AQP4-Dependent Water Transport Plays a Functional Role in Exercise-Induced Skeletal Muscle Adaptations

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Basco, Davide ^a   Blaauw, Bert ^b,c   Pisani, Francesco ^a   Sparaneo, Angelo ^a   Nicchia, Grazia Paola ^a   Mola, Maria Grazia ^a   Reggiani, Carlo ^c,d   Svelto, Maria ^a   Frigeri, Antonio ^a  

^a UNIVERSITY OF BARI   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

^d CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AQUAPORIN 4; MESSENGER RNA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDURANCE; EXERCISE; FUNCTIONAL ASSESSMENT; MALE; MOUSE; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE TWITCH; NONHUMAN; OSMOSIS; PHYSICAL ACTIVITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; QUADRICEPS FEMORIS MUSCLE; RAT; SARCOLEMMA; SKELETAL MUSCLE; WATER PERMEABILITY; WATER TRANSPORT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; AQUAPORIN 4; BIOLOGICAL TRANSPORT, ACTIVE; MALE; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE FIBERS, FAST-TWITCH; MUSCLE PROTEINS; OSMOTIC PRESSURE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, WISTAR; WATER;

EID: 84874781379     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0058712     Document Type: Article

References (37)

1. Usher-Smith JA, Huang CL, Fraser JA, (2009) Control of cell volume in skeletal muscle. Biol Rev Camb Philos Soc 84: 143-159.
2. Frigeri A, Gropper MA, Umenishi F, Kawashima M, Brown D, et al. (1995) Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues. J Cell Sci108 (Pt 9): 2993-3002.
3. Jung JS, Bhat RV, Preston GM, Guggino WB, Baraban JM, et al. (1994) Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance. Proc Natl Acad Sci U S A 91: 13052-13056.
4. Verbavatz JM, Ma T, Gobin R, Verkman AS, (1997) Absence of orthogonal arrays in kidney, brain and muscle from transgenic knockout mice lacking water channel aquaporin-4. J Cell Sci110 (Pt 22): 2855-2860.
5. Silberstein C, Bouley R, Huang Y, Fang P, Pastor-Soler N, et al. (2004) Membrane organization and function of M1 and M23 isoforms of aquaporin-4 in epithelial cells. Am J Physiol Renal Physiol 287: F501-511.
6. Nicchia GP, Rossi A, Mola MG, Pisani F, Stigliano C, et al. (2010) Higher order structure of aquaporin-4. Neuroscience 168: 903-914.
7. Assereto S, Mastrototaro M, Stringara S, Gazzerro E, Broda P, et al. (2008) Aquaporin-4 expression is severely reduced in human sarcoglycanopathies and dysferlinopathies. Cell Cycle 7: 2199-2207.
8. Frigeri A, Nicchia GP, Nico B, Quondamatteo F, Herken R, et al. (2001) Aquaporin-4 deficiency in skeletal muscle and brain of dystrophic mdx mice. Faseb J 15: 90-98.
9. Frigeri A, Nicchia GP, Repetto S, Bado M, Minetti C, et al. (2002) Altered aquaporin-4 expression in human muscular dystrophies: a common feature? Faseb J 16: 1120-1122.
10. Schotland DL, Bonilla E, Wakayama Y, (1981) Freeze fracture studies of muscle plasma membrane in human muscular dystrophy. Acta Neuropathol 54: 189-197.
11. Wakayama Y, Jimi T, Inoue M, Kojima H, Murahashi M, et al. (2002) Reduced aquaporin 4 expression in the muscle plasma membrane of patients with Duchenne muscular dystrophy. Arch Neurol 59: 431-437.
12. Crenshaw AG, Thornell LE, Friden J, (1994) Intramuscular pressure, torque and swelling for the exercise-induced sore vastus lateralis muscle. Acta Physiol Scand 152: 265-277.
13. Greenleaf JE, Van Beaumont W, Brock PJ, Morse JT, Mangseth GR, (1979) Plasma volume and electrolyte shifts with heavy exercise in sitting and supine positions. Am J Physiol 236: R206-214.
14. Lindinger MI, Spriet LL, Hultman E, Putman T, McKelvie RS, et al. (1994) Plasma volume and ion regulation during exercise after low- and high-carbohydrate diets. Am J Physiol 266: R1896-1906.
15. Basco D, Nicchia GP, D'Alessandro A, Zolla L, Svelto M, et al. (2011) Absence of aquaporin-4 in skeletal muscle alters proteins involved in bioenergetic pathways and calcium handling. PLoS One 6: e19225.
