A minimal dose of electrically induced muscle activity regulates distinct gene signaling pathways in humans with spinal cord injury

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Petrie, Michael A ^a   Suneja, Manish ^a   Faidley, Elizabeth ^a   Shields, Richard K ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; BIOLOGICAL MARKER;

ABRA GENE; ACADVL GENE; ADULT; ARTICLE; BRP44 GENE; BRP44L GENE; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRODE; ELECTROSTIMULATION THERAPY; EXERCISE; GENE; GENE EXPRESSION; HUMAN; HUMAN TISSUE; IFRD1 GENE; MFF GENE; MFN1 GENE; MFN2 GENE; MUSCLE BIOPSY; MUSCLE CONTRACTION; MUSCLE STIMULATOR; MYH6 GENE; MYH7 GENE; MYL2 GENE; MYL3 GENE; NR4A3 GENE; PARAPLEGIA; PDK4 GENE; PGC 1A GENE; PHENOTYPE; SDHB GENE; SIGNAL TRANSDUCTION; SLOW MUSCLE FIBER; SOLEUS MUSCLE; SPINAL CORD INJURY; THERAPY EFFECT; ADAPTATION; COMPLICATION; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; MUSCULOSKELETAL FUNCTION; PARALYSIS; PATHOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKELETAL MUSCLE; SPINAL CORD INJURIES;

ADAPTATION, PHYSIOLOGICAL; ADULT; BIOMARKERS; ELECTRIC STIMULATION THERAPY; EXERCISE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MUSCLE, SKELETAL; MUSCULOSKELETAL PHYSIOLOGICAL PHENOMENA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES;

EID: 84919619317     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115791     Document Type: Article

References (62)

