The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.
The ageing systemic milieu negatively regulates neurogenesis and cognitive function
Open accessAbstract
In the central nervous system, ageing results in a precipitous decline in adult neural stem/progenitor cells and neurogenesis, with concomitant impairments in cognitive functions. Interestingly, such impairments can be ameliorated through systemic perturbations such as exercise. Here, using heterochronic parabiosis we show that blood-borne factors present in the systemic milieu can inhibit or promote adult neurogenesis in an age-dependent fashion in mice. Accordingly, exposing a young mouse to an old systemic environment or to plasma from old mice decreased synaptic plasticity, and impaired contextual fear conditioning and spatial learning and memory. We identify chemokines--including CCL11 (also known as eotaxin)--the plasma levels of which correlate with reduced neurogenesis in heterochronic parabionts and aged mice, and the levels of which are increased in the plasma and cerebrospinal fluid of healthy ageing humans. Lastly, increasing peripheral CCL11 chemokine levels in vivo in young mice decreased adult neurogenesis and impaired learning and memory. Together our data indicate that the decline in neurogenesis and cognitive impairments observed during ageing can be in part attributed to changes in blood-borne factors.
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In the citing paper
“Recent findings from parabiosis models (left) have shown that exposure to young blood restores neurogenesis, learning and memory and neuronal functions in older mice via increase in growth factors and endothelial remodeling in older mice(Baruch et al, 2014;Katsimpardi et al, 2014;Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“parabiosis experiments have demonstrated that the decline in neural and muscle stem cell function in old mice can be reversed by systemic factors from young mice”
From The Hallmarks of Aging (2013) · cites this paper as Villeda et al., 2011
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“the rejuvenation strategies based on the use of blood-borne systemic factors identified in parabiosis experiments (Conboy et al., 2005; Loffredo et al., 2013; Villeda et al., 2011).”
From The Hallmarks of Aging (2013) · cites this paper as Villeda et al., 2011
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Exposure to pro-aging circulating factors present in the blood of aged mice induces neuroinflammation and triggers age-related cognitive decline in young rodents27,28.”
From MT1-MMP inhibition rejuvenates ageing brain and rescues cognitive deficits in obesity (2025) · cites this paper as [27]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“CCL11 efficiently crosses the blood brain barrier56, has been implicated in neuroinflammatory disorders and SARS-CoV-2 (COVID-19) cognitive impairment57,58, and impairs neurogenesis54,58,59.”
From Senescent-like microglia limit remyelination through the senescence associated secretory phenotype (2025) · cites this paper as [54]
The cited source says what the claim attributes to it.
In the citing paper
“CCL11/Eotaxin1 is a chemokine that selectively recruits eosinophils, is elevated with age in humans and mice52–54, and has been shown to promote senescence55.”
From Senescent-like microglia limit remyelination through the senescence associated secretory phenotype (2025) · cites this paper as [54]
The cited source says what the claim attributes to it.
In the citing paper
“Excitingly, proof of principle exists for rejuvenation through blood-borne systemic factors (Conboy et al., 2005; Loffredo et al., 2013; Villeda et al., 2011).”
From The Hallmarks of Aging (2013) · cites this paper as Villeda et al., 2011
The cited source says what the claim attributes to it.
In the citing paper
“CCL11 (eotaxin) has been associated with lower neurogenesis and improper learning and memory in mice. 66”
From Three Tiers to biological escape velocity: The quest to outwit aging (2022) · cites this paper as [66]
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“and similarly, we did not see a difference in CCL11 [25].”
From Rejuvenation of three germ layers tissues by exchanging old blood plasma with saline-albumin (2020) · cites this paper as [25]
Experimental — accuracy not yet measuredIn the citing paper
“a chemokine whose serum and cerebrospinal fluid levels increase with age and correlate with reduced neurogenesis,40”
From Whole-genome sequencing suggests a chemokine gene cluster that modifies age at onset in familial Alzheimer's disease (2015) · cites this paper as [40]
In the citing paper
“In agreement with previous studies,40 eotaxin-1 levels increased with age in the total cohort.”
