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Cap-independent translation of GPLD1 enhances markers of brain health in long-lived mutant and drug-treated mice
dc.contributor.authorLi, Xinna
dc.contributor.authorShi, Xiaofang
dc.contributor.authorMcPherson, Madaline
dc.contributor.authorHager, Mary
dc.contributor.authorGarcia, Gonzalo G.
dc.contributor.authorMiller, Richard A.
dc.date.accessioned2022-10-05T15:51:44Z
dc.date.available2023-10-05 11:51:43en
dc.date.available2022-10-05T15:51:44Z
dc.date.issued2022-09
dc.identifier.citationLi, Xinna; Shi, Xiaofang; McPherson, Madaline; Hager, Mary; Garcia, Gonzalo G.; Miller, Richard A. (2022). "Cap-independent translation of GPLD1 enhances markers of brain health in long-lived mutant and drug-treated mice." Aging Cell (9): n/a-n/a.
dc.identifier.issn1474-9718
dc.identifier.issn1474-9726
dc.identifier.urihttps://hdl.handle.net/2027.42/174922
dc.description.abstractGlycosylphosphatidylinositol-specific phospholipase D1 (GPLD1) hydrolyzes inositol phosphate linkages in proteins anchored to the cell membrane. Mice overexpressing GPLD1 show enhanced neurogenesis and cognition. Snell dwarf (DW) and growth hormone receptor knockout (GKO) mice show delays in age-dependent cognitive decline. We hypothesized that augmented GPLD1 might contribute to retained cognitive function in these mice. We report that DW and GKO show higher GPLD1 levels in the liver and plasma. These mice also have elevated levels of hippocampal brain-derived neurotrophic factor (BDNF) and of doublecortin (DCX), suggesting a mechanism for maintenance of cognitive function at older ages. GPLD1 was not increased in the hippocampus of DW or GKO mice, suggesting that plasma GPLD1 increases elevated these brain proteins. Alteration of the liver and plasma GPLD1 was unaltered in mice with liver-specific GHR deletion, suggesting that the GH effect was not intrinsic to the liver. GPLD1 was also induced by caloric restriction and by each of four drugs that extend lifespan. The proteome of DW and GKO mice is molded by selective translation of mRNAs, involving cap-independent translation (CIT) of mRNAs marked by N6 methyladenosine. Because GPLD1 protein increases were independent of the mRNA level, we tested the idea that GPLD1 might be regulated by CIT. 4EGI-1, which enhances CIT, increased GPLD1 protein without changes in GPLD1 mRNA in cultured fibroblasts and mice. Furthermore, transgenic overexpression of YTHDF1, which promotes CIT by reading m6A signals, also led to increased GPLD1 protein, showing that elevation of GPLD1 reflects selective mRNA translation.Two kinds of long-lived mice, Snell dwarf and GHRKO, have higher levels of GPLD1 in liver and plasma, as well as higher levels of two GPLD1-stimulated brain proteins, BDNF and DCX. Increased GPLD1 reflects selective cap-independent mRNA translation rather than transcriptional changes. Last, GPLD1 can be increased, in cultured cells and in mice, by a transgene and by a drug that turns on cap-independent translation.
dc.publisherWiley Periodicals, Inc.
dc.subject.othergrowth hormone
dc.subject.otherglycosylphosphatidylinositol specific phospholipase D1
dc.subject.othercap-independent translation
dc.subject.otheraging
dc.titleCap-independent translation of GPLD1 enhances markers of brain health in long-lived mutant and drug-treated mice
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/174922/1/acel13685_am.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/174922/2/acel13685.pdf
dc.identifier.doi10.1111/acel.13685
dc.identifier.sourceAging Cell
dc.identifier.citedreferenceMiller, R. A., Harrison, D. E., Astle, C. M., Fernandez, E., Flurkey, K., Han, M., Javors, M. A., Li, X., Nadon, N. L., Nelson, J. F., Pletcher, S., Salmon, A. B., Sharp, Z. D., van Roekel, S., Winkleman, L., & Strong, R. ( 2014 ). Rapamycin-mediated lifespan increase in mice is dose and sex dependent and metabolically distinct from dietary restriction. Aging Cell, 13 ( 3 ), 468 – 477. https://doi.org/10.1111/acel.12194
dc.identifier.citedreferenceMeyer, K. D., Patil, D. P., Zhou, J., Zinoviev, A., Skabkin, M. A., Elemento, O., Pestova, T. V., Qian, S. B., & Jaffrey, S. R. ( 2015 ). 5’ UTR m(6)A promotes cap-independent translation. Cell, 163 ( 4 ), 999 – 1010. https://doi.org/10.1016/j.cell.2015.10.012
dc.identifier.citedreferenceMiller, R. A., Harrison, D. E., Allison, D. B., Bogue, M., Debarba, L., Diaz, V., Fernandez, E., Galecki, A., Garvey, W. T., Jayarathne, H., Kumar, N., Javors, M. A., Ladiges, W. C., Macchiarini, F., Nelson, J., Reifsnyder, P., Rosenthal, N. A., Sadagurski, M., Salmon, A. B., … Strong, R. ( 2020 ). Canagliflozin extends life span in genetically heterogeneous male but not female mice. JCI Insight, 5 ( 21 ), 1 – 13. https://doi.org/10.1172/jci.insight.140019
dc.identifier.citedreferenceMiller, R. A., Harrison, D. E., Astle, C. M., Baur, J. A., Boyd, A. R., de Cabo, R., Fernandez, E., Flurkey, K., Javors, M. A., Nelson, J. F., Orihuela, C. J., Pletcher, S., Sharp, Z. D., Sinclair, D., Starnes, J. W., Wilkinson, J. E., Nadon, N. L., & Strong, R. ( 2011 ). Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. Journals of Gerontology – Series A Biological Sciences and Medical Sciences, 66 ( 2 ), 191 – 201. https://doi.org/10.1093/gerona/glq178
dc.identifier.citedreferenceMiranda, M., Morici, J. F., Zanoni, M. B., & Bekinschtein, P. ( 2019 ). Brain-derived neurotrophic factor: A key molecule for memory in the healthy and the pathological brain. Frontiers in Cellular Neuroscience, 13, 363. https://doi.org/10.3389/fncel.2019.00363
dc.identifier.citedreferenceMoerke, N. J., Aktas, H., Chen, H., Cantel, S., Reibarkh, M. Y., Fahmy, A., Gross, J. D., Degterev, A., Yuan, J., Chorev, M., Halperin, J. A., & Wagner, G. ( 2007 ). Small-molecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell, 128 ( 2 ), 257 – 267. https://doi.org/10.1016/j.cell.2006.11.046
dc.identifier.citedreferenceOzkurede, U., Kala, R., Johnson, C., Shen, Z., Miller, R. A., & Garcia, G. G. ( 2019 ). Cap-independent mRNA translation is upregulated in long-lived endocrine mutant mice. Journal of Molecular Endocrinology, 63 ( 2 ), 123 – 138. https://doi.org/10.1530/jme-19-0021
dc.identifier.citedreferencePark, H., & Poo, M. M. ( 2013 ). Neurotrophin regulation of neural circuit development and function. Nature Reviews Neuroscience, 14 ( 1 ), 7 – 23. https://doi.org/10.1038/nrn3379
dc.identifier.citedreferenceQin, W., Liang, Y. Z., Qin, B. Y., Zhang, J. L., & Xia, N. ( 2016 ). The clinical significance of glycoprotein phospholipase D levels in distinguishing early stage latent autoimmune diabetes in adults and type 2 diabetes. PLoS One, 11 ( 6 ), e0156959. https://doi.org/10.1371/journal.pone.0156959
dc.identifier.citedreferenceRomo-Araiza, A., Gutiérrez-Salmeán, G., Galván, E. J., Hernández-Frausto, M., Herrera-López, G., Romo-Parra, H., García-Contreras, V., Fernández-Presas, A. M., Jasso-Chávez, R., Borlongan, C. V., & Ibarra, A. ( 2018 ). Probiotics and prebiotics as a therapeutic strategy to improve memory in a model of middle-aged rats. Frontiers in Aging Neuroscience, 10, 416. https://doi.org/10.3389/fnagi.2018.00416
dc.identifier.citedreferenceShatsky, I. N., Terenin, I. M., Smirnova, V. V., & Andreev, D. E. ( 2018 ). Cap-independent translation: What’s in a name? Trends in Biochemical Sciences, 43 ( 11 ), 882 – 895. https://doi.org/10.1016/j.tibs.2018.04.011
dc.identifier.citedreferenceShen, Z., Hinson, A., Miller, R. A., & Garcia, G. G. ( 2021 ). Cap-independent translation: A shared mechanism for lifespan extension by rapamycin, acarbose, and 17α-estradiol. Aging Cell, 20 ( 5 ), e13345. https://doi.org/10.1111/acel.13345
dc.identifier.citedreferenceSpriggs, K. A., Bushell, M., & Willis, A. E. ( 2010 ). Translational regulation of gene expression during conditions of cell stress. Molecular Cell, 40 ( 2 ), 228 – 237. https://doi.org/10.1016/j.molcel.2010.09.028
dc.identifier.citedreferenceStrong, R., Miller, R. A., Antebi, A., Astle, C. M., Bogue, M., Denzel, M. S., Fernandez, E., Flurkey, K., Hamilton, K. L., Lamming, D. W., Javors, M. A., Magalhães, J. P., Martinez, P. A., McCord, J. M., Miller, B. F., Müller, M., Nelson, J. F., Ndukum, J., Rainger, G. E., … Harrison, D. E. ( 2016 ). Longer lifespan in male mice treated with a weakly estrogenic agonist, an antioxidant, an α-glucosidase inhibitor or a Nrf2-inducer. Aging Cell, 15 ( 5 ), 872 – 884. https://doi.org/10.1111/acel.12496
dc.identifier.citedreferenceSun, L. Y., Al-Regaiey, K., Masternak, M. M., Wang, J., & Bartke, A. ( 2005 ). Local expression of GH and IGF-1 in the hippocampus of GH-deficient long-lived mice. Neurobiol Aging, 26 ( 6 ), 929 – 937. https://doi.org/10.1016/j.neurobiolaging.2004.07.010
dc.identifier.citedreferenceSun, L. Y., Evans, M. S., Hsieh, J., Panici, J., & Bartke, A. ( 2005 ). Increased neurogenesis in dentate gyrus of long-lived Ames dwarf mice. Endocrinology, 146 ( 3 ), 1138 – 1144. https://doi.org/10.1210/en.2004-1115
dc.identifier.citedreferenceSun, L. Y., Spong, A., Swindell, W. R., Fang, Y., Hill, C., Huber, J. A., Boehm, J. D., Westbrook, R., Salvatori, R., & Bartke, A. ( 2013 ). Growth hormone-releasing hormone disruption extends lifespan and regulates response to caloric restriction in mice. Elife, 2, e01098. https://doi.org/10.7554/eLife.01098
dc.identifier.citedreferenceSun, L. Y., Steinbaugh, M. J., Masternak, M. M., Bartke, A., & Miller, R. A. ( 2009 ). Fibroblasts from long-lived mutant mice show diminished ERK1/2 phosphorylation but exaggerated induction of immediate early genes. Free Radical Biology and Medicine, 47 ( 12 ), 1753 – 1761. https://doi.org/10.1016/j.freeradbiomed.2009.09.021
dc.identifier.citedreferenceWang, X., Lu, Z., Gomez, A., Hon, G. C., Yue, Y., Han, D., Fu, Y., Parisien, M., Dai, Q., Jia, G., Ren, B., Pan, T., & He, C. ( 2014 ). N6-methyladenosine-dependent regulation of messenger RNA stability. Nature, 505 ( 7481 ), 117 – 120. https://doi.org/10.1038/nature12730
dc.identifier.citedreferenceWang, X., Zhao, B. S., Roundtree, I. A., Lu, Z., Han, D., Ma, H., Weng, X., Chen, K., Shi, H., & He, C. ( 2015 ). N(6)-methyladenosine modulates messenger RNA translation efficiency. Cell, 161 ( 6 ), 1388 – 1399. https://doi.org/10.1016/j.cell.2015.05.014
dc.identifier.citedreferenceWilhelm, O. G., Wilhelm, S., Escott, G. M., Lutz, V., Magdolen, V., Schmitt, M., Rifkin, D. B., Wilson, E. L., Graeff, H., & Brunner, G. ( 1999 ). Cellular glycosylphosphatidylinositol-specific phospholipase D regulates urokinase receptor shedding and cell surface expression. Journal of Cellular Physiology, 180 ( 2 ), 225 – 235. doi: 10.1002/(sici)1097-4652(199908)180:2<225::Aid-jcp10>3.0.Co;2-2
dc.identifier.citedreferenceYamamoto, Y., Hirakawa, E., Mori, S., Hamada, Y., Kawaguchi, N., & Matsuura, N. ( 2005 ). Cleavage of carcinoembryonic antigen induces metastatic potential in colorectal carcinoma. Biochemical and Biophysical Research Communications, 333 ( 1 ), 223 – 229. https://doi.org/10.1016/j.bbrc.2005.05.084
dc.identifier.citedreferenceZhou, J., Wan, J., Gao, X., Zhang, X., Jaffrey, S. R., & Qian, S. B. ( 2015 ). Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature, 526 ( 7574 ), 591 – 594. https://doi.org/10.1038/nature15377
dc.identifier.citedreferenceZhou, Y., Xu, B. C., Maheshwari, H. G., He, L., Reed, M., Lozykowski, M., Okada, S., Cataldo, L., Coschigamo, K., Wagner, T. E., Baumann, G., & Kopchick, J. J. ( 1997 ). A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proceedings of the National Academy of Sciences of the United States of America, 94 ( 24 ), 13215 – 13220. https://doi.org/10.1073/pnas.94.24.13215
dc.identifier.citedreferenceZou, Z. Q., Xu, J., Li, L., & Han, Y. S. ( 2015 ). Down-regulation of SENCR promotes smooth muscle cells proliferation and migration in db/db mice through up-regulation of FoxO1 and TRPC6. Biomed Pharmacother, 74, 35 – 41. https://doi.org/10.1016/j.biopha.2015.06.009
dc.identifier.citedreferenceAberg, M. A., Aberg, N. D., Hedbäcker, H., Oscarsson, J., & Eriksson, P. S. ( 2000 ). Peripheral infusion of IGF-I selectively induces neurogenesis in the adult rat hippocampus. Journal of Neuroscience, 20 ( 8 ), 2896 – 2903. https://doi.org/10.1523/jneurosci.20-08-02896.2000
dc.identifier.citedreferenceAshpole, N. M., Sanders, J. E., Hodges, E. L., Yan, H., & Sonntag, W. E. ( 2015 ). Growth hormone, insulin-like growth factor-1 and the aging brain. Experimental Gerontology, 68, 76 – 81. https://doi.org/10.1016/j.exger.2014.10.002
dc.identifier.citedreferenceAyanlaja, A. A., Xiong, Y., Gao, Y., Ji, G., Tang, C., Abdikani Abdullah, Z., & Gao, D. ( 2017 ). Distinct features of doublecortin as a marker of neuronal migration and its implications in cancer cell mobility. Frontiers in Molecular Neuroscience, 10, 199. https://doi.org/10.3389/fnmol.2017.00199