1. Bjornholm M, Zierath JR (2005) Insulin signal transduction in human skeletal muscle: identifying the defects in Type II diabetes. Biochem Soc Trans 33: 354-357.
2. Crameri RM, Weston A, Climstein M, Davis GM, Sutton JR (2002) Effects of electrical stimulationinduced leg training on skeletal muscle adaptability in spinal cord injury. Scand J Med Sci Sports 12: 316-322.
3. Shields RK, Law LF, Reiling B, Sass K, Wilwert J (1997) Effects of electrically induced fatigue on the twitch and tetanus of paralyzed soleus muscle in humans. J Appl Physiol (1985) 82: 1499-1507.
4. Shields RK (1995) Fatigability, relaxation properties, and electromyographic responses of the human paralyzed soleus muscle. J Neurophysiol 73: 2195-2206.
5. Shields RK, Chang YJ, Dudley-Javoroski S, Lin CH (2006) Predictive model of muscle fatigue after spinal cord injury in humans. Muscle Nerve 34: 84-91.
6. Shields RK, Dudley-Javoroski S (2006) Musculoskeletal plasticity after acute spinal cord injury: effects of long-term neuromuscular electrical stimulation training. J Neurophysiol 95: 2380-2390.
7. Grimby G, Broberg C, Krotkiewska I, Krotkiewski M (1976) Muscle fiber composition in patients with traumatic cord lesion. Scand J Rehabil Med 8: 37-42.
8. Petrie MA, Suneja M, Faidley E, Shields RK (2014) Low force contractions induce fatigue consistent with muscle mRNA expression in people with spinal cord injury. Physiol Rep 2: e00248.
9. Stuart CA, McCurry MP, Marino A, South MA, Howell MEA, et al. (2013) Slow-Twitch Fiber Proportion in Skeletal Muscle Correlates With Insulin Responsiveness. Journal of Clinical Endocrinology & Metabolism 98: 2027-2036.
10. Duckworth WC, Solomon SS, Jallepalli P, Heckemeyer C, Finnern J, et al. (1980) Glucose intolerance due to insulin resistance in patients with spinal cord injuries. Diabetes 29: 906-910.
11. BaumanWA, Adkins RH, Spungen AM, Waters RL (1999) The effect of residual neurological deficit on oral glucose tolerance in persons with chronic spinal cord injury. Spinal cord 37: 765-771.
12. Lavela SL, Weaver FM, Goldstein B, Chen K, Miskevics S, et al. (2006) Diabetes mellitus in individuals with spinal cord injury or disorder. J Spinal Cord Med 29: 387-395.
13. Jensen MP, Molton IR, Groah SL, Campbell ML, Charlifue S, et al. (2012) Secondary health conditions in individuals aging with SCI: terminology, concepts and analytic approaches. Spinal Cord 50: 373-378.
14. Cragg JJ, Noonan VK, Dvorak M, Krassioukov A, Mancini GB, et al. (2013) Spinal cord injury and type 2 diabetes: results from a population health survey. Neurology 81: 1864-1868.
15. Adams CM, Suneja M, Dudley-Javoroski S, Shields RK (2011) Altered mRNA expression after longterm soleus electrical stimulation training in humans with paralysis. Muscle Nerve 43: 65-75.
16. Dudley-Javoroski S, Littmann AE, Chang SH, McHenry CL, Shields RK (2011) Enhancing muscle force and femur compressive loads via feedback-controlled stimulation of paralyzed quadriceps in humans. Arch Phys Med Rehabil 92: 242-249.
17. Zijdewind I, Thomas CK (2012) Firing patterns of spontaneously active motor units in spinal cordinjured subjects. J Physiol 590: 1683-1697.
18. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, et al. (2003) PGC-1alpharesponsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet 34: 267-273.
19. Egan B, Zierath JR (2013) Exercise metabolism and the molecular regulation of skeletal muscle adaptation. Cell Metab 17: 162-184.
20. Egan B, Carson BP, Garcia-Roves PM, Chibalin AV, Sarsfield FM, et al. (2010) Exercise intensitydependent regulation of peroxisome proliferator-activated receptor coactivator-1 mRNA abundance is associated with differential activation of upstream signalling kinases in human skeletal muscle. J Physiol 588: 1779-1790.
21. Wallace MA, Hock MB, Hazen BC, Kralli A, Snow RJ, et al. (2011) Striated muscle activator of Rho signalling (STARS) is a PGC-1alpha/oestrogen-related receptor-alpha target gene and is upregulated in human skeletal muscle after endurance exercise. J Physiol 589: 2027-2039.
22. Kulkarni SS, Salehzadeh F, Fritz T, Zierath JR, Krook A, et al. (2012) Mitochondrial regulators of fatty acid metabolism reflect metabolic dysfunction in type 2 diabetes mellitus. Metabolism 61: 175-185.
23. Kawasaki E, Hokari F, Sasaki M, Sakai A, Koshinaka K, et al. (2009) Role of local muscle contractile activity in the exercise-induced increase in NR4A receptor mRNA expression. J Appl Physiol 106: 1826-1831.
24. Pearen MA, Eriksson NA, Fitzsimmons RL, Goode JM, Martel N, et al. (2012) The nuclear receptor, Nor-1, markedly increases type II oxidative muscle fibers and resistance to fatigue. Mol Endocrinol 26: 372-384.
25. Micheli L, Leonardi L, Conti F, Maresca G, Colazingari S, et al. (2011) PC4/Tis7/IFRD1 stimulates skeletal muscle regeneration and is involved in myoblast differentiation as a regulator of MyoD and NFkappaB. J Biol Chem 286: 5691-5707.
26. Wallace MA, Lamon S, Russell AP (2012) The regulation and function of the striated muscle activator of rho signaling (STARS) protein. Front Physiol 3: 469.
27. Lamon S, Wallace MA, Leger B, Russell AP (2009) Regulation of STARS and its downstream targets suggest a novel pathway involved in human skeletal muscle hypertrophy and atrophy. J Physiol 587: 1795-1803.
28. Spriet LL, Heigenhauser GJ (2002) Regulation of pyruvate dehydrogenase (PDH) activity in human skeletal muscle during exercise. Exerc Sport Sci Rev 30: 91-95.
29. Pilegaard H, Birk JB, Sacchetti M, Mourtzakis M, Hardie DG, et al. (2006) PDH-E1alpha dephosphorylation and activation in human skeletal muscle during exercise: effect of intralipid infusion. Diabetes 55: 3020-3027.
30. Brown RM, Head RA, Boubriak, II, Leonard JV, Thomas NH, et al. (2004) Mutations in the gene for the E1beta subunit: a novel cause of pyruvate dehydrogenase deficiency. Hum Genet 115: 123-127.