From Whole-genome sequencing suggests a chemokine gene cluster that modifies age at onset in familial Alzheimer's disease (2015) · cites this paper as [40]
In the citing paper
“Eotaxin-1 levels increase throughout life and this increase is correlated with reduced neurogenesis.40”
From Whole-genome sequencing suggests a chemokine gene cluster that modifies age at onset in familial Alzheimer's disease (2015) · cites this paper as [40]
In the citing paper
“Exposing a young mouse to plasma from old mice impairs synaptic plasticity, neurogenesis and cognition,310,311 suggesting that aged blood contributes to brain ageing.”
From Antiageing strategy for neurodegenerative diseases: from mechanisms to clinical advances (2025) · cites this paper as [310]
In the citing paper
“During ageing, the levels of pro-ageing factors such as C-C motif chemokine ligand 11 (CCL11) and β2-microglobulin (B2M) in the blood gradually increase, which damages synapse, neurogenesis and cognition.310,320,321”
From Antiageing strategy for neurodegenerative diseases: from mechanisms to clinical advances (2025) · cites this paper as [310]
In the citing paper
“These observations suggest that the SASP from peripheral blood negatively impacts neurogenesis and cognitive functions. 63”
From Senescence, brain inflammation, and oligomeric tau drive cognitive decline in Alzheimer's disease: Evidence from clinical and preclinical studies (2024) · cites this paper as [63]
In the citing paper
“This elevation of SASP components in AD patients correlates with CSF tau levels, inflammation, and cognitive impairment.”
From Senescence, brain inflammation, and oligomeric tau drive cognitive decline in Alzheimer's disease: Evidence from clinical and preclinical studies (2024) · cites this paper as [63]
In the citing paper
“Elevated CCL11 in the plasma and cerebrospinal fluid seen in aging mice and humans are associated with declining neurogenesis, neurodegenerative disease, and cognitive decline and may contribute to driving neovascularisation in AMD via interaction with CCR3 [1, 93, 123].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [123]
In the citing paper
“Elevated CCL11 in the plasma and cerebrospinal fluid seen in aging mice and humans are associated with declining neurogenesis, neurodegenerative disease, and cognitive decline and may contribute to driving neovascularisation in AMD via interaction with CCR3 [1, 93, 123].”
From Fecal microbiota transfer between young and aged mice reverses hallmarks of the aging gut, eye, and brain (2022) · cites this paper as [123]
In the citing paper
“This surgical intervention also enhances rates of neurogenesis, remyelination and other measures of neural function in the old parabiont, suggesting that changes in stem cell function in the aging central nervous system are also affected by blood-borne factors165–167.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [165]
In the citing paper
“This surgical intervention also enhances rates of neurogenesis, remyelination and other measures of neural function in the old parabiont, suggesting that changes in stem cell function in the aging central nervous system are also affected by blood-borne factors165–167.”
From Stem cell aging: mechanisms, regulators and therapeutic opportunities (2014) · cites this paper as [165]
In the citing paper
“Elevated circulating cytokine/chemokine levels, particularly CCL11, can also limit neurogenesis and contribute to cognitive impairment (Villeda et al., 2011).”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Villeda et al., 2011
In the citing paper
“Elevated levels of CCL11 found in mice after respiratory infection with either SARS-CoV-2 or H1N1 influenza, and in humans with cognitive symptoms after COVID, can cause deficient hippocampal neurogenesis as shown here and previously (Villeda et al., 2011), and induces microglial reactivity specifically in the hippocampus.”
