CoChat
Sign Up
Cited by 34

The DOI matches its Crossref record; 8 of the 8 references it cites were found in a registry or an index.

Muscle-specificity of age-related changes in markers of autophagy and sphingolipid metabolism

Russ, David W., Boyd, Iva M., McCoy, Katherine M., McCorkle, Katherine W.·2015·Biogerontology
DOI 10.1007/s10522-015-9598-4
Open this paper in CoChat — free account

Abstract

Our previous findings indicate that the gastrocnemius muscle of aging rats exhibits impairments of muscle quality (force/unit muscle tissue) and autophagy and increased sarcoplasmic reticulum stress. The purpose of this study was to examine age-related changes in soleus muscle contractility and in markers of autophagy in the soleus and gastrocnemius muscles. We assessed in situ muscle force and size in the soleus muscle of adult (7-8 months) and aged (24-26 months) male, F344/BN rats. We used immunoblotting to compare abundance of markers of autophagy, sarcoplasmic reticulum (SR) stress and sphingolipid metabolism in the soleus and medial gastrocnemius (MG) muscles of these animals. Relative to adults, aged rats maintained soleus muscle quality and increased muscle size, resulting in increased tetanic force production. Immunoblotting revealed a general pattern of an age-related reduction of basal autophagy, despite increases in indicators of SR stress and upstream autophagic pathway activation in the MG. The MG also exhibited changes in markers of sphingolipid metabolism suggestive of increased muscle ceramide. Minimal age-related changes were observed in the soleus. The soleus maintains muscle mass and quality with age, and exhibits fewer age-related changes in markers of stress and autophagy than the MG. Based on these data, we suggest that maintenance of autophagy may preserve muscle quality by preventing excessive SR stress.