31. Spriet LL, Tunstall RJ, Watt MJ, Mehan KA, Hargreaves M, et al. (2004) Pyruvate dehydrogenase activation and kinase expression in human skeletal muscle during fasting. J Appl Physiol (1985) 96: 2082-2087.
32. Sugden MC, Holness MJ (2003) Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDKs. Am J Physiol Endocrinol Metab 284: E855-862.
33. Pruitt K, Brown G, Tatusova T, Maglott. D (Oct. 9, 2002) The Reference Sequence (RefSeq) Database. In: J McEntyre JO, editor. The NCBI Handbook [Internet]. Bethesda, MD National Center for Biotechnology Information (US).
34. Strauss AW, Powell CK, Hale DE, Anderson MM, Ahuja A, et al. (1995) Molecular basis of human mitochondrial very-long-chain acyl-CoA dehydrogenase deficiency causing cardiomyopathy and sudden death in childhood. Proc Natl Acad Sci U S A 92: 10496-10500.
35. Andresen BS, Bross P, Vianey-Saban C, Divry P, Zabot MT, et al. (1996) Cloning and characterization of human very-long-chain acyl-CoA dehydrogenase cDNA, chromosomal assignment of the gene and identification in four patients of nine different mutations within the VLCAD gene. Hum Mol Genet 5: 461-472.
36. Lea W, Abbas AS, Sprecher H, Vockley J, Schulz H (2000) Long-chain acyl-CoA dehydrogenase is a key enzyme in the mitochondrial beta-oxidation of unsaturated fatty acids. Biochim Biophys Acta 1485: 121-128.
37. Bricker DK, Taylor EB, Schell JC, Orsak T, Boutron A, et al. (2012) A Mitochondrial Pyruvate Carrier Required for Pyruvate Uptake in Yeast, Drosophila, and Humans. Science 337: 96-100.
38. Gaignard P, Menezes M, Schiff M, Bayot A, Rak M, et al. (2013) Mutations in CYC1, encoding cytochrome c1 subunit of respiratory chain complex III, cause insulin-responsive hyperglycemia. Am J Hum Genet 93: 384-389.
39. Iqbal S, Ostojic O, Singh K, Joseph AM, Hood DA (2013) Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve 48: 963-970.
40. Palikaras K, Tavernarakis N (2014) Mitochondrial homeostasis: The interplay between mitophagy and mitochondrial biogenesis. Exp Gerontol.
41. Shields RK, Dudley-Javoroski S (2007) Musculoskeletal adaptations in chronic spinal cord injury: effects of long-term soleus electrical stimulation training. Neurorehabil Neural Repair 21: 169-179.
42. Shields RK, Dudley-Javoroski S, Littmann AE (2006) Postfatigue potentiation of the paralyzed soleus muscle: evidence for adaptation with long-term electrical stimulation training. J Appl Physiol (1985) 101: 556-565.
43. Chu V, Hamarneh G. MATLAB-ITK interface for medical image filtering, segmentation, and registration. In: Reinhardt JM, Pluim JPW, editors; 2006; San Diego, CA, USA. SPIE. pp. 61443T-61448.
44. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.
45. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
46. Dudley-Javoroski S, Saha PK, Liang G, Li C, Gao Z, et al. (2012) High dose compressive loads attenuate bone mineral loss in humans with spinal cord injury. Osteoporos Int 23: 2335-2346.
47. Shields RK, Dudley-Javoroski S, Law LA (2006) Electrically induced muscle contractions influence bone density decline after spinal cord injury. Spine (Phila Pa 1976) 31: 548-553.
48. Henneman E (1985) The size-principle: a deterministic output emerges from a set of probabilistic connections. J Exp Biol 115: 105-112.
49. Bigland-Ritchie B, Johansson R, Lippold OC, Smith S, Woods JJ (1983) Changes in motoneurone firing rates during sustained maximal voluntary contractions. J Physiol 340: 335-346.
50. Holmstrom MH, Iglesias-Gutierrez E, Zierath JR, Garcia-Roves PM (2012) Tissue-specific control of mitochondrial respiration in obesity-related insulin resistance and diabetes. Am J Physiol Endocrinol Metab 302: E731-739.
51. Little JP, Safdar A, Bishop D, Tarnopolsky MA, Gibala MJ (2011) An acute bout of high-intensity interval training increases the nuclear abundance of PGC-1alpha and activates mitochondrial biogenesis in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 300: R1303-1310.
52. Arai A, Spencer JA, Olson EN (2002) STARS, a striated muscle activator of Rho signaling and serum response factor-dependent transcription. J Biol Chem 277: 24453-24459.
53. Giger JM, Bodell PW, Zeng M, Baldwin KM, Haddad F (2009) Rapid muscle atrophy response to unloading: pretranslational processes involving MHC and actin. J Appl Physiol (1985) 107: 1204-1212.
54. Jin W, Goldfine AB, Boes T, Henry RR, Ciaraldi TP, et al. (2011) Increased SRF transcriptional activity in human and mouse skeletal muscle is a signature of insulin resistance. J Clin Invest 121: 918-929.
55. Bricker DK, Taylor EB, Schell JC, Orsak T, Boutron A, et al. (2012) A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science 337: 96-100.
56. Barbour JA, Turner N (2014) Mitochondrial Stress Signaling Promotes Cellular Adaptations. Int J Cell Biol 2014: 156020.
57. Kim JA, Wei Y, Sowers JR (2008) Role of mitochondrial dysfunction in insulin resistance. Circ Res 102: 401-414.
58. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, et al. (2001) Restoration of insulinsensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc Natl Acad Sci U S A 98: 3820-3825.
59. Babraj JA, Vollaard NB, Keast C, Guppy FM, Cottrell G, et al. (2009) Extremely short duration high intensity interval training substantially improves insulin action in young healthy males. BMC Endocr Disord 9: 3.
60. Winnick JJ, Sherman WM, Habash DL, Stout MB, Failla ML, et al. (2008) Short-term aerobic exercise training in obese humans with type 2 diabetes mellitus improves whole-body insulin sensitivity through gains in peripheral, not hepatic insulin sensitivity. J Clin Endocrinol Metab 93: 771-778.
61. Little JP, Gillen JB, Percival ME, Safdar A, Tarnopolsky MA, et al. (2011) Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. J Appl Physiol 111: 1554-1560.
62. Fritz T, Caidahl K, Osler M, Ostenson CG, Zierath JR, et al. (2011) Effects of Nordic walking on healthrelated quality of life in overweight individuals with type 2 diabetes mellitus, impaired or normal glucose tolerance. Diabet Med 28: 1362-1372.