Combined walking exercise and alkali therapy in patients with CKD4-5 regulates intramuscular free amino acid pools and ubiquitin E3 ligase expression

European Journal of Applied Physiology

Volumn 113, Issue 8, 2013, Pages 2111-2124

  Watson, Emma L ^a   Kosmadakis, George C ^b   Smith, Alice C ^a,b   Viana, Joao L ^c,d   Brown, Jeremy R ^b   Molyneux, Karen ^a,b   Pawluczyk, Izabella Z A ^a   Mulheran, Michael ^a   Bishop, Nicolette C ^c   Shirreffs, Susan ^c   Maughan, Ronald J ^c   Owen, Paul J ^e   John, Stephen G ^e   McIntyre, Christopher W ^e   Feehally, John ^a,b   Bevington, Alan ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

^b UNIVERSITY HOSPITALS OF LEICESTER NHS TRUST   (United Kingdom)

^c LOUGHBOROUGH UNIVERSITY   (United Kingdom)

^d RESEARCH CENTER IN SPORTS SCIENCES   (Portugal)

^e UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Acidosis; Aerobic exercise; Amino acids; Chronic kidney disease; Skeletal muscle; Ubiquitin proteasome pathway

Indexed keywords

AMINO ACID; BICARBONATE; LACTIC ACID; MUSCLE PROTEIN; PROTEIN KINASE B; TRIM63 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ADULT; AGED; ARTICLE; BLOOD; CHRONIC KIDNEY FAILURE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; FEMALE; GENETICS; HUMAN; KINESIOTHERAPY; MALE; METABOLISM; MIDDLE AGED; MULTIMODALITY CANCER THERAPY; RANDOMIZED CONTROLLED TRIAL; SKELETAL MUSCLE; VERY ELDERLY; WALKING;

ADULT; AGED; AGED, 80 AND OVER; AMINO ACIDS; BICARBONATES; COMBINED MODALITY THERAPY; EXERCISE THERAPY; FEMALE; HUMANS; LACTIC ACID; MALE; MIDDLE AGED; MUSCLE PROTEINS; MUSCLE, SKELETAL; PROTO-ONCOGENE PROTEINS C-AKT; RENAL INSUFFICIENCY, CHRONIC; UBIQUITIN-PROTEIN LIGASES; WALKING;

EID: 84880830273     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-013-2628-5     Document Type: Article

References (58)

