for Intergenerational Epigenetic Transmission of Stress and Trauma in Humans
Zhou, A., & Ryan, J. (2023) · Genes · doi:10.3390/genes14081639 · Cited by 57
“Likewise, paternal stress prior to conception can influence offspring behavior and DNA methylation patterns [77], and a mechanistic role for sperm microRNAs in the transgenerational transmission of stress reactivity to the offspring has also been demonstrated [70].”
Background
Epigenetic Inheritance: Intergenerational Effects of Pesticides and Other Endocrine Disruptors on Cancer Development
Nicolella, H. D., & de Assis, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23094671 · Cited by 64
The Epigenetics of Gametes and Early Embryos and Potential Long-Range Consequences in Livestock Species—Filling in the Picture With Epigenomic Analyses
Zhu, L., Marjani, S. L., & Jiang, Z. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.557934 · Cited by 62
The Effects of Early Life Stress on the Brain and Behaviour: Insights From Zebrafish Models
Eachus, H., Choi, M., & Ryu, S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.657591 · Cited by 55
Genetic and epigenetic factors and early life inflammation as predictors of neurodevelopmental outcomes
Oldenburg, K. S., O’Shea, T. M., & Fry, R. C. (2020) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2020.101115 · Cited by 58
Paternal preconception ethanol exposure blunts hypothalamic-pituitary-adrenal axis responsivity and stress-induced excessive fluid intake in male mice
Rompala, G. R., Finegersh, A., & Homanics, G. E. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.03.006 · Cited by 53
An Exercise‐Only Intervention in Obese Fathers Restores Glucose and Insulin Regulation in Conjunction with the Rescue of Pancreatic Islet Cell Morphology and MicroRNA Expression in Male Offspring
McPherson, N. O., Lane, M., Sandeman, L., Owens, J. A., & Fullston, T. (2017) · Nutrients · doi:10.3390/nu9020122 · Cited by 57
Medaka as a model for studying environmentally induced epigenetic transgenerational inheritance of phenotypes
Bhandari, R. K. (2016) · Current Zoology · doi:10.1093/eep/dvv010 · Cited by 55
Maternal overnutrition induces long-term cognitive deficits across several generations
Sarker, G., & Peleg-Raibstein, D. (2018) · Nutrients · doi:10.3390/nu11010007 · Cited by 52
Epigenetic mechanisms impacted by chronic stress across the rodent lifespan
Dion, A., Muñoz, P., & Franklin, T. B. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100434 · Cited by 54
Consumption of a high-fat diet alters the seminal fluid and gut microbiomes in male mice
Javurek, A. B., Spollen, W. G., Johnson, S., Bivens, N. J., Bromert, K. H., Givan, S. A., & Rosenfeld, C. S. (2016) · Reproduction Fertility and Development · doi:10.1071/rd16119 · Cited by 55
DNA methylation correlates of PTSD: Recent findings and technical challenges
Morrison, F. G., Miller, M. W., Logue, M. W., Assef, M., & Wolf, E. J. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.11.011 · Cited by 56
Prenatal Stress and Maternal Immune Dysregulation in Autism Spectrum Disorders: Potential Points for Intervention
Beversdorf, D. Q., Stevens, H. E., Margolis, K. G., & de Water, J. V. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666191119093335 · Cited by 60
Paternal epigenetic influences on placental health and their impacts on offspring development and disease
Bhadsavle, S. S., & Golding, M. C. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.1068408 · Cited by 57
Small RNA shuffling between murine sperm and their cytoplasmic droplets during epididymal maturation
Wang, H., Wang, Z., Zhou, T., Morris, D., Chen, S., Li, M., Wang, Y., Zheng, H., Wei-neng, F., & Yan, W. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.03.010 · Cited by 52
Female-Specific Intergenerational Transmission Patterns of the Human Corticolimbic Circuitry
