Cited by 145

The DOI matches its Crossref record; 28 of the 28 references it cites were found in a registry or an index.

A toolbox for the longitudinal assessment of healthspan in aging mice

Bellantuono, I., de Cabo, R., Ehninger, D., Di Germanio, C., Lawrie, A., Miller, J., Mitchell, S. J., Navas-Enamorado, I., Potter, P. K., Tchkonia, T., Trejo, J. L., Lamming, D. W.·2020·Nature Protocols

Overview

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41596-019-0256-1

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Verification

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • TAC-treated aged mice showed improved rotarod performance and grip strength.

    “In addition, TAC-treated aged mice showed improved rotarod performance and grip strength (Figures S5H and S5I, respectively), which are known to decline with advancing age,40 consistent with improved motor coordination and muscle strength.”

Self-check

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

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

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 105

  1. Bellantuono, I. Find drugs that delay many diseases of old age. Nature 554, 293–295 (2018). · DOI
  2. Arriola Apelo, S. I., Pumper, C. P., Baar, E. L., Cummings, N. E. & Lamming, D. W. Intermittent administration of rapamycin extends the life span of female C57BL/6J mice. J. Gerontol. A Biol. Sci. Med. Sci. 71, 876–881 (2016). · DOI
  3. Richardson, A. et al. Measures of healthspan as indices of aging in mice-a recommendation. J. Gerontol. A Biol. Sci. Med. Sci. 71, 427–430 (2016). · DOI · Paper page
  4. Kane, A. E., Keller, K. M., Heinze-Milne, S., Grandy, S. A. & Howlett, S. E. A murine frailty index based on clinical and laboratory measurements: links between frailty and pro-inflammatory cytokines differ in a sex-specific manner. J. Gerontol. A Biol. Sci. Med. Sci. 74, 275–282 (2019). · DOI
  5. Whitehead, J. C. et al. A clinical frailty index in aging mice: comparisons with frailty index data in humans. J. Gerontol. A Biol. Sci. Med. Sci. 69, 621–632 (2014). · DOI
  6. Hamm, R. J., Pike, B. R., O’Dell, D. M., Lyeth, B. G. & Jenkins, L. W. The rotarod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J. Neurotrauma 11, 187–196 (1994). · DOI
  7. Wolff, B. S., Raheem, S. A. & Saligan, L. N. Comparing passive measures of fatigue-like behavior in mice. Sci. Rep. 8, 14238 (2018).
  8. Schafer, M. J. et al. Exercise prevents diet-induced cellular senescence in adipose tissue. Diabetes 65, 1606–1615 (2016). · DOI · Paper page
  9. Halldorsdottir, S., Carmody, J., Boozer, C. N., Leduc, C. A. & Leibel, R. L. Reproducibility and accuracy of body composition assessments in mice by dual energy x-ray absorptiometry and time domain nuclear magnetic resonance. Int. J. Body Compos. Res. 7, 147–154 (2009).
  10. Potter, P. K. et al. Novel gene function revealed by mouse mutagenesis screens for models of age-related disease. Nat. Commun. 7, 12444 (2016). · DOI
  11. Xie, K. et al. Epigenetic alterations in longevity regulators, reduced life span, and exacerbated aging-related pathology in old father offspring mice. Proc. Natl Acad. Sci. USA 115, E2348–E2357 (2018). · DOI
  12. Lamming, D. W. et al. Young and old genetically heterogeneous HET3 mice on a rapamycin diet are glucose intolerant but insulin sensitive. Aging Cell 12, 712–718 (2013). · DOI
  13. Lamming, D. W. et al. Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335, 1638–1643 (2012). · DOI · Paper page
  14. Stout, M. B. et al. 17alpha-Estradiol alleviates age-related metabolic and inflammatory dysfunction in male mice without inducing feminization. J. Gerontol. A Biol. Sci. Med. Sci. 72, 3–15 (2017). · DOI · Paper page
  15. Diaz-Ruiz, A. et al.Overexpression of CYB5R3 and NQO1, two NAD(+) -producing enzymes, mimics aspects of caloric restriction. Aging Cell, e12767 (2018). · DOI
  16. Allard, J. S. et al. Prolonged metformin treatment leads to reduced transcription of Nrf2 and neurotrophic factors without cognitive impairment in older C57BL/6J mice. Behav. Brain. Res. 301, 1–9 (2016). · DOI · Paper page
  17. Lee, S. et al. Assessment of cognitive impairment in a mouse model of high-fat diet-induced metabolic stress with touchscreen-based automated battery system. Exp. Neurobiol. 27, 277–286 (2018). · DOI
  18. Benice, T. S. & Raber, J. Object recognition analysis in mice using nose-point digital video tracking. J. Neurosci. Methods 168, 422–430 (2008). · DOI
  19. Bettis, T. & Jacobs, L. F. Sex differences in object recognition are modulated by object similarity. Behav. Brain Res. 233, 288–292 (2012). · DOI
  20. McCullough, L. D., McCarthy, M. M. & de Vries, G. J. NIH policy: status quo is also costly. Nature 510, 340 (2014). · DOI
  21. Brooks, S. P., Pask, T., Jones, L. & Dunnett, S. B. Behavioural profiles of inbred mouse strains used as transgenic backgrounds. II: Cogn. tests. Genes Brain Behav. 4, 307–317 (2005).
  22. Feridooni, H. A., Sun, M. H., Rockwood, K. & Howlett, S. E. Reliability of a frailty index based on the clinical assessment of health deficits in male C57BL/6J mice. J. Gerontol. A Biol. Sci. Med. Sci. 70, 686–693 (2015). · DOI
  23. Sukoff Rizzo, S. J. et al. Assessing healthspan and lifespan measures in aging mice: optimization of testing protocols, replicability, and rater reliability. Curr. Protoc. Mouse Biol. 8, e45 (2018). · DOI
  24. Palmer, A. K. et al. Targeting senescent cells alleviates obesity-induced metabolic dysfunction. Aging Cell, e12950 (2019). · DOI · Paper page
  25. Cummings, N. E. et al. Restoration of metabolic health by decreased consumption of branched-chain amino acids. J. Physiol. 596, 623–645 (2018). · DOI
  26. Xie, K. et al. Every-other-day feeding extends lifespan but fails to delay many symptoms of aging in mice. Nat. Commun. 8, 155 (2017).
  27. McGreevy, K. R. et al. Intergenerational transmission of the positive effects of physical exercise on brain and cognition. Proc. Natl Acad. Sci. USA (2019). · DOI
  28. Lamming, D. W. et al. Depletion of Rictor, an essential protein component of mTORC2, decreases male lifespan. Aging Cell 13, 911–917 (2014). · DOI · Paper page
  29. Yousefzadeh, M. J. et al. Fisetin is a senotherapeutic that extends health and lifespan. EbioMedicine 36, 18–28 (2018). · DOI · Paper page
  30. Mercken, E. M. et al. SRT2104 extends survival of male mice on a standard diet and preserves bone and muscle mass. Aging Cell 13, 787–796 (2014). · DOI
  31. Mitchell, S. J. et al. The SIRT1 activator SRT1720 extends lifespan and improves health of mice fed a standard diet. Cell Rep. 6, 836–843 (2014). · DOI
  32. Minor, R. K. et al. SRT1720 improves survival and healthspan of obese mice. Sci. Rep. 1, 70 (2011). · DOI
  33. Kane, A. E. et al. Impact of longevity interventions on a validated mouse clinical frailty index. J. Gerontol. A Biol. Sci. Med. Sci. 71, 333–339 (2016). · DOI
  34. Kane, A. E. et al. A comparison of two mouse frailty assessment tools. J. Gerontol. A Biol. Sci. Med. Sci. 72, 904–909 (2017). · DOI
  35. Yu, D. et al. Short-term methionine deprivation improves metabolic health via sexually dimorphic, mTORC1-independent mechanisms. FASEB J. 32, 3471–3482 (2018). · DOI
  36. Darcy, J. et al. Increased environmental temperature normalizes energy metabolism outputs between normal and Ames dwarf mice. Aging 10, 2709–2722 (2018). · DOI
  37. Cohen, D. E., Supinski, A. M., Bonkowski, M. S., Donmez, G. & Guarente, L. P. Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction. Genes Dev. 23, 2812–2817 (2009). · DOI
  38. Bitto, A. et al. Transient rapamycin treatment can increase lifespan and healthspan in middle-aged mice. eLife 5, https://doi.org/10.7554/eLife.16351 (2016). · DOI · Paper page
  39. Chen, C., Liu, Y., Liu, Y. & Zheng, P. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci. Signal 2, ra75 (2009).
  40. Dai, D. F. et al. Altered proteome turnover and remodeling by short-term caloric restriction or rapamycin rejuvenate the aging heart. Aging Cell 13, 529–539 (2014). · DOI