1. Asola MR, Virtanen KA, Peltoniemi P et al (2001) Amino acid transport into skeletal muscle is impaired in chronic renal failure. J Am Soc Nephrol 12:64A
2. Bailey JL, Zheng B, Hu Z, Price SR, Mitch WE (2006) Chronic kidney disease causes defects in signaling through the insulin receptor substrate/phosphatidylinositol 3-kinase/Akt pathway: implications for muscle atrophy. J Am Soc Nephrol 17:1388-1394. doi: 10.1681/ASN.2004100842
3. Baird FE, Pinilla-Tenas JJ, Ogilvie WL, Ganapathy V, Hundal HS, Taylor PM (2006) Evidence for allosteric regulation of pH-sensitive System A (SNAT2) and System N (SNAT5) amino acid transporter activity involving a conserved histidine residue. Biochem J 397:369-375. doi: 10.1042/BJ20060026
4. Baird FE, Bett KJ, MacLean C, Tee AR, Hundal HS, Taylor PM (2009) Tertiary active transport of amino acids reconstituted by coexpression of System A and L transporters in Xenopus oocytes. Am J Physiol Endocrinol Metab 297:E822-E829. doi: 10.1152/ajpendo.00330.2009
5. Bergstrom J, Alvestrand A, Furst P (1990) Plasma and muscle free amino acids in maintenance hemodialysis patients without protein malnutrition. Kidney Int 38:108-114
6. Biolo G, Tipton KD, Klein S, Wolfe RR (1997) An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 273:E122-E129
7. Bodine SC, Stitt TN, Gonzalez M et al (2001) Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014-1019. doi: 10.1038/ncb1101-1014
8. Borg GA (1982) Psychophysical bases of perceived exertion. Med Sci Sports Exerc 14:377-381
9. Cheema B, Abas H, Smith B et al (2007a) Randomized controlled trial of intradialytic resistance training to target muscle wasting in ESRD: the Progressive Exercise for Anabolism in Kidney Disease (PEAK) study. Am J Kidney Dis 50:574-584. doi: 10.1053/j.ajkd.2007.07.005
10. Cheema B, Abas H, Smith B et al (2007b) Progressive exercise for anabolism in kidney disease (PEAK): a randomized, controlled trial of resistance training during hemodialysis. J Am Soc Nephrol 18:1594-1601. doi: 10.1681/ASN.2006121329
11. Diesel W, Noakes TD, Swanepoel C, Lambert M (1990) Isokinetic muscle strength predicts maximum exercise tolerance in renal patients on chronic hemodialysis. Am J Kidney Dis 16:109-114
12. Dreyer HC, Drummond MJ, Pennings B et al (2008) Leucine-enriched essential amino acid and carbohydrate ingestion following resistance exercise enhances mTOR signaling and protein synthesis in human muscle. Am J Physiol Endocrinol Metab 294:E392-E400. doi: 10.1152/ajpendo.00582.2007
13. Du J, Wang X, Miereles C et al (2004) Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115-123. doi: 10.1172/JCI18330
14. Durozard D, Pimmel P, Baretto S et al (1993) 31P NMR spectroscopy investigation of muscle metabolism in hemodialysis patients. Kidney Int 43:885-892
15. Elia M, Carter A, Bacon S, Winearls CG, Smith R (1981) Clinical usefulness of urinary 3-methylhistidine excretion in indicating muscle protein breakdown. Br Med J (Clin Res Ed) 282:351-354
16. Evans K, Nasim Z, Brown J et al (2007) Acidosis-sensing glutamine pump SNAT2 determines amino acid levels and mammalian target of rapamycin signalling to protein synthesis in L6 muscle cells. J Am Soc Nephrol 18:1426-1436. doi: 10.1681/ASN.2006091014
17. Evans K, Nasim Z, Brown J et al (2008) Inhibition of SNAT2 by metabolic acidosis enhances proteolysis in skeletal muscle. J Am Soc Nephrol 19:2119-2129. doi: 10.1681/ASN.2007101108
18. Franch HA, Raissi S, Wang X, Zheng B, Bailey JL, Price SR (2004) Acidosis impairs insulin receptor substrate-1-associated phosphoinositide 3-kinase signaling in muscle cells: consequences on proteolysis. Am J Physiol Renal Physiol 287:F700-F706. doi: 10.1152/ajprenal.00440.2003
19. Goldberg AP, Geltman EM, Hagberg JM et al (1983) Therapeutic benefits of exercise training for hemodialysis patients. Kidney Int Suppl 16:S303-S309
20. Goldberg AP, Geltman EM, Gavin JR 3rd et al (1986) Exercise training reduces coronary risk and effectively rehabilitates hemodialysis patients. Nephron 42:311-316
21. Greenhaff PL, Gleeson M, Maughan RJ (1987) The effects of dietary manipulation on blood acid-base status and the performance of high intensity exercise. Eur J Appl Physiol Occup Physiol 56:331-337
22. Hyde R, Taylor PM, Hundal HS (2003) Amino acid transporters: roles in amino acid sensing and signalling in animal cells. Biochem J 373:1-18
23. Johansen KL (2007) Exercise in the end-stage renal disease population. J Am Soc Nephrol 18:1845-1854. doi: 10.1681/ASN.2007010009
24. Johansen KL, Painter PL, Sakkas GK, Gordon P, Doyle J, Shubert T (2006) Effects of resistance exercise training and nandrolone decanoate on body composition and muscle function among patients who receive hemodialysis: a randomized, controlled trial. J Am Soc Nephrol 17:2307-2314. doi: 10.1681/ASN.2006010034
25. Jones NL, Sutton JR, Taylor R, Toews CJ (1977) Effect of pH on cardiorespiratory and metabolic responses to exercise. J Appl Physiol 43:959-964
26. Kaizu Y, Ohkawa S, Odamaki M et al (2003) Association between inflammatory mediators and muscle mass in long-term hemodialysis patients. Am J Kidney Dis 42:295-302
27. Karlsson HK, Nilsson PA, Nilsson J, Chibalin AV, Zierath JR, Blomstrand E (2004) Branched-chain amino acids increase p70S6 k phosphorylation in human skeletal muscle after resistance exercise. Am J Physiol Endocrinol Metab 287:E1-E7. doi: 10.1152/ajpendo.00430.2003