Yamagata, B., Murayama, K., Black, J. M., Hancock, R., Mimura, M., Yang, T. T., Reiss, A. L., & Hoeft, F. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.4974-14.2016 · Cited by 51
mi RNA Regulation of Immune Tolerance in Early Pregnancy
Schjenken, J. E., Zhang, B., Chan, H. Y., Sharkey, D. J., Fullston, T., & Robertson, S. A. (2016) · American Journal of Reproductive Immunology · doi:10.1111/aji.12490 · Cited by 50
Epigenetic control of variation and stochasticity in metabolic disease
Panzeri, I., & Pospisilik, J. A. (2018) · Molecular Metabolism · doi:10.1016/j.molmet.2018.05.010 · Cited by 50
Sperm miRNAs— potential mediators of bull age and early embryo development
Wu, C., Blondin, P., Vigneault, C., Labrecque, R., & Sirard, M. (2020) · BMC Genomics · doi:10.1186/s12864-020-07206-5 · Cited by 49
SIRT1-dependent modulation of methylation and acetylation of histone H3 on lysine 9 (H3K9) in the zygotic pronuclei improves porcine embryo development
Adámková, K., Yi, Y., Petr, J., Žalmanová, T., Hošková, K., Jelinkova, P., Moravec, J., Králíčková, M., Sutovsky, M., Šutovský, P., et al. (2017) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-017-0214-0 · Cited by 53
Parental breeding age effects on descendants’ longevity interact over 2 generations in matrilines and patrilines
Wylde, Z., Spagopoulou, F., Hooper, A. K., Maklakov, A. A., & Bonduriansky, R. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000556 · Cited by 48
Cryopreservation Induces Alterations of miRNA and mRNA Fragment Profiles of Bull Sperm
Shangguan, A., Zhou, H., Sun, W., Ding, R., Li, X., Liu, J., Zhou, Y., Chen, X., Ding, F., Yang, L., et al. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.00419 · Cited by 48
Transgenerational epigenetic inheritance of traumatic experience in mammals
Švorcová, J. (2023) · Genes · doi:10.3390/genes14010120 · Cited by 47
Association of maternal and paternal perinatal depression and anxiety with infant development: A longitudinal study
Rogers, A., Youssef, G. J., Teague, S. J., Sunderland, M., Bas, G. A. L., Macdonald, J. A., Mattick, R. P., ALLSOP, S. J., Elliott, E. J., Olsson, C. A., et al. (2023) · Journal of Affective Disorders · doi:10.1016/j.jad.2023.06.020 · Cited by 52
Paternal transgenerational epigenetic mechanisms mediating stress phenotypes of offspring
Cunningham, A. M., Walker, D. M., & Nestler, E. J. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14582 · Cited by 50
Non-coding RNAs Shaping Muscle
Martone, J., Mariani, D., Desideri, F., & Ballarino, M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2019.00394 · Cited by 49
Transgenerational Inheritance of Paternal Neurobehavioral Phenotypes: Stress, Addiction, Ageing and Metabolism
Yuan, T., Li, A., Sun, X., Ouyang, H., Campos, C., Rocha, N., Arias-Carrión, Ó., Machado, S. E. D. C., Hou, G., & So, K. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9526-2 · Cited by 46
Molecular insights into the transgenerational inheritance of stress memory
Zhang, Q., & Tian, Y. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.11.015 · Cited by 51
Paternal and maternal preconception urinary phthalate metabolite concentrations and child behavior
Messerlian, C., Bellinger, D. C., Mínguez‐Alarcón, L., Romano, M. E., Ford, J. B., Williams, P. L., Calafat, A. M., Hauser, R. B., & Braun, J. M. (2017) · Environmental Research · doi:10.1016/j.envres.2017.07.032 · Cited by 46
The Transmission of Intergenerational Epigenetic Information by Sperm microRNAs
Lee, G. S., & Conine, C. C. (2022) · Epigenomes · doi:10.3390/epigenomes6020012 · Cited by 47
Epididymal acquired sperm microRNAs modify post-fertilization embryonic gene expression
Trigg, N. A., & Conine, C. C. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114698 · Cited by 47
Infant circulating MicroRNAs as biomarkers of effect in fetal alcohol spectrum disorders