  41. Flynn, J. M. et al. Late-life rapamycin treatment reverses age-related heart dysfunction. Aging Cell 12, 851–862 (2013). · DOI
  42. Hou, Y. et al. NAD+ supplementation normalizes key Alzheimer’s features and DNA damage responses in a new AD mouse model with introduced DNA repair deficiency. Proc. Natl Acad. Sci. USA 115, E1876–E1885 (2018). · DOI · Paper page
  43. Fontana, L., Kennedy, B. K., Longo, V. D., Seals, D. & Melov, S. Medical research: treat ageing. Nature 511, 405–407 (2014). · DOI
  44. Mitchell, S. J. et al. Daily fasting improves health and survival in male mice independent of diet composition and calories. Cell Metab. 29, 221–228 e223 (2019). · DOI
  45. Wilkinson, J. E. et al. Rapamycin slows aging in mice. Aging Cell 11, 675–682 (2012). · DOI · Paper page
  46. Turturro, A. et al. Growth curves and survival characteristics of the animals used in the Biomarkers of Aging Program. J. Gerontol. A Biol. Sci. Med. Sci. 54, B492–501 (1999). · DOI
  47. Dumas, S. N. & Lamming, D. W. Next generation strategies for geroprotection via mTORC1 inhibition. J. Gerontol. A Biol. Sci. Med. Sci., https://doi.org/10.1093/gerona/glz056 (2019). · DOI
  48. Harrison, D. E. et al. Acarbose, 17-alpha-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell 13, 273–282 (2014). · DOI · Paper page
  49. Lamming, D. W. Diminished mTOR signaling: a common mode of action for endocrine longevity factors. SpringerPlus 3, 735 (2014). · DOI · Paper page
  50. Miller, R. A. et al. Rapamycin-mediated lifespan increase in mice is dose and sex dependent and metabolically distinct from dietary restriction. Aging Cell 13, 468–477 (2014). · DOI
  51. Fontana, L. et al. Decreased consumption of branched-chain amino acids improves metabolic health. Cell Rep. 16, 520–530 (2016). · DOI · Paper page
  52. De Leon, E. R. et al. Age-dependent protection of insulin secretion in diet induced obese mice. Sci. Rep. 8, 17814 (2018). · DOI
  53. Graber, T. G., Ferguson-Stegall, L., Liu, H. & Thompson, L. V. Voluntary aerobic exercise reverses frailty in old mice. J. Gerontol. A Biol. Sci. Med. Sci. 70, 1045–1058 (2015). · DOI
  54. Chellappa, K. et al. Hypothalamic mTORC2 is essential for metabolic health and longevity. Aging Cell 18, e13014 (2019). · DOI · Paper page
  55. Yu, D. et al. Calorie-restriction-induced insulin sensitivity is mediated by adipose mTORC2 and not required for lifespan extension. Cell Rep. 29, 236–248.e3 (2019). · DOI · Paper page
  56. Nadon, N. L., Strong, R., Miller, R. A. & Harrison, D. E. NIA interventions testing program: investigating putative aging intervention agents in a genetically heterogeneous mouse model. EbioMedicine 21, 3–4 (2017). · DOI
  57. Ryan, D. P. et al. A paternal methyl donor-rich diet altered cognitive and neural functions in offspring mice. Mol. Psychiatry 23, 1345–1355 (2018). · DOI
  58. Fernandez-Twinn, D. S., Constancia, M. & Ozanne, S. E. Intergenerational epigenetic inheritance in models of developmental programming of adult disease. Semin. Cell Dev. Biol. 43, 85–95 (2015). · DOI
  59. Martin-Gronert, M. S. & Ozanne, S. E. Early life programming of obesity. Med. Wieku Rozwoj. 17, 7–12 (2013).
  60. Menting, M. D. et al. Maternal obesity in pregnancy impacts offspring cardiometabolic health: Systematic review and meta-analysis of animal studies. Obes. Rev. 20, 675–685 (2019). · DOI
  61. Dearden, L., Bouret, S. G. & Ozanne, S. E. Sex and gender differences in developmental programming of metabolism. Mol. Metab. 15, 8–19 (2018). · DOI
  62. Evered, L., Scott, D. A. & Silbert, B. Cognitive decline associated with anesthesia and surgery in the elderly: does this contribute to dementia prevalence? Curr. Opin. Psychiatry 30, 220–226 (2017). · DOI
  63. Schulte, P. J. et al. Association between exposure to anaesthesia and surgery and long-term cognitive trajectories in older adults: report from the Mayo Clinic Study of Aging. Br. J. Anaesth. 121, 398–405 (2018). · DOI