28. Kemp GJ, Crowe AV, Anijeet HK et al (2004) Abnormal mitochondrial function and muscle wasting, but normal contractile efficiency, in haemodialysed patients studied non-invasively in vivo. Nephrol Dial Transplant 19:1520-1527. doi: 10.1093/ndt/gfh189
29. Kopple JD, Wang H, Casaburi R et al (2007) Exercise in maintenance hemodialysis patients induces transcriptional changes in genes favoring anabolic muscle. J Am Soc Nephrol 18:2975-2986. doi: 10.1681/ASN.2006070794
30. Kosmadakis GC, Bevington A, Smith AC et al (2010) Physical exercise in patients with severe kidney disease. Nephron Clin Pract 115:c7-c16. doi: 10.1159/000286344
31. Kosmadakis GC, John SG, Clapp EL et al (2011) Benefits of regular walking exercise in advanced pre-dialysis chronic kidney disease. Nephrol Dial Transplant. doi: 10.1093/ndt/gfr364
32. Kouidi E, Grekas D, Deligiannis A, Tourkantonis A (2004) Outcomes of long-term exercise training in dialysis patients: comparison of two training programs. Clin Nephrol 61(Suppl 1):S31-S38
33. Kovacic V, Roguljic L, Kovacic V (2003) Metabolic acidosis of chronically hemodialyzed patients. Am J Nephrol 23:158-164. doi: 10.1159/000070205
34. Lecker SH, Goldberg AL, Mitch WE (2006) Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17:1807-1819. doi: 10.1681/ASN.2006010083
35. Lofberg E, Wernerman J, Anderstam B, Bergstrom J (1997) Correction of acidosis in dialysis patients increases branched-chain and total essential amino acid levels in muscle. Clin Nephrol 48:230-237
36. Mackenzie B, Erickson JD (2004) Sodium-coupled neutral amino acid (System N/A) transporters of the SLC38 gene family. Pflugers Arch 447:784-795. doi: 10.1007/s00424-003-1117-9
37. MacRae HS, Dennis SC, Bosch AN, Noakes TD (1992) Effects of training on lactate production and removal during progressive exercise in humans. J Appl Physiol 72:1649-1656
38. Majchrzak KM, Pupim LB, Flakoll PJ, Ikizler TA (2008) Resistance exercise augments the acute anabolic effects of intradialytic oral nutritional supplementation. Nephrol Dial Transplant 23:1362-1369. doi: 10.1093/ndt/gfm773
39. Matthews DE (2005) Observations of branched-chain amino acid administration in humans. J Nutr 135:1580S-1584S
40. Mitch WE (2006) Metabolic and clinical consequences of metabolic acidosis. J Nephrol 19(Suppl 9):S70-S75
41. Movilli E, Viola BF, Camerini C, Mazzola G, Cancarini GC (2009) Correction of metabolic acidosis on serum albumin and protein catabolism in hemodialysis patients. J Ren Nutr 19:172-177. doi: 10.1053/j.jrn.2008.08.012
42. Nader GA (2006) Concurrent strength and endurance training: from molecules to man. Med Sci Sports Exerc 38:1965-1970. doi: 10.1249/01.mss. 0000233795.39282.33
43. Nicklin P, Bergman P, Zhang B et al (2009) Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136:521-534. doi: 10.1016/j.cell.2008.11.044
44. Painter P (2005) Physical functioning in end-stage renal disease patients: update 2005. Hemodial Int 9:218-235. doi: 10.1111/j.1492-7535.2005. 01136.x
45. Painter P, Moore GE (1994) The impact of recombinant human erythropoietin on exercise capacity in hemodialysis patients. Adv Ren Replace Ther 1:55-65
46. Painter P, Carlson L, Carey S, Paul SM, Myll J (2000) Physical functioning and health-related quality-of-life changes with exercise training in hemodialysis patients. Am J Kidney Dis 35:482-492
47. Painter PL, Hector L, Ray K et al (2002) A randomized trial of exercise training after renal transplantation. Transplantation 74:42-48
48. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
49. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR (1997) Mixed muscle protein synthesis and breakdown after resistance exercise in humans. Am J Physiol 273:E99-E107
50. Proud CG (2004) mTOR-mediated regulation of translation factors by amino acids. Biochem Biophys Res Commun 313:429-436
51. Reaich D, Channon SM, Scrimgeour CM, Daley SE, Wilkinson R, Goodship TH (1993) Correction of acidosis in humans with CRF decreases protein degradation and amino acid oxidation. Am J Physiol 265:E230-E235
52. Stein A, Moorhouse J, Iles-Smith H et al (1997) Role of an improvement in acid-base status and nutrition in CAPD patients. Kidney Int 52:1089-1095
53. Stitt TN, Drujan D, Clarke BA et al (2004) The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395-403
54. Szeto CC, Wong TY, Chow KM, Leung CB, Li PK (2003) Oral sodium bicarbonate for the treatment of metabolic acidosis in peritoneal dialysis patients: a randomized placebo-control trial. J Am Soc Nephrol 14:2119-2126
55. Tawney KW, Tawney PJ, Kovach J (2003) Disablement and rehabilitation in end-stage renal disease. Semin Dial 16:447-452
56. Wang XH, Du J, Klein JD, Bailey JL, Mitch WE (2009) Exercise ameliorates chronic kidney disease-induced defects in muscle protein metabolism and progenitor cell function. Kidney Int 76:751-759. doi: 10.1038/ki.2009.260
57. Workeneh BT, Rondon-Berrios H, Zhang L et al (2006) Development of a diagnostic method for detecting increased muscle protein degradation in patients with catabolic conditions. J Am Soc Nephrol 17:3233-3239. doi: 10.1681/ASN.2006020131
58. Zhang Z, Zander CB, Grewer C (2011) The C-terminal domain of the neutral amino acid transporter SNAT2 regulates transport activity through voltage-dependent processes. Biochem J 434:287-296. doi: 10.1042/BJ20100507