dc.identifier.citedreferenceBale, L. K., & Conover, C. A. ( 2005 ). Disruption of insulin-like growth factor-II imprinting during embryonic development rescues the dwarf phenotype of mice null for pregnancy-associated plasma protein-A. Journal of Endocrinology, 186 ( 2 ), 325 – 331. https://doi.org/10.1677/joe.1.06259
dc.identifier.citedreferenceBalthazart, J., & Ball, G. F. ( 2014 ). Commentary on Vellema M et al. (2014): Evaluating the predictive value of doublecortin as a marker for adult neurogenesis in canaries (Serinus canaria). J Comparative Neurol 522:1299–1315. Brain, Behavior and Evolution, 84 ( 1 ), 1 – 4. https://doi.org/10.1159/000362917
dc.identifier.citedreferenceBartke, A., Hascup, E., Hascup, K., & Masternak, M. M. ( 2021 ). Growth hormone and aging: New findings. World Journal of Men’s Health, 39 ( 3 ), 454 – 465. https://doi.org/10.5534/wjmh.200201
dc.identifier.citedreferenceBednarski, E., Lauterborn, J. C., Gall, C. M., & Lynch, G. ( 1998 ). Lysosomal dysfunction reduces brain-derived neurotrophic factor expression. Experimental Neurology, 150 ( 1 ), 128 – 135. https://doi.org/10.1006/exnr.1997.6747
dc.identifier.citedreferenceBrown-Borg, H. M., Borg, K. E., Meliska, C. J., & Bartke, A. ( 1996 ). Dwarf mice and the ageing process. Nature, 384 ( 6604 ), 33. https://doi.org/10.1038/384033a0
dc.identifier.citedreferenceClancy, D. J., Gems, D., Harshman, L. G., Oldham, S., Stocker, H., Hafen, E., Leevers, S. J., & Partridge, L. ( 2001 ). Extension of life-span by loss of CHICO, a Drosophila insulin receptor substrate protein. Science, 292 ( 5514 ), 104 – 106. https://doi.org/10.1126/science.1057991
dc.identifier.citedreferenceCouillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H. G., & Aigner, L. ( 2005 ). Doublecortin expression levels in adult brain reflect neurogenesis. European Journal of Neuroscience, 21 ( 1 ), 1 – 14. https://doi.org/10.1111/j.1460-9568.2004.03813.x
dc.identifier.citedreferenceDecroly, E., Ferron, F., Lescar, J., & Canard, B. ( 2011 ). Conventional and unconventional mechanisms for capping viral mRNA. Nature Reviews Microbiology, 10 ( 1 ), 51 – 65. https://doi.org/10.1038/nrmicro2675
dc.identifier.citedreferenceDennis, M. D., Shenberger, J. S., Stanley, B. A., Kimball, S. R., & Jefferson, L. S. ( 2013 ). Hyperglycemia mediates a shift from cap-dependent to cap-independent translation via a 4E-BP1-dependent mechanism. Diabetes, 62 ( 7 ), 2204 – 2214. https://doi.org/10.2337/db12-1453
dc.identifier.citedreferenceDominick, G., Bowman, J., Li, X., Miller, R. A., & Garcia, G. G. ( 2017 ). mTOR regulates the expression of DNA damage response enzymes in long-lived Snell dwarf, GHRKO, and PAPPA-KO mice. Aging Cell, 16 ( 1 ), 52 – 60. https://doi.org/10.1111/acel.12525
dc.identifier.citedreferenceFlurkey, K., Papaconstantinou, J., Miller, R. A., & Harrison, D. E. ( 2001 ). Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proceedings of the National Academy of Sciences of the United States of America, 98 ( 12 ), 6736 – 6741. https://doi.org/10.1073/pnas.111158898