From Mild respiratory COVID can cause multi-lineage neural cell and myelin dysregulation (2022) · cites this paper as Villeda et al., 2011
In the citing paper
“including the demonstration that plasma infusions alone are sufficient to exert these effects,65,69”
From Asynchronous, contagious and digital aging (2021) · cites this paper as [65]
In the citing paper
“Based on early work from our laboratories that ushered in a new era of the use of the technique of parabiosis in aging research, it is clear that systemic factors originating from distant tissues in the body are able to either promote or reverse cell and tissue aging phenotypes.63,64,65”
From Asynchronous, contagious and digital aging (2021) · cites this paper as [65]
In the citing paper
“blood factors that can influence NSC ageing and rejuvenation include inflammatory cytokines (for example, CXCL11) (likely circulating in the blood), circulating enzymes produced by the liver and complement factors (likely circulating in the blood146–148)”
From Ageing and rejuvenation of tissue stem cells and their niches (2023) · cites this paper as [148]
In the citing paper
“Conversely, younger mice heterochronically paired with older mice showed reduced cell proliferation in the dentate gyrus and impaired neurogenesis.”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“Additional evidence for the role of blood-borne systemic factors in aging-induced impairments was provided by Villeda et al (2011) who showed that older mice that share a blood supply with younger mice show increased neurogenesis, enhanced LTP and improved cognitive functioning.”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“In particular, aging-associated increase in systemic levels of CCL11 was associated with impaired neurogenesis and learning deficits, which were reversed by systemic and intrahippocampal administration of neutralizing anti-CCL11 antibody in the aged mice (Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“Furthermore, plasma transfer from younger mice into the aged was sufficient to replicate the findings from the parabiosis experiments, elucidating the role of blood-borne soluble factors, and not blood cells, in reversing aging-associated impairments in the brain (Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“Recent findings from parabiosis models (left) have shown that exposure to young blood restores neurogenesis, learning and memory and neuronal functions in older mice via increase in growth factors and endothelial remodeling in older mice(Baruch et al, 2014;Katsimpardi et al, 2014;Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“Recent findings from parabiosis models (left) have shown that exposure to young blood restores neurogenesis, learning and memory and neuronal functions in older mice via increase in growth factors and endothelial remodeling in older mice(Baruch et al, 2014;Katsimpardi et al, 2014;Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
In the citing paper
“Recent findings from parabiosis models (left) have shown that exposure to young blood restores neurogenesis, learning and memory and neuronal functions in older mice via increase in growth factors and endothelial remodeling in older mice(Baruch et al, 2014;Katsimpardi et al, 2014;Villeda et al, 2011).”
From Microglia Priming with Aging and Stress (2017) · cites this paper as Villeda et al, 2011
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Citations
Cites
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566
Gage, F. H. (2000) · Science · doi:10.1126/science.287.5457.1433 · Cited by 4,786
Mechanisms and Functional Implications of Adult Neurogenesis
Zhao, C., Deng, W., & Gage, F. H. (2008) · Cell · doi:10.1016/j.cell.2008.01.033 · Cited by 3,007
Functional neurogenesis in the adult hippocampus
van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., & Gage, F. H. (2002) · Nature · doi:10.1038/4151030a · Cited by 2,853