Overview

Integrity signals

Registry

Crossref · 10.1007/s10522-015-9598-4

Cites

8 of 8 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

Citations

Cites

Flagged first, then by citations

Show all 8 references

Research works printed but not linked: 48

  1. Akima H et al (2001) Muscle function in 164 men and women aged 20–84 years. Med Sci Sports Exerc 33:220–226 · DOI
  2. Bean JF, Kiely DK, Herman S, Leveille SG, Mizer K, Frontera WR, Fielding RA (2002) The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc 50:461–467 · DOI · Paper page
  3. Bernales S, Schuck S, Walter P (2007) ER-phagy: selective autophagy of the endoplasmic reticulum. Autophagy 3:285–287 · DOI
  4. Bloemberg D, Quadrilatero J (2012) Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS ONE 7:e35273. doi: 10.1371/journal.pone.0035273 · DOI
  5. Borchman D, Tang D, Yappert MC (1999) Lipid composition, membrane structure relationships in lens and muscle sarcoplasmic reticulum membranes. Biospectroscopy 5:151–167. doi: 10.1002/(SICI)1520-6343(1999)5:3<151:AID-BSPY5>3.0.CO;2-D · DOI
  6. Bost ER, Frye GS, Ahn B, Ferreira LF (2015) Diaphragm dysfunction caused by sphingomyelinase requires the p47(phox) subunit of NADPH oxidase. Respir Physiol Neurobiol 205:47–52. doi: 10.1016/j.resp.2014.10.011 · DOI
  7. Carnio S et al (2014) Autophagy impairment in muscle induces neuromuscular junction degeneration and precocious aging. Cell Rep 8:1509–1521. doi: 10.1016/j.celrep.2014.07.061 · DOI · Paper page
  8. Carter EE, Thomas MM, Murynka T, Rowan SL, Wright KJ, Huba E, Hepple RT (2010) Slow twitch soleus muscle is not protected from sarcopenia in senescent rats. Exp Gerontol. doi: 10.1016/j.exger.2010.04.001 · DOI
  9. Degens H, Alway SE (2006) Control of muscle size during disuse, disease, and aging. Int J Sports Med 27:94–99. doi: 10.1055/s-2005-837571 · DOI
  10. Drost MR et al (2008) Both type 1 and type 2a muscle fibers can respond to enzyme therapy in Pompe disease. Muscle Nerve 37:251–255. doi: 10.1002/mus.20896 · DOI
  11. Eng CM, Smallwood LH, Rainiero MP, Lahey M, Ward SR, Lieber RL (2008) Scaling of muscle architecture and fiber types in the rat hindlimb. J Exp Biol 211:2336–2345. doi: 10.1242/jeb.017640 · DOI
  12. Ferreira LF, Moylan JS, Gilliam LA, Smith JD, Nikolova-Karakashian M, Reid MB (2010) Sphingomyelinase stimulates oxidant signaling to weaken skeletal muscle and promote fatigue. Am J Physiol Cell Physiol 299:C552–560. doi: 10.1152/ajpcell.00065.2010 · DOI
  13. Fragala MS, Clark MH, Walsh SJ, Kleppinger A, Judge JO, Kuchel GA, Kenny AM (2012) Gender differences in anthropometric predictors of physical performance in older adults. Gend Med 9:445–456. doi: 10.1016/j.genm.2012.10.004 · DOI
  14. Fry AC, Allemeier CA, Staron RS (1994) Correlation between percentage fiber type area and myosin heavy chain content in human skeletal muscle. Eur J Appl Physiol Occup Physiol 68:246–251 · DOI
  15. Garvey SM et al (2014) Metabolomic profiling reveals severe skeletal muscle group-specific perturbations of metabolism in aged FBN rats. Biogerontology 15:217–232. doi: 10.1007/s10522-014-9492-5 · DOI
  16. Hagen JL, Krause DJ, Baker DJ, Fu MH, Tarnopolsky MA, Hepple RT (2004) Skeletal muscle aging in F344BN F1-hybrid rats: i. Mitochondrial dysfunction contributes to the age-associated reduction in VO2max. J Gerontol A Biol Sci Med Sci 59:1099–1110 · DOI
  17. Hubbard VM, Valdor R, Macian F, Cuervo AM (2012) Selective autophagy in the maintenance of cellular homeostasis in aging organisms. Biogerontology 13:21–35. doi: 10.1007/s10522-011-9331-x · DOI
  18. Komatsu M et al (2005) Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 169:425–434. doi: 10.1083/jcb.200412022 · DOI · Paper page
  19. Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84:275–294 · DOI
  20. Libera LD, Zennaro R, Sandri M, Ambrosio GB, Vescovo G (1999) Apoptosis and atrophy in rat slow skeletal muscles in chronic heart failure. Am J Physiol 277:C982–986 · DOI
  21. Locke M, Atkinson BG, Tanguay RM, Noble EG (1994) Shifts in type I fiber proportion in rat hindlimb muscle are accompanied by changes in HSP72 content. Am J Physiol 266:C1240–1246 · DOI
  22. Madaro L, Marrocco V, Carnio S, Sandri M, Bouche M (2013) Intracellular signaling in ER stress-induced autophagy in skeletal muscle cells. Faseb J 27:1990–2000. doi: 10.1096/fj.12-215475 · DOI
  23. McMillan EM, Quadrilatero J (2011) Differential apoptosis-related protein expression, mitochondrial properties, proteolytic enzyme activity, and DNA fragmentation between skeletal muscles. Am J Physiol Regul Integr Comp Physiol 300:R531–543. doi: 10.1152/ajpregu.00488.2010 · DOI
  24. Metskas LA, Kulp M, Scordilis SP (2010) Gender dimorphism in the exercise-naive murine skeletal muscle proteome. Cell Mol Biol Lett 15:507–516. doi: 10.2478/s11658-010-0020-6 · DOI
  25. Metter EJ, Talbot LA, Schrager M, Conwit R (2002) Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol A Biol Sci Med Sci 57:B359–365 · DOI
  26. Mizunoya W, Wakamatsu J, Tatsumi R, Ikeuchi Y (2008) Protocol for high-resolution separation of rodent myosin heavy chain isoforms in a mini-gel electrophoresis system. Anal Biochem 377:111–113. doi: 10.1016/j.ab.2008.02.021 · DOI
  27. Naidoo N (2009) ER and aging-Protein folding and the ER stress response. Ageing Res Rev 8:150–159. doi: 10.1016/j.arr.2009.03.001 · DOI
  28. Nikolova-Karakashian MN, Rozenova KA (2010) Ceramide in stress response. Adv Exp Med Biol 688:86–108 · DOI
  29. Perrotta C, Clementi E (2010) Biological roles of acid and neutral sphingomyelinases and their regulation by nitric oxide. Physiology 25:64–71. doi: 10.1152/physiol.00048.2009 · DOI
  30. Purves-Smith FM, Sgarioto N, Hepple RT (2014) Fiber typing in aging muscle. Exerc Sport Sci Rev 42:45–52. doi: 10.1249/JES.0000000000000012 · DOI
  31. Renganathan M, Delbono O (1998) Caloric restriction prevents age-related decline in skeletal muscle dihydropyridine receptor and ryanodine receptor expression. FEBS Lett 434:346–350 · DOI
  32. Rowan SL, Purves-Smith FM, Solbak NM, Hepple RT (2011) Accumulation of severely atrophic myofibers marks the acceleration of sarcopenia in slow and fast twitch muscles. Exp Gerontol 46:660–669. doi: 10.1016/j.exger.2011.03.005 · DOI
  33. Rudolf R, Khan MM, Labeit S, Deschenes MR (2014) Degeneration of neuromuscular junction in age and dystrophy. Front Aging Neurosci 6:99. doi: 10.3389/fnagi.2014.00099 · DOI
  34. Russ DW, Grandy JS, Toma K, Ward CW (2011) Ageing, but not yet senescent, rats exhibit reduced muscle quality and sarcoplasmic reticulum function. Acta Physiol (Oxf) 201:391–403. doi: 10.1111/j.1748-1716.2010.02191.x · DOI · Paper page
  35. Russ DW, Gregg-Cornell K, Conaway MJ, Clark BC (2012a) Evolving concepts on the age-related changes in “muscle quality”. J Cachexia Sarcopenia Muscle 3:95–109. doi: 10.1007/s13539-011-0054-2 · DOI
  36. Russ DW, Krause J, Wills A, Arreguin R (2012b) “SR stress” in mixed hindlimb muscles of aging male rats. Biogerontology 13:547–555. doi: 10.1007/s10522-012-9399-y · DOI · Paper page
  37. Russ DW, Wills AM, Boyd IM, Krause J (2014) Weakness. SR function and stress in gastrocnemius muscles of aged male rats Exp Gerontol 50:40–44. doi: 10.1016/j.exger.2013.11.018 · DOI
  38. Sabbadini RA, Danieli-Betto D, Betto R (1999) The role of sphingolipids in the control of skeletal muscle function: a review. Ital J Neurol Sci 20:423–430 · DOI
  39. Separovic D, Kelekar A, Nayak AK, Tarca AL, Hanada K, Pierce JS, Bielawski J (2010) Increased ceramide accumulation correlates with downregulation of the autophagy protein ATG-7 in MCF-7 cells sensitized to photodamage. Arch Biochem Biophys 494:101–105. doi: 10.1016/j.abb.2009.11.023 · DOI
  40. Sharma C, Smith T, Li S, Schroepfer GJ Jr, Needleman DH (2000) Inhibition of Ca2+ release channel (ryanodine receptor) activity by sphingolipid bases: mechanism of action. Chem Phys Lipids 104:1–11 · DOI
  41. Staron RS, Kraemer WJ, Hikida RS, Fry AC, Murray JD, Campos GE (1999) Fiber type composition of four hindlimb muscles of adult Fisher 344 rats. Histochem Cell Biol 111:117–123 · DOI
  42. Terman A, Brunk UT (2006) Oxidative stress, accumulation of biological ‘garbage’, and aging. Antioxid Redox Signal 8:197–204. doi: 10.1089/ars.2006.8.197 · DOI
  43. Turturro A, Witt WW, Lewis S, Hass BS, Lipman RD, Hart RW (1999) 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 · DOI
  44. Volmer R, van der Ploeg K, Ron D (2013) Membrane lipid saturation activates endoplasmic reticulum unfolded protein response transducers through their transmembrane domains. Proc Natl Acad Sci USA 110:4628–4633. doi: 10.1073/pnas.1217611110 · DOI
  45. Volpe P, Villa A, Podini P, Martini A, Nori A, Panzeri MC, Meldolesi J (1992) The endoplasmic reticulum-sarcoplasmic reticulum connection: distribution of endoplasmic reticulum markers in the sarcoplasmic reticulum of skeletal muscle fibers. Proc Natl Acad Sci USA 89:6142–6146 · DOI
  46. Weisleder N et al (2006) Muscle aging is associated with compromised Ca2+ spark signaling and segregated intracellular Ca2+ release. J Cell Biol 174:639–645 · DOI
  47. Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C (2010) Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 45:138–148. doi: 10.1016/j.exger.2009.11.002 · DOI · Paper page
  48. Zha BS et al (2013) HIV protease inhibitors disrupt lipid metabolism by activating endoplasmic reticulum stress and inhibiting autophagy activity in adipocytes. PLoS One 8:e59514. doi: 10.1371/journal.pone.0059514 · DOI

Cited by

Sorted by citations

See all 34

Metadata

Authors
Russ, D. W., Boyd, I. M., McCoy, K. M., & McCorkle, K. W.
Venue
Biogerontology
Publisher
Springer Science and Business Media LLC
Published
2015-08-22
Volume
16
Issue
6
Pages
747-759
ISSN
  • 1389-5729
  • 1573-6768
DOI
10.1007/s10522-015-9598-4
Cited by
34
References
8
Language
en
Licence
www.springer.com/tdm (tdm)
Funders
Ohio Musculskeletal Neurological Institute

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