  64. Steinmetz, J. & Rasmussen, L. S. Anesthesia and the risk of dementia in the elderly. Presse Med. 47, e45–e51 (2018). · DOI
  65. Butterfield, N. N., Graf, P., Ries, C. R. & MacLeod, B. A. The effect of repeated isoflurane anesthesia on spatial and psychomotor performance in young and aged mice. Anesth. Analg. 98, 1305–1311 (2004). · DOI
  66. Xu, H. et al. Smaller sized inhaled anesthetics have more potency on senescence-accelerated prone-8 mice compared with senescence-resistant-1 mice. J. Alzheimers Dis. 39, 29–34 (2014). · DOI
  67. Li, X. M. et al. Disruption of hippocampal neuregulin 1-ErbB4 signaling contributes to the hippocampus-dependent cognitive impairment induced by isoflurane in aged mice. Anesthesiology 121, 79–88 (2014). · DOI
  68. Li, R. L. et al. Postoperative impairment of cognitive function in old mice: a possible role for neuroinflammation mediated by HMGB1, S100B, and RAGE. J. Surg. Res. 185, 815–824 (2013). · DOI
  69. Linnemann, A. K. et al. Glucagon-like peptide-1 regulates cholecystokinin production in beta-cells to protect from apoptosis. Mol. Endocrinol. 29, 978–987 (2015). · DOI
  70. Renner, S., Blutke, A., Streckel, E., Wanke, R. & Wolf, E. Incretin actions and consequences of incretin-based therapies: lessons from complementary animal models. J. Pathol. 238, 345–358 (2016). · DOI
  71. Leiter, E. H., Premdas, F., Harrison, D. E. & Lipson, L. G. Aging and glucose homeostasis in C57BL/6J male mice. FASEB J. 2, 2807–2811 (1988). · DOI
  72. Leger, M. et al. Object recognition test in mice. Nat. Prot. 8, 2531–2537 (2013). · DOI · Paper page
  73. Servick, K. Mouse microbes may make scientific studies harder to replicate. Science, https://doi.org/10.1126/science.aah7199 (2016). · DOI
  74. Cheng, C. J., Gelfond, J. A. L., Strong, R. & Nelson, J. F. Genetically heterogeneous mice exhibit a female survival advantage that is age- and site-specific: results from a large multi-site study. Aging Cell, e12905, https://doi.org/10.1111/acel.12905 (2019). · DOI
  75. Kalueff, A. V., Keisala, T., Minasyan, A., Kuuslahti, M. & Tuohimaa, P. Temporal stability of novelty exploration in mice exposed to different open field tests. Behav. Process. 72, 104–112 (2006). · DOI
  76. Ennaceur, A. One-trial object recognition in rats and mice: methodological and theoretical issues. Behav. Brain Res. 215, 244–254 (2010). · DOI · Paper page
  77. Raber, J. Novel images and novel locations of familiar images as sensitive translational cognitive tests in humans. Behav. Brain Res. 285, 53–59 (2015). · DOI
  78. Frick, K. M. & Gresack, J. E. Sex differences in the behavioral response to spatial and object novelty in adult C57BL/6 mice. Behav. Neurosci. 117, 1283–1291 (2003). · DOI
  79. Prut, L. & Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3–33 (2003). · DOI
  80. Klein, S. M. et al. Noninvasive in vivo assessment of muscle impairment in the mdx mouse model—a comparison of two common wire hanging methods with two different results. J. Neurosci. Methods 203, 292–297 (2012). · DOI
  81. Karp, N. A., Segonds-Pichon, A., Gerdin, A. K., Ramirez-Solis, R. & White, J. K. The fallacy of ratio correction to address confounding factors. Lab. Anim. 46, 245–252 (2012). · DOI
  82. Gregg, T. et al. Pancreatic beta-cells from mice offset ageaAssociated mitochondrial deficiency with reduced KATP channel activity. Diabetes 65, 2700–2710 (2016). · DOI
  83. Schnelle, M. et al. Echocardiographic evaluation of diastolic function in mouse models of heart disease. J. Mol. Cell. Cardiol. 114, 20–28 (2018). · DOI
  84. Majumder, S. et al. Lifelong rapamycin administration ameliorates age-dependent cognitive deficits by reducing IL-1beta and enhancing NMDA signaling. Aging Cell 11, 326–335 (2012). · DOI
  85. Lin, A. L. et al. Chronic rapamycin restores brain vascular integrity and function through NO synthase activation and improves memory in symptomatic mice modeling Alzheimer’s disease. J. Cereb. Blood Flow. Metab. 33, 1412–1421 (2013). · DOI