dc.identifier.citedreferenceFrancis, F., Koulakoff, A., Boucher, D., Chafey, P., Schaar, B., Vinet, M. C., Friocourt, G., McDonnell, N., Reiner, O., Kahn, A., McConnell, S. K., Berwald-Netter, Y., Denoulet, P., & Chelly, J. ( 1999 ). Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron, 23 ( 2 ), 247 – 256. https://doi.org/10.1016/s0896-6273(00)80777-1
dc.identifier.citedreferenceGarratt, M., Bower, B., Garcia, G. G., & Miller, R. A. ( 2017 ). Sex differences in lifespan extension with acarbose and 17-α estradiol: Gonadal hormones underlie male-specific improvements in glucose tolerance and mTORC2 signaling. Aging Cell, 16 ( 6 ), 1256 – 1266. https://doi.org/10.1111/acel.12656
dc.identifier.citedreferenceGemma, C., & Bickford, P. C. ( 2007 ). Interleukin-1beta and caspase-1: Players in the regulation of age-related cognitive dysfunction. Reviews in the Neurosciences, 18 ( 2 ), 137 – 148. https://doi.org/10.1515/revneuro.2007.18.2.137
dc.identifier.citedreferenceGleeson, J. G., Lin, P. T., Flanagan, L. A., & Walsh, C. A. ( 1999 ). Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron, 23 ( 2 ), 257 – 271. https://doi.org/10.1016/s0896-6273(00)80778-3
dc.identifier.citedreferenceGreenberg, M. E., Xu, B., Lu, B., & Hempstead, B. L. ( 2009 ). New insights in the biology of BDNF synthesis and release: Implications in CNS function. Journal of Neuroscience, 29 ( 41 ), 12764 – 12767. https://doi.org/10.1523/jneurosci.3566-09.2009
dc.identifier.citedreferenceHarada, C. N., Natelson Love, M. C., & Triebel, K. L. ( 2013 ). Normal cognitive aging. Clinics in Geriatric Medicine, 29 ( 4 ), 737 – 752. https://doi.org/10.1016/j.cger.2013.07.002
dc.identifier.citedreferenceHarrison, D. E., Strong, R., Alavez, S., Astle, C. M., DiGiovanni, J., Fernandez, E., Flurkey, K., Garratt, M., Gelfond, J. A. L., Javors, M. A., Levi, M., Lithgow, G. J., Macchiarini, F., Nelson, J. F., Sukoff Rizzo, S. J., Slaga, T. J., Stearns, T., Wilkinson, J. E., & Miller, R. A. ( 2019 ). Acarbose improves health and lifespan in aging HET3 mice. Aging Cell, 18 ( 2 ), e12898. https://doi.org/10.1111/acel.12898
dc.identifier.citedreferenceHarrison, D. E., Strong, R., Allison, D. B., Ames, B. N., Astle, C. M., Atamna, H., Fernandez, E., Flurkey, K., Javors, M. A., Nadon, N. L., Nelson, J. F., Pletcher, S., Simpkins, J. W., Smith, D., Wilkinson, J. E., & Miller, R. A. ( 2014 ). Acarbose, 17-α-estradiol, and nordihydroguaiaretic acid extend mouse lifespan preferentially in males. Aging Cell, 13 ( 2 ), 273 – 282. https://doi.org/10.1111/acel.12170
dc.identifier.citedreferenceHarrison, D. E., Strong, R., Sharp, Z. D., Nelson, J. F., Astle, C. M., Flurkey, K., Nadon, N. L., Wilkinson, J. E., Frenkel, K., Carter, C. S., Pahor, M., Javors, M. A., Fernandez, E., & Miller, R. A. ( 2009 ). Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature, 460 ( 7253 ), 392 – 395. https://doi.org/10.1038/nature08221
dc.identifier.citedreferenceHascup, K. N., Lynn, M. K., Fitzgerald, P. J., Randall, S., Kopchick, J. J., Boger, H. A., Bartke, A., & Hascup, E. R. ( 2017 ). Enhanced cognition and hypoglutamatergic signaling in a growth hormone receptor knockout mouse model of successful aging. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 72 ( 3 ), 329 – 337. https://doi.org/10.1093/gerona/glw088
dc.identifier.citedreferenceHorowitz, A. M., Fan, X., Bieri, G., Smith, L. K., Sanchez-Diaz, C. I., Schroer, A. B., Gontier, G., Casaletto, K. B., Kramer, J. H., Williams, K. E., & Villeda, S. A. ( 2020 ). Blood factors transfer beneficial effects of exercise on neurogenesis and cognition to the aged brain. Science, 369 ( 6500 ), 167 – 173. https://doi.org/10.1126/science.aaw2622
dc.identifier.citedreferenceHummler, E., Dousse, A., Rieder, A., Stehle, J. C., Rubera, I., Osterheld, M. C., Beermann, F., Frateschi, S., & Charles, R. P. ( 2013 ). The channel-activating protease CAP1/Prss8 is required for placental labyrinth maturation. PLoS One, 8 ( 2 ), e55796. https://doi.org/10.1371/journal.pone.0055796
dc.identifier.citedreferenceIcyuz, M., Fitch, M., Zhang, F., Challa, A., & Sun, L. Y. ( 2020 ). Physiological and metabolic features of mice with CRISPR/Cas9-mediated loss-of-function in growth hormone-releasing hormone. Aging (Albany NY), 12 ( 10 ), 9761 – 9780. https://doi.org/10.18632/aging.103242
dc.identifier.citedreferenceIkeno, Y., Bronson, R. T., Hubbard, G. B., Lee, S., & Bartke, A. ( 2003 ). Delayed occurrence of fatal neoplastic diseases in ames dwarf mice: Correlation to extended longevity. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 58 ( 4 ), 291 – 296. https://doi.org/10.1093/gerona/58.4.b291
dc.identifier.citedreferenceIkeno, Y., Hubbard, G. B., Lee, S., Cortez, L. A., Lew, C. M., Webb, C. R., Berryman, D. E., List, E. O., Kopchick, J. J., & Bartke, A. ( 2009 ). Reduced incidence and delayed occurrence of fatal neoplastic diseases in growth hormone receptor/binding protein knockout mice. Journals of Gerontology Series A: Biomedical Sciences and Medical Sciences, 64 ( 5 ), 522 – 529. https://doi.org/10.1093/gerona/glp017
dc.identifier.citedreferenceJackson, R. J., Hellen, C. U., & Pestova, T. V. ( 2010 ). The mechanism of eukaryotic translation initiation and principles of its regulation. Nature Reviews Molecular Cell Biology, 11 ( 2 ), 113 – 127. https://doi.org/10.1038/nrm2838
dc.identifier.citedreferenceKimura, K. D., Tissenbaum, H. A., Liu, Y., & Ruvkun, G. ( 1997 ). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science, 277 ( 5328 ), 942 – 946. https://doi.org/10.1126/science.277.5328.942
dc.identifier.citedreferenceKinney, B. A., Coschigano, K. T., Kopchick, J. J., Steger, R. W., & Bartke, A. ( 2001 ). Evidence that age-induced decline in memory retention is delayed in growth hormone resistant GH-R-KO (Laron) mice. Physiology & Behavior, 72 ( 5 ), 653 – 660. https://doi.org/10.1016/s0031-9384(01)00423-1
dc.identifier.citedreferenceKinney, B. A., Meliska, C. J., Steger, R. W., & Bartke, A. ( 2001 ). Evidence that Ames dwarf mice age differently from their normal siblings in behavioral and learning and memory parameters. Hormones and Behavior, 39 ( 4 ), 277 – 284. https://doi.org/10.1006/hbeh.2001.1654
dc.identifier.citedreferenceKuipers, S. D., & Bramham, C. R. ( 2006 ). Brain-derived neurotrophic factor mechanisms and function in adult synaptic plasticity: New insights and implications for therapy. Current Opinion in Drug Discovery and Development, 9 ( 5 ), 580 – 586.
dc.identifier.citedreferenceLacerda, R., Menezes, J., & Romão, L. ( 2017 ). More than just scanning: The importance of cap-independent mRNA translation initiation for cellular stress response and cancer. Cellular and Molecular Life Sciences, 74 ( 9 ), 1659 – 1680. https://doi.org/10.1007/s00018-016-2428-2
dc.identifier.citedreferenceLeal, S. L., & Yassa, M. A. ( 2015 ). Neurocognitive aging and the hippocampus across species. Trends in Neurosciences, 38 ( 12 ), 800 – 812. https://doi.org/10.1016/j.tins.2015.10.003
dc.identifier.citedreferenceLeBoeuf, R. C., Caldwell, M., Guo, Y., Metz, C., Davitz, M. A., Olson, L. K., & Deeg, M. A. ( 1998 ). Mouse glycosylphosphatidylinositol-specific phospholipase D (Gpld1) characterization. Mammalian Genome, 9 ( 9 ), 710 – 714. https://doi.org/10.1007/s003359900851
dc.identifier.citedreferenceLi, X., Frazier, J. A., Spahiu, E., McPherson, M., & Miller, R. A. ( 2020 ). Muscle-dependent regulation of adipose tissue function in long-lived growth hormone-mutant mice. Aging (Albany NY), 12 ( 10 ), 8766 – 8789. https://doi.org/10.18632/aging.103380
dc.identifier.citedreferenceLi, X., McPherson, M., Hager, M., Fang, Y., Bartke, A., & Miller, R. A. ( 2022 ). Transient early life growth hormone exposure permanently alters brain, muscle, liver, macrophage, and adipocyte status in long-lived Ames dwarf mice. The FASEB Journal, 36 ( 7 ), e22394. https://doi.org/10.1096/fj.202200143R
dc.identifier.citedreferenceLin, K., Dorman, J. B., Rodan, A., & Kenyon, C. ( 1997 ). daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science, 278 ( 5341 ), 1319 – 1322. https://doi.org/10.1126/science.278.5341.1319
dc.identifier.citedreferenceList, E. O., Berryman, D. E., Funk, K., Gosney, E. S., Jara, A., Kelder, B., Wang, X., Kutz, L., Troike, K., Lozier, N., Mikula, V., Lubbers, E. R., Zhang, H., Vesel, C., Junnila, R. K., Frank, S. J., Masternak, M. M., Bartke, A., & Kopchick, J. J. ( 2013 ). The role of GH in adipose tissue: Lessons from adipose-specific GH receptor gene-disrupted mice. Molecular Endocrinology, 27 ( 3 ), 524 – 535. https://doi.org/10.1210/me.2012-1330
dc.identifier.citedreferenceList, E. O., Berryman, D. E., Funk, K., Jara, A., Kelder, B., Wang, F., Stout, M. B., Zhi, X., Sun, L., White, T. A., LeBrasseur, N. K., Pirtskhalava, T., Tchkonia, T., Jensen, E. A., Zhang, W., Masternak, M. M., Kirkland, J. L., Miller, R. A., Bartke, A., & Kopchick, J. J. ( 2014 ). Liver-specific GH receptor gene-disrupted (LiGHRKO) mice have decreased endocrine IGF-I, increased local IGF-I, and altered body size, body composition, and adipokine profiles. Endocrinology, 155 ( 5 ), 1793 – 1805. https://doi.org/10.1210/en.2013-2086
dc.identifier.citedreferenceList, E. O., Berryman, D. E., Ikeno, Y., Hubbard, G. B., Funk, K., Comisford, R., Young, J. A., Stout, M. B., Tchkonia, T., Masternak, M. M., Bartke, A., Kirkland, J. L., Miller, R. A., & Kopchick, J. J. ( 2015 ). Removal of growth hormone receptor (GHR) in muscle of male mice replicates some of the health benefits seen in global GHR−/− mice. Aging (Albany NY), 7 ( 7 ), 500 – 512. https://doi.org/10.18632/aging.100766
dc.identifier.citedreferenceLoprinzi, P. D., & Frith, E. ( 2019 ). A brief primer on the mediational role of BDNF in the exercise-memory link. Clinical Physiology and Functional Imaging, 39 ( 1 ), 9 – 14. https://doi.org/10.1111/cpf.12522
dc.identifier.citedreferenceMacPherson, R. E. K. ( 2017 ). Filling the void: A role for exercise-induced BDNF and brain amyloid precursor protein processing. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 313 ( 5 ), R585 – R593. https://doi.org/10.1152/ajpregu.00255.2017
dc.identifier.citedreferenceMatsuda, T., & Cepko, C. L. ( 2004 ). Electroporation and RNA interference in the rodent retina in vivo and in vitro. Proceedings of the National Academy of Sciences of the United States of America, 101 ( 1 ), 16 – 22. https://doi.org/10.1073/pnas.2235688100
dc.working.doiNOen
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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