Inflammatory Blockade Restores Adult Hippocampal Neurogenesis
Monje, M. L., Toda, H., & Palmer, T. D. (2003) · Science · doi:10.1126/science.1088417 · Cited by 2,426
Rejuvenation of aged progenitor cells by exposure to a young systemic environment
Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., & Rando, T. A. (2005) · Nature · doi:10.1038/nature03260 · Cited by 2,287
Self-citationNew neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?
Deng, W., Aimone, J. B., & Gage, F. H. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2822 · Cited by 2,120
Exercise enhances learning and hippocampal neurogenesis in aged mice
van Praag, H., Shubert, T., Zhao, C., & Gage, F. H. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1731-05.2005 · Cited by 2,078
Local self-renewal can sustain CNS microglia maintenance and function throughout adult life
Ajami, B., Bennett, J. L., Krieger, C., Tetzlaff, W., & Rossi, F. M. V. (2007) · Nature Neuroscience · doi:10.1038/nn2014 · Cited by 1,643
A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation
Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., Jessberger, S., Saksida, L. M., Barker, R. A., Gage, F. H., et al. (2009) · Science · doi:10.1126/science.1173215 · Cited by 1,642
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Cantero‐Fortiz, Y., & Boada, M. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1439125 · Cited by 34
Stem Cells as Vehicles for Youthful Regeneration of Aged Tissues
Rando, T. A., & Wyss‐Coray, T. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu043 · Cited by 34
Self-citationAntisenescence effect of mouse embryonic stem cell conditioned medium through a PDGF/FGF pathway
Bae, Y., Choi, J. H., Nagy, A., Sung, H., & Kim, J. (2015) · The FASEB Journal · doi:10.1096/fj.15-278846 · Cited by 34
Ma, Y., Liu, Y., Han, F., Qiu, H., Shi, J., Huang, N., Hou, N., & Sun, X. (2021) · Aging · doi:10.18632/aging.202881 · Cited by 33
Gillotin, S., Sahni, V., Lepko, T., Hanspal, M. A., Swartz, J., Alexopoulou, Z., & Marshall, F. H. (2021) · Ageing Research Reviews · doi:10.1016/j.arr.2021.101447 · Cited by 34
Exposure to widespread drinking water chemicals, blood inflammation markers, and colorectal cancer
Villanueva, C. M., Espinosa, A., Gràcia‐Lavedan, E., Vlaanderen, J. J., Vermeulen, R. C. H., Molina, A. J., Amiano, P., Gómez‐Acebo, I., Castaño‐Vinyals, G., Vineis, P., et al. (2021) · Environment International · doi:10.1016/j.envint.2021.106873 · Cited by 34
Kao, J., & Frankland, P. W. (2022) · Cell · doi:10.1016/j.cell.2022.06.020 · Cited by 34
The Effects of Extrinsic and Intrinsic Factors on Neurogenesis
Jiang, M. H., Jang, S. E., & Zeng, L. (2023) · Cells · doi:10.3390/cells12091285 · Cited by 34
Giloteaux, L., Li, J., Hornig, M., Lipkin, W. I., Ruppert, D., & Hanson, M. R. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04179-3 · Cited by 34
Aging of Stem and Progenitor Cells: Mechanisms, Impact on Therapeutic Potential, and Rejuvenation
Nurković, J., Volarević, V., Lako, M., Armstrong, L., Arsenijević, N., & Stojković, M. (2015) · Rejuvenation Research · doi:10.1089/rej.2015.1676 · Cited by 34
The systemic milieu as a mediator of dietary influence on stem cell function during ageing
Murphy, T., & Thuret, S. (2014) · Ageing Research Reviews · doi:10.1016/j.arr.2014.11.004 · Cited by 34
Aging, metabolism and stem cells: Spotlight on muscle stem cells
García-Prat, L., & Muñoz-Cánoves, P. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.021 · Cited by 34
CCL11 promotes migration and proliferation of mouse neural progenitor cells
Wang, F., Baba, N., Shen, Y., Yamashita, T., Tsuru, E., Tsuda, M., Maeda, N., & Sagara, Y. (2017) · Stem Cell Research & Therapy · doi:10.1186/s13287-017-0474-9 · Cited by 34
Yang, R., Fu, S., Zhao, L., Zhen, B., Ye, L., Niu, X., Li, X., Zhang, P., & Bai, J. (2017) · Clinical Science · doi:10.1042/cs20171028 · Cited by 34
Magalhaes, P. V. S., Jansen, K., Stertz, L., Ferrari, P., Pinheiro, R. T., da Silva, R. A., & Kapczinski, F. (2014) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.10.007 · Cited by 33
Modeling motor neuron disease: the matter of time
Arbab, M., Baars, S., & Geijsen, N. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.07.008 · Cited by 33
Chronic traumatic encephalopathy: Diagnostic updates and advances
Pierre, K., Molina, V., Shukla, S., Avila, A., Fong, N., Nguyen, J., & Lucke-Wold, B. P. (2022) · AIMS neuroscience · doi:10.3934/neuroscience.2022030 · Cited by 33
Aging as a loss of morphostatic information: A developmental bioelectricity perspective
Pio‐Lopez, L., & Levin, M. G. (2024) · Ageing Research Reviews · doi:10.1016/j.arr.2024.102310 · Cited by 36
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Blanc, R. S., Shah, N., Hachmer, S., Salama, N., Meng, F. W., Mousaei, A., Puri, G., Hwang, J. H., Wacker, E. E., Yang, B. A., et al. (2025) · Nature Aging · doi:10.1038/s43587-025-00902-5 · Cited by 35
Huang, J., Yang, G., Xiong, X., Wang, M., Yuan, J., Zhang, Q., Gong, C., Qiu, Z., Meng, Z., Xu, R., et al. (2020) · Aging and Disease · doi:10.14336/ad.2019.1229 · Cited by 33
Yegla, B., Boles, J. S., Kumar, A., & Foster, T. C. (2021) · Glia · doi:10.1002/glia.23975 · Cited by 33
Almulla, A. F., Al-Rawi, K. F., Maes, M. H. J., & Al‐Hakeim, H. K. (2021) · Journal of Affective Disorders · doi:10.1016/j.jad.2021.03.062 · Cited by 33
Mamtilahun, M., Jiang, L., Song, Y., Shi, X., Liu, C., Jiang, Y., Deng, L., Zheng, H., Shen, H., Li, Y., et al. (2021) · Stroke and Vascular Neurology · doi:10.1136/svn-2020-000774 · Cited by 33
He, J., Liu, T., Li, Y., Mi, X., Han, D., Yang, N., Chen, L., Li, Y., Hong, J., Kuang, C., et al. (2021) · International Immunopharmacology · doi:10.1016/j.intimp.2021.107962 · Cited by 33
Kim, D., Kyung, J., Park, D., Choi, E., Kim, K. S., Shin, K., Lee, H., Shin, I. S., Kang, S. K., Ra, J. C., et al. (2015) · Stem Cells Translational Medicine · doi:10.5966/sctm.2015-0011 · Cited by 33
Time limited immunomodulatory functions of transplanted neural precursor cells
Fainstein, N., Einstein, O., Cohen, M. E., Brill, L., Lavon, I., & Ben‐Hur, T. (2012) · Glia · doi:10.1002/glia.22420 · Cited by 33
Berg, D. A., Yoon, K., Will, B., Xiao, A. Y., Kim, N.-S., Christian, K. M., Song, H., & Ming, G. (2015) · Frontiers in Biology · doi:10.1007/s11515-015-1364-0 · Cited by 33
CCL 11‐induced eosinophils inhibit the formation of blood vessels and cause tumor necrosis
Xing, Y., Tian, Y., Kurosawa, T., Matsui, S., Touma, M., Yanai, T., Wu, Q., & Sugimoto, K. (2016) · Genes to Cells · doi:10.1111/gtc.12371 · Cited by 33
Distinct roles for hyaluronan in neural stem cell niches and perineuronal nets
Su, W., Matsumoto, S. G., Sorg, B. A., & Sherman, L. S. (2018) · Matrix Biology · doi:10.1016/j.matbio.2018.01.022 · Cited by 33
Kynurenic acid accumulation underlies learning and memory impairment associated with agingPreprint
Vohra, M., Lemieux, G. A., Lin, L., & Ashrafi, K. (2018) · Genes & Development · doi:10.1101/gad.307918.117 · Cited by 33
Blood biomarkers for assessment of mild traumatic brain injury and chronic traumatic encephalopathy
Hiskens, M. I., Schneiders, A. G., Angoa-Pérez, M., Vella, R. K., & Fenning, A. S. (2020) · Biomarkers · doi:10.1080/1354750x.2020.1735521 · Cited by 32
Enhanced Ccl2-Ccr2 signaling drives more severe choroidal neovascularization with aging
Robbie, S. J., Georgiadis, A., Barker, S. E., Durán, Y., Smith, A. J., Ali, R. R., Luhmann, U. F. O., & Bainbridge, J. W. (2016) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2015.12.019 · Cited by 32
Lack of association between blood donor age and survival of transfused patients
Vasan, S. K., Chiesa, F., Rostgaard, K., Magnusson, P. K. E., Halmin, M., Nielsen, K. R., Titlestad, K. E., Hjalgrim, H., & Edgren, G. (2015) · Blood · doi:10.1182/blood-2015-11-683862 · Cited by 32
Therapeutic potential of systemic brain rejuvenation strategies for neurodegenerative disease
Horowitz, A. M., & Villeda, S. (2017) · F1000Research · doi:10.12688/f1000research.11437.1 · Cited by 32
Self-citationPerinatal Micro-Bleeds and Neuroinflammation in E19 Rat Fetuses Exposed to Utero-Placental Ischemia
Giambrone, A. B., Logue, O. C., Shao, Q., Bidwell, G. L., & Warrington, J. P. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20164051 · Cited by 32
Serre-Miranda, C., Roque, S., Santos, N. C., Costa, P., Sousa, N., Palha, J. A., & Correia‐Neves, M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02045 · Cited by 32
Hiskens, M. I., Schneiders, A. G., Vella, R. K., & Fenning, A. S. (2021) · PLoS ONE · doi:10.1371/journal.pone.0251315 · Cited by 32
Sanchez-Molina, P., Almolda, B., Giménez‐Llort, L., González, B., & Castellano, B. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.12.026 · Cited by 32
Predicting progression to Alzheimer’s disease with human hippocampal progenitors exposed to serum
Maruszak, A., Silajdžić, E., Lee, H.-A., Murphy, T., Liu, B., Shi, L., de Lucia, C., Douiri, A., Salta, E., Nevado‐Holgado, A. J., et al. (2022) · Brain · doi:10.1093/brain/awac472 · Cited by 32
Nutritional factors and aging in demyelinating diseases
Adamo, A. M. (2013) · Genes & Nutrition · doi:10.1007/s12263-013-0360-8 · Cited by 32
Shahaduzzaman, M., Golden, J. E., Green, S., Gronda, A. E., Adrien, E., Ahmed, A., Sanberg, P. R., Bickford, P. C., Gemma, C., & Willing, A. E. (2012) · AGE · doi:10.1007/s11357-012-9496-5 · Cited by 32
A Common Language: How Neuroimmunological Cross Talk Regulates Adult Hippocampal Neurogenesis
Leiter, O., Kempermann, G., & Walker, T. L. (2016) · Stem Cells International · doi:10.1155/2016/1681590 · Cited by 32
Priming of the Cells: Hypoxic Preconditioning for Stem Cell Therapy.
Wei, Z. Z., Zhu, Y., Zhang, J. Y., McCrary, M. R., Wang, S., Zhang, Y., Yu, S., & Wei, L. (2017) · PubMed Central · doi:10.4103/0366-6999.215324 · Cited by 32
Miller‐Rhodes, P., Kong, C., Baht, G. S., Saminathan, P., Rodriguiz, R. M., Wetsel, W. C., Gelbard, H. A., & Terrando, N. (2019) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1582-5 · Cited by 33
Nutrition and microRNAs: Novel Insights to Fight Sarcopenia
Barbiera, A., Pelosi, L., Sica, G., & Scicchitano, B. M. (2020) · Antioxidants · doi:10.3390/antiox9100951 · Cited by 32
Dluzen, D. F., Noren Hooten, N., & Evans, M. K. (2017) · WIREs RNA · doi:10.1002/wrna.1385 · Cited by 31
The aged hematopoietic system promotes hippocampal‐dependent cognitive decline
Smith, L. K., Verovskaya, E., Bieri, G., Horowitz, A. M., von Ungern‐Sternberg, S. N. I., Lin, K., Seizer, P., Passegué, E., & Villeda, S. A. (2020) · Aging Cell · doi:10.1111/acel.13192 · Cited by 31
Self-citationMüller, L., & Benedetto, S. D. (2023) · Immunity & Ageing · doi:10.1186/s12979-023-00341-z · Cited by 31
Body-wide multi-omic counteraction of aging with GLP-1R agonism
Huang, J., Kwok, A. J., Li, J. C. Y., Chiu, C. L. H., Ip, B. Y. M., Tung, L. Y., Chan, R. C. H., Chan, D. T.-M., Wang, Z., Zheng, X., et al. (2025) · Cell Metabolism · doi:10.1016/j.cmet.2025.10.014 · Cited by 31
Hisamatsu, D., Ohno‐Oishi, M., Nakamura, S., Mabuchi, Y., & Naka-Kaneda, H. (2016) · Aging · doi:10.18632/aging.100982 · Cited by 31
Takayama, K., Kawakami, Y., Lavasani, M., Mu, X., Cummins, J. H., Yurube, T., Kuroda, R., Kurosaka, M., Fu, F. H., Robbins, P. D., et al. (2016) · Journal of Orthopaedic Research® · doi:10.1002/jor.23409 · Cited by 31
Aging Systemic Milieu Impairs Outcome after Ischemic Stroke in Rats
Pan, M., Wang, P., Zheng, C., Zhang, H., Lin, S., Shao, B., Zhuge, Q., & Jin, K. (2017) · Aging and Disease · doi:10.14336/ad.2017.0710 · Cited by 31
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Schwartz, M., Ramos, J. M. P., & Ben-Yehuda, H. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1900844 · Cited by 31
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Liu, J., van Beusekom, H. M. M., Bu, X., Chen, G., Rosado-de-Castro, P. H., Chen, X., Chen, X., Clarkson, A. N., Farr, T. D., Fu, Y., et al. (2023) · Neuroprotection/Neuroprotection (Chichester, England. Print) · doi:10.1002/nep3.23 · Cited by 32
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Gao, N., Wang, Y., Zheng, C., Gao, Y., Li, H., Li, Y., Fu, T., Xu, L., Wang, W., Ying, S., et al. (2017) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00516.2016 · Cited by 31
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Castellano, J. M., Palner, M., Li, S., Freeman, G. M., Nguyen, A., Shen, B., Stan, T. M., Mosher, K. I., Chin, F. T., de Lecea, L., et al. (2016) · Scientific Reports · doi:10.1038/srep29015 · Cited by 29
Self-citationEndogenous neural precursor cells in health and disease
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Yang, J., Kong, C., Jia, L., Li, T., Quan, M., Li, Y., Lyu, D., Li, F., Jin, H., Li, Y., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00845-0 · Cited by 29
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Scabia, G., Testa, G., Scali, M., Turco, S. D., Desiato, G., Berardi, N., Sale, A., Matteoli, M., Maffei, L., Maffei, M., et al. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.08.222 · Cited by 29
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Zocher, S., & Toda, T. (2023) · Hippocampus · doi:10.1002/hipo.23494 · Cited by 29
Huang, Y., Ma, Y., Gao, P., Wang, Z., Huang, L., Hou, J., Tan, L., & Yu, J. (2023) · Alzheimer s Research & Therapy · doi:10.1186/s13195-023-01217-6 · Cited by 29
Sayec, M. L., Carregosa, D., Khalifa, K. N., de Lucia, C., Aarsland, D., dos Santos, C. N., & Rodriguez‐Mateos, A. (2023) · Food & Function · doi:10.1039/d3fo01913f · Cited by 29
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Hippocampal Neurogenesis and Ageing
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Self-citation
Metadata
- Authors
- Villeda, S. A., Luo, J., Mosher, K. I., Zou, B., Britschgi, M., Bieri, G., Stan, T. M., Fainberg, N., Ding, Z., Eggel, A., Lucin, K. M., Czirr, E., Park, J.-S., Couillard-Després, S., Aigner, L., Li, G., Peskind, E. R., Kaye, J. A., Quinn, J. F., Galasko, D. R., Xie, X. S., Rando, T. A., & Wyss-Coray, T.
- Affiliations
- Stanford Medicine (US)
- AfaSci (United States) (US)
- Paracelsus Medical University (AT)
- University of Washington (US)
- Oregon Health & Science University (US)
- University of California San Diego (US)
- VA Palo Alto Health Care System (US)
- ORCID
- Venue
- Nature
- Published
- 2011-08-31
- Volume
- 477
- Issue
- 7362
- Pages
- 90-94
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3170097
- OpenAlex
- W1969905245
- Cited by
- 1,763
- References
- 33
- Citations by year
- 2026: 74 · 2025: 110 · 2024: 118 · 2023: 142 · 2022: 159 · 2021: 135 · 2020: 146 · 2019: 109 · 2018: 117 · 2017: 117 · 2016: 127 · 2015: 116 · 2014: 100 · 2013: 100 · 2012: 81
- FWCI
- 30.59
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institutes of Health (DP1OD000392)
- National Institute on Aging (P30 AG 08017, R01AG027505, P30AG008017, P50AG005136, F31AG034045)
- National Institute of Mental Health (R01MH078194)
- National Institute of Allergy and Infectious Diseases (T32AI007290)
- National Institute of Neurological Disorders and Stroke (F31NS066676)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR056849)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- aging, adult neurogenesis, cognitive decline, heterochronic parabiosis, blood-borne factors, eotaxin, chemokines, beta2-microglobulin, neural stem/progenitor cells, synaptic plasticity, learning and memory, plasma proteomics, cerebrospinal fluid
- MeSH terms
- Aging, Animals, Female, Learning, Learning Disabilities, Male, Memory Disorders, Mice, Inbred C57BL, Parabiosis, Plasma, Time Factors, Chemokines, Mice, Chemokine CCL11, Neurogenesis
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