  86. Lee, A. S. et al. Aged skeletal muscle retains the ability to fully regenerate functional architecture. Bioarchitecture 3, 25–37 (2013). · DOI
  87. van Norren, K. et al. Behavioural changes are a major contributing factor in the reduction of sarcopenia in caloric-restricted ageing mice. J. Cachexia Sarcopenia Muscle 6, 253–268 (2015). · DOI
  88. Ge, X. et al. Grip strength is potentially an early indicator of age-related decline in mice. Pathobiol. Aging Age Relat. Dis. 6, 32981 (2016). · DOI
  89. Hirsch, C. H., Buzkova, P., Robbins, J. A., Patel, K. V. & Newman, A. B. Predicting late-life disability and death by the rate of decline in physical performance measures. Age Ageing 41, 155–161 (2012). · DOI
  90. Bogue, M. A. et al. Accessing data resources in the mouse phenome database for genetic analysis of murine life span and health span. J. Gerontol. A Biol. Sci. Med. Sci. 71, 170–177 (2016). · DOI
  91. Peterson, R. L., Parkinson, K. C. & Mason, J. B. Manipulation of ovarian function significantly influenced sarcopenia in postreproductive-age mice. J. Transplant. 2016, 4570842 (2016). · DOI
  92. Graber, T. G., Ferguson-Stegall, L., Kim, J. H. & Thompson, L. V. C57BL/6 neuromuscular healthspan scoring system. J. Gerontol. A Biol. Sci. Med. Sci. 68, 1326–1336 (2013). · DOI
  93. Simmons, D. A. et al. A small molecule TrkB ligand reduces motor impairment and neuropathology in R6/2 and BACHD mouse models of Huntington’s disease. J. Neurosci. 33, 18712–18727 (2013). · DOI
  94. Jeong, H. et al. Sirt1 mediates neuroprotection from mutant huntingtin by activation of the TORC1 and CREB transcriptional pathway. Nat. Med. 18, 159–165 (2011). · DOI
  95. Zhang, Y. et al. Rapamycin extends life and health in C57BL/6 mice. J. Gerontol. A Biol. Sci. Med. Sci. 69, 119–130 (2014). · DOI
  96. Cummings, N. E. & Lamming, D. W. Regulation of metabolic health and aging by nutrient-sensitive signaling pathways. Mol. Cell. Endocrinol. 455, 13–22 (2017). · DOI
  97. Lamming, D. W. & Anderson, R. M. Metabolic effects of caloric restriction in eLS. (John Wiley & Sons, Ltd, 2014). · DOI
  98. Malloy, V. L. et al. Methionine restriction decreases visceral fat mass and preserves insulin action in aging male Fischer 344 rats independent of energy restriction. Aging Cell 5, 305–314 (2006). · DOI
  99. Green, C. L. & Lamming, D. W. Regulation of metabolic health by essential dietary amino acids. Mech. Ageing Dev. 177, 186–200 (2018). · DOI
  100. Brewer, R. A., Gibbs, V. K. & Smith, D. L. Jr. Targeting glucose metabolism for healthy aging. Nutr. Healthy Aging 4, 31–46 (2016). · DOI
  101. Tschop, M. H. et al. A guide to analysis of mouse energy metabolism. Nat. Methods 9, 57–63 (2011). · DOI · Paper page
  102. Lusk, G. ANIMAL CALORIMETRY: Twenty-Fourth Paper. ANALYSIS OF THE OXIDATION OF MIXTURES OF CARBOHYDRATE AND FAT. J. Biol. Chem. 59, 41–42 (1924). · DOI
  103. Solon-Biet, S. M. et al. Dietary protein to carbohydrate ratio and caloric restriction: comparing metabolic outcomes in mice. Cell Rep. 11, 1529–1534 (2015). · DOI · Paper page
  104. Taffet, G. E., Pham, T. T. & Hartley, C. J. The age-associated alterations in late diastolic function in mice are improved by caloric restriction. J. Gerontol. A Biol. Sci. Med. Sci. 52, B285–290 (1997). · DOI
  105. Casaclang-Verzosa, G., Enriquez-Sarano, M., Villaraga, H. R. & Miller, J. D. Echocardiographic approaches and protocols for comprehensive phenotypic characterization of valvular heart disease in mice. J. Vis. Exp. https://doi.org/10.3791/54110 (2017). · DOI

Cited by

Sorted by citations

Metadata

Authors
Bellantuono, I., de Cabo, R., Ehninger, D., Di Germanio, C., Lawrie, A., Miller, J., Mitchell, S. J., Navas-Enamorado, I., Potter, P. K., Tchkonia, T., Trejo, J. L., & Lamming, D. W.
Venue
Nature Protocols
Published
2020-01-08
Volume
15
Issue
2
Pages
540-574
ISSN
  • 1754-2189
  • 1750-2799
Cited by
145
References
28
Language
en

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