Mahnke, A. H., Sideridis, G. D., Salem, N. A., Tseng, A. M., Carter, R. C., Dodge, N. C., Rathod, A. B., Molteno, C. D., Meintjes, E. M., Jacobson, S. W., et al. (2021) · Scientific Reports · doi:10.1038/s41598-020-80734-y · Cited by 43
Evolutionary expansion of DNA hypomethylation in the mammalian germline genomePreprint
Qu, J., Hodges, E. C., Molaro, A., Gagneux, P., Dean, M. D., Hannon, G. J., & Smith, A. D. (2017) · Genome Research · doi:10.1101/gr.225896.117 · Cited by 46
Paternal adverse childhood experiences: Associations with infant DNA methylation
Merrill, S. M., Moore, S. R., Gladish, N., Giesbrecht, G. F., Dewey, D., Konwar, C., MacIssac, J. L., Kobor, M. S., & Letourneau, N. L. (2021) · Developmental Psychobiology · doi:10.1002/dev.22174 · Cited by 42
Paternal effects in a wild‐type zebrafish implicate a role of sperm‐derived small RNAs
Ord, J., Heath, P. R., Fazeli, A., & Watt, P. J. (2020) · Molecular Ecology · doi:10.1111/mec.15505 · Cited by 44
Transmission of the adverse consequences of childhood maltreatment across generations: Focus on gestational biology
Moog, N. K., Heim, C. C., Entringer, S., Simhan, H. N., Wadhwa, P. D., & Buß, C. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173372 · Cited by 49
Paternal overweight is associated with increased breast cancer risk in daughters in a mouse model
Fontelles, C. C., Carney, E., Clarke, J., Nguyen, N. M., Yin, C., Lu, J., Cruz, M. I., Ong, T. P., Hilakivi-Clarke, L. A., & de Assis, S. (2016) · Scientific Reports · doi:10.1038/srep28602 · Cited by 46
Review: Sperm–oocyte interactions and their implications for bull fertility, with emphasis on the ubiquitin–proteasome system
Šutovský, P. (2018) · animal · doi:10.1017/s1751731118000253 · Cited by 47
Mini-review: Epigenetic mechanisms that promote transgenerational actions of endocrine disrupting chemicals: Applications to behavioral neuroendocrinology
Martini, M., Corces, V. G., & Rissman, E. F. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104677 · Cited by 42
Adolescent binge-pattern alcohol exposure alters genome-wide DNA methylation patterns in the hypothalamus of alcohol-naïve male offspring
Asimes, A., Torcaso, A., Pinceti, E., Kim, C. K., Zeleznik‐Le, N. J., & Pak, T. R. (2016) · Alcohol · doi:10.1016/j.alcohol.2016.10.010 · Cited by 42
DNA methylation changes induced by BDE-209 are related to DNA damage response and germ cell development in GC-2spd
Li, X., Zhang, Y., Dong, X., Zhou, G., Sang, Y., Gao, L., Zhou, X., & Sun, Z. (2021) · Journal of Environmental Sciences · doi:10.1016/j.jes.2021.04.001 · Cited by 41

Authors: Rodgers, A. B., Morgan, C. P., Leu, N. A., & Bale, T. L.
Affiliations: University of Pennsylvania (US)
ORCID: Morgan, Christopher P.
Bale, Tracy L.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2015-10-19
Volume: 112
Issue: 44
Pages: 13699-13704
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1508347112
PMC: PMC4640733
OpenAlex: W1949928978
Cited by: 751
References: 48
Citations by year: 2026: 50 · 2025: 40 · 2024: 54 · 2023: 74 · 2022: 69 · 2021: 70 · 2020: 81 · 2019: 67 · 2018: 107 · 2017: 72 · 2016: 61 · 2015: 3
FWCI: 35.19
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.pnas.org/site/misc/userlicense.xhtml (vor, 183 d)
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: HHS | NIH | National Institute of Mental Health (MH073030, MH091258, MH087597, MH099910, MH104184)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords: sperm microRNA, paternal stress, chronic stress, hypothalamic-pituitary-adrenal axis, zygote microinjection, blood-brain barrier permeability, extracellular matrix, collagen, maternal mRNA degradation, SIRT1, chromatin remodeling, germ cells, single-cell transcriptomics
MeSH terms: Animals, Hypothalamo-Hypophyseal System, Male, Mice, Inbred C57BL, Spermatozoa, Stress, Physiological, Paternal Exposure, MicroRNAs, Epigenesis, Genetic, Mice, Transcriptome

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

Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks