Long-lived mice with reduced growth hormone signaling have a constitutive upregulation of hepatic chaperone-mediated autophagy

References

• Sinha RA, Singh BK, Yen PM. Reciprocal crosstalk between autophagic and endocrine signaling in metabolic homeostasis. Endocr Rev. 2017;38:69–102.
   PubMed Web of Science ®Google Scholar
• Feng Y, He D, Yao Z, et al. The machinery of macroautophagy. Cell Res. 2013;24:24–41.
   PubMed Web of Science ®Google Scholar
• Li -W-W, Li J, Bao J-K. Microautophagy: lesser-known self-eating. Cell Mol Life Sci. 2011;69:1125–1136.
   PubMed Web of Science ®Google Scholar
• Sahu R, Kaushik S, Clement CC, et al. Microautophagy of cytosolic proteins by late endosomes. Dev Cell. 2011;20:131–139.
   PubMed Web of Science ®Google Scholar
• Smith RE, Farquhar MG. Lysosome function in the regulation of the secretory process in cells of the anterior pituitary gland. J Cell Biol. 1966;31:319–347.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Bandyopadhyay U, Sridhar S, et al. Chaperone-mediated autophagy at a glance. J Cell Sci. 2011;124:495–499.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Cuervo AM. The coming of age of chaperone-mediated autophagy. Nat Rev Mol Cell Biol. 2018;19:365–381.
   PubMed Web of Science ®Google Scholar
• Lescat L, Herpin A, Mourot B, et al. CMA restricted to mammals and birds: myth or reality? Autophagy. 2018;14:1267–1270.
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Bergamini E, Brunk UT, et al. Autophagy and aging: the importance of maintaining “Clean” cells. Autophagy. 2005;1:131–140.
   PubMed Web of Science ®Google Scholar
• Pyo J-O, Yoo S-M, Ahn -H-H, et al. Overexpression of Atg5 in mice activates autophagy and extends lifespan. Nat Commun. 2013:4:1–9.
   Web of Science ®Google Scholar
• Fernández ÁF, Sebti S, Wei Y, et al. Disruption of the beclin 1-BCL2 autophagy regulatory complex promotes longevity in mice. Nature. 2018;558:136–140.
   PubMed Web of Science ®Google Scholar
• Simonsen A, Cumming RC, Brech A, et al. Promoting basal levels of autophagy in the nervous system enhances longevity and oxidant resistance in adult Drosophila. Autophagy. 2014;4:176–184.
   Web of Science ®Google Scholar
• Chen S-F, Kang M-L, Chen Y-C, et al. Autophagy-related gene 7 is downstream of heat shock protein 27 in the regulation of eye morphology, polyglutamine toxicity, and lifespan in Drosophila. J Biomed Sci. 2012;19:1.
   PubMed Web of Science ®Google Scholar
• Meléndez A, Talloczy Z, Seaman M, et al. Autophagy genes are essential for dauer development andlife-span extension in C. elegans. Science. 2003;301:1387–1391.
   PubMed Web of Science ®Google Scholar
• Tóth ML, Sigmond T, Borsos É, et al. Longevity pathways converge on autophagy genes to regulate life span in Caenorhabditis elegans. Autophagy. 2014;4:330–338.
   Web of Science ®Google Scholar
• Cuervo AM, Dice JF. Age-related decline in chaperone-mediated autophagy. J Biol Chem. 2000;275:31505–31513.
   PubMed Web of Science ®Google Scholar
• Zhang C, Cuervo AM. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med. 2008;14:959–965.
   PubMed Web of Science ®Google Scholar
• Kiffin R, Kaushik S, Zeng M, et al. Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J Cell Sci. 2007;120:782–791.
   PubMed Web of Science ®Google Scholar
• Rodriguez-Navarro JA, Kaushik S, Koga H, et al. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. PNAS. 2012;109:E705–14.
   PubMed Web of Science ®Google Scholar
• Kaushik S, Massey AC, Cuervo AM. Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. Embo J. 2006;25:3921–3933.
   PubMed Web of Science ®Google Scholar
• Xilouri M, Brekk OR, Polissidis A, et al. Impairment of chaperone-mediated autophagy induces dopaminergic neurodegeneration in rats. Autophagy. 2016;12:2230–2247.
   PubMed Web of Science ®Google Scholar
• Xilouri M, Brekk OR, Landeck N, et al. Boosting chaperone-mediated autophagy in vivo mitigates α-synuclein-induced neurodegeneration. Brain. 2013;136:2130–2146.
   PubMed Web of Science ®Google Scholar
• Massey AC, Kaushik S, Sovak G, et al. Consequences of the selective blockage of chaperone-mediated autophagy. PNAS. 2006;103:5805–5810.
   PubMed Web of Science ®Google Scholar
• Gomes LR, Menck CFM, Cuervo AM. Chaperone-mediated autophagy prevents cellular transformation by regulating MYC proteasomal degradation. Autophagy. 2017;13:928–940.
   PubMed Web of Science ®Google Scholar
• Junttila MR, Puustinen P, Niemelä M, et al. CIP2A inhibits PP2A in human malignancies. Cell. 2007;130:51–62.
   PubMed Web of Science ®Google Scholar
• Westermarck J, Hahn WC. Multiple pathways regulated by the tumor suppressor PP2A in transformation. Trends Mol Med. 2008;14:152–160.
   PubMed Web of Science ®Google Scholar
• Xilouri M, Stefanis L. Chaperone mediated autophagy in aging: starve to prosper. Ageing Res Rev. 2016;32:13–21.
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Knecht E, Terlecky SR, et al. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol. 1995;269:C1200–C1208.
   PubMed Web of Science ®Google Scholar
• Arias E, Koga H, Diaz A, et al. Lysosomal mTORC2/PHLPP1/Akt regulate chaperone-mediated autophagy. Mol Cell. 2015;59:270–284.
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay U, Sridhar S, Kaushik S, et al. Identification of regulators of chaperone-mediated autophagy. Mol Cell. 2010;39:535–547.
   PubMed Web of Science ®Google Scholar
• Dominick G, Berryman DE, List EO, et al. Regulation of mTOR activity in Snell dwarf and GH receptor gene-disrupted mice. Endocrinology. 2015;156:565–575.
   PubMed Web of Science ®Google Scholar
• Dominick G, Bowman J, Li X, et al. mTOR regulates the expression of DNA damage response enzymes in long-lived Snell dwarf, GHRKO, and PAPPA-KO mice. Aging Cell. 2016;16:1–9.
   Web of Science ®Google Scholar
• Paquette M, El-Houjeiri L, Pause A. mTOR pathways in cancer and autophagy. Cancers (Basel). 2018;10:1–15.
   Web of Science ®Google Scholar
• Coschigano KT, Holland AN, Riders ME, et al. Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology. 2003;144:3799–3810.
   PubMed Web of Science ®Google Scholar
• Flurkey K, Papaconstantinou J, Miller RA, et al. Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci USA. 2001;98:6736–6741.
   PubMed Web of Science ®Google Scholar
• Anisimov VN, Bartke A. The key role of growth hormone-insulin-IGF-1 signaling in aging and cancer. Crit Rev Oncol Hematol. 2013;87:201–223.
   PubMed Web of Science ®Google Scholar
• Murakami S, Salmon A, Miller RA. Multiplex stress resistance in cells from long-lived dwarf mice. Faseb J. 2003;17:1565–1566.
   PubMed Web of Science ®Google Scholar
• Wang M, Miller RA. Fibroblasts from long lived mutant mice exhibit increased autophagy and lower TOR activity after nutrient deprivation or oxidative stress. Aging Cell. 2012;11:668–674.
   PubMed Web of Science ®Google Scholar
• Schneider JL, Suh Y, Cuervo AM. Deficient Chaperone-mediated autophagy in liver leads to metabolic dysregulation. Cell Metab. 2014;20:417–432.
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Terlecky SR, Dice JF, et al. Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J Biol. 1994;269:26374–26380.
   Google Scholar
• Dice JF. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci. 1990;15:305–309.
   PubMed Web of Science ®Google Scholar
• Chiang H-L, Terlecky T, Plant CP, et al. A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science. 1989;246:382–385.
   PubMed Web of Science ®Google Scholar
• Agarraberes FA, Dice JF. A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci. 2001;114:2491–2499.
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Dice JF, Knecht E. A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J Biol Chem. 1997;272:5606–5615.
   PubMed Web of Science ®Google Scholar
• Aniento F, Roche E, Cuervo AM, et al. Uptake and degradation of glyceraldehyde-3-phosphate dehydrogenase by rat liver lysosomes. J Biol Chem. 1993;268:10463–10470.
   PubMed Web of Science ®Google Scholar
• Lin S-C, Sen L, Drolet DW, et al. Pituitary ontogeny of the Snell dwarf mouse reveals Pit-1-independent and Pit-1-dependent origins of the thyrotrope. Development. 1994;120:515–522.
   PubMed Web of Science ®Google Scholar
• Bartke A, Westbrook R. Metabolic characteristics of long-lived mice. Front Genet. 2012;3:288.
   PubMedGoogle Scholar
• List EO, Berryman DE, Funk K, et al. 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. 2014;155:1793–1805.
   PubMed Web of Science ®Google Scholar
• Cuervo AM, Dice JF. Regulation of lamp2a levels in the lysosomal membrane. Traffic. 2000;1:570–583.
   PubMed Web of Science ®Google Scholar
• Kundra R, Kornfeld S. Asparagine-linked oligosaccharides protect lamp-1 and lamp-2 from intracellular proteolysis*. J Biol Chem. 1999;274:31039–31046.
   PubMed Web of Science ®Google Scholar
• Újvári A, Aron R, Eisenhaure T, et al. Translation rate of human tyrosinase determines its N-linked glycosylation level. J Biol Chem. 2001;276:5924–5931.
   PubMed Web of Science ®Google Scholar
• Drake JC, Bruns DR, Peelor FF III, et al. Long-lived Snell dwarf mice display increased proteostatic mechanisms that are not dependent on decreased mTORC1 activity. Aging Cell. 2015;14:474–482.
   PubMed Web of Science ®Google Scholar
• Bandyopadhyay U, Kaushik S, Varticovski L, et al. The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell. 2008;28:5747–5763.
   Web of Science ®Google Scholar
• Haspel J, Shaik RS, Ifedigbo E, et al. Characterization of macroautophagic flux in vivo using a leupeptin-based assay. Autophagy. 2014;7:629–642.
   Web of Science ®Google Scholar
• Kaushik S, Cuervo AM. AMPK-dependent phosphorylation of lipid droplet protein PLIN2 triggers its degradation by CMA. Autophagy. 2016;12:432–438.
   PubMed Web of Science ®Google Scholar
• Come C, Laine A, Chanrion M, et al. CIP2A is associated with human breast cancer aggressivity. Clin Cancer Res. 2009;15:5092–5100.
   PubMed Web of Science ®Google Scholar
• Young JA, List EO, Kopchick JJ. Deconstructing the Growth Hormone Receptor(GHR): physical and metabolic phenotypes of tissue-specific GHR gene-disrupted mice. Prog Mol Biol Transl Sci. 2016;138:27–39.
   PubMed Web of Science ®Google Scholar
• Hofmann JW, Zhao X, De Cecco M, et al. Reduced expression of MYC increases longevity and enhances healthspan. Cell. 2015;160:477–488.
   PubMed Web of Science ®Google Scholar
• Troncoso R, Vicencio JM, Parra V, et al. Energy-preserving effects of IGF-1 antagonize starvation-induced cardiac autophagy. Cardiovasc Res. 2011;93:320–329.
   PubMed Web of Science ®Google Scholar
• Brooks NL, Trent CM, Raetzsch CF, et al. Low utilization of circulating glucose after food withdrawal in Snell dwarf mice. J Biol Chem. 2007;282:35069–35077.
   PubMed Web of Science ®Google Scholar
• Liu Y, Palanivel R, Rai E, et al. Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice. Diabetes. 2014;64:36–48.
   PubMed Web of Science ®Google Scholar
• Sinha RA, You S-H, Zhou J, et al. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J Clin Investig. 2012;122:2428–2438.
   PubMed Web of Science ®Google Scholar
• Coschigano KT, Clemmons D, Bellush LL, et al. Assessment of growth parameters and life span of GHR/BP gene-disrupted mice*. Endocrinology. 2000;141:2608–2613.
   PubMed Web of Science ®Google Scholar
• Al-Regaiey KA, Masternak MM, Bonkowski M, et al. Long-lived growth hormone receptor knockout mice: interaction of reduced insulin-like growth factor I/insulin signaling and caloric restriction. Endocrinology. 2005;146:851–860.
   PubMed Web of Science ®Google Scholar
• Hauck SJ, Hunter WS, Danilovich N, et al. Reduced levels of thyroid hormones, insulin, and glucose, and lower body core temperature in the growth hormone receptor/binding protein knockout mouse. Exp Biol Med. 2001;226:552–558.
   Web of Science ®Google Scholar
• Westbrook R, Bonkowski MS, Strader AD, et al. Alterations in oxygen consumption, respiratory quotient, and heat production in long-lived GHRKO and ames dwarf mice, and short-lived bGH transgenic mice. J Gerontol A. 2009;64A:443–451.
   Google Scholar
• Zhou Y, Xu BC, Maheshwari HG, et al. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor. PNAS. 1997;94:13215–13220.
   PubMed Web of Science ®Google Scholar
• Wendeler M, Sandhoff K. Hexosaminidase assays. Glycoconj J. 2008;26:945–952.
   Web of Science ®Google Scholar
• Miller RA, Harrison DE, Astle CM, et al. An aging interventions testing program: study design and interim report. Aging Cell. 2007;6:565–575.
   PubMed Web of Science ®Google Scholar
• Miller RA, Burke D, Nadon NL. Announcement: four-way cross mouse stocks: a new, genetically heterogeneous resource for aging research. J Gerontol. 1999;54A:B358–B360.
   Google Scholar