16. Yang B, Verbavatz JM, Song Y, Vetrivel L, Manley G, et al. (2000) Skeletal muscle function and water permeability in aquaporin-4 deficient mice. Am J Physiol Cell Physiol 278: C1108-1115.
17. Basco D, Nicchia GP, Desaphy JF, Camerino DC, Frigeri A, et al. (2010) Analysis by two-dimensional Blue Native/SDS-PAGE of membrane protein alterations in rat soleus muscle after hindlimb unloading. Eur J Appl Physiol 110: 1215-1224.
18. Frigeri A, Nicchia GP, Desaphy JF, Pierno S, De Luca A, et al. (2001) Muscle loading modulates aquaporin-4 expression in skeletal muscle. Faseb J 15: 1282-1284.
19. Kaakinen M, Salmela P, Zelenin S, Metsikko K, (2007) Distribution of aquaporin 4 on sarcolemma of fast-twitch skeletal myofibres. Cell Tissue Res 329: 529-539.
20. Aldridge GM, Podrebarac DM, Greenough WT, Weiler IJ, (2008) The use of total protein stains as loading controls: an alternative to high-abundance single-protein controls in semi-quantitative immunoblotting. Journal of neuroscience methods 172: 250-254.
21. Dittmer A, Dittmer J, (2006) Beta-actin is not a reliable loading control in Western blot analysis. Electrophoresis 27: 2844-2845.
22. Romero-Calvo I, Ocon B, Martinez-Moya P, Suarez MD, Zarzuelo A, et al. (2010) Reversible Ponceau staining as a loading control alternative to actin in Western blots. Analytical biochemistry 401: 318-320.
23. Liu YF, Chen HI, Wu CL, Kuo YM, Yu L, et al. (2009) Differential effects of treadmill running and wheel running on spatial or aversive learning and memory: roles of amygdalar brain-derived neurotrophic factor and synaptotagmin I. J Physiol 587: 3221-3231.
24. Waters JC, (2009) Accuracy and precision in quantitative fluorescence microscopy. The Journal of cell biology 185: 1135-1148.
25. Blaauw B, Canato M, Agatea L, Toniolo L, Mammucari C, et al. (2009) Inducible activation of Akt increases skeletal muscle mass and force without satellite cell activation. Faseb J 23: 3896-3905.
26. Frigeri A, Nicchia GP, Verbavatz JM, Valenti G, Svelto M, (1998) Expression of aquaporin-4 in fast-twitch fibers of mammalian skeletal muscle. J Clin Invest 102: 695-703.
27. Frigeri A, Nicchia GP, Balena R, Nico B, Svelto M, (2004) Aquaporins in skeletal muscle: reassessment of the functional role of aquaporin-4. Faseb J 18: 905-907.
28. Fraysse B, Desaphy JF, Pierno S, De Luca A, Liantonio A, et al. (2003) Decrease in resting calcium and calcium entry associated with slow-to-fast transition in unloaded rat soleus muscle. Faseb J 17: 1916-1918.
29. Schiaffino S, Reggiani C, (2011) Fiber types in mammalian skeletal muscles. Physiological reviews 91: 1447-1531.
30. Pisani F, Rossi A, Nicchia GP, Svelto M, (2011) Frigeri (2011) A Translational regulation mechanisms of aquaporin-4 supramolecular organization in astrocytes. Glia 59: 1923-1932.
31. Hinnebusch A (2000) In:Sonenberg N, Hershey JWB, Mathews MB, editors. Translational Control of Gene Expression. Cold Spring HarborvNY:Cold Spring Harbor Laboratory Press. pp. 185-243.
32. She P, Zhang Z, Marchionini D, Diaz WC, Jetton TJ, et al. (2011) Molecular characterization of skeletal muscle atrophy in the R6/2 mouse model of Huntington's disease. American journal of physiology Endocrinology and metabolism 301: E49-61.
33. Fan Y, Zhang J, Sun XL, Gao L, Zeng XN, et al. (2005) Sex- and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice. J Neurosci Res 82: 458-464.
34. Fathi R, Ghanbari-Niaki A, Kraemer RR, Talebi-Garakani E, Saghebjoo M, (2010) The effect of exercise intensity on plasma and tissue acyl ghrelin concentrations in fasted rats. Regul Pept 165: 133-137.
35. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, et al. (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10: 197-205.
36. Bustin SA, Benes V, Nolan T, Pfaffl MW, (2005) Quantitative real-time RT-PCR--a perspective. Journal of molecular endocrinology 34: 597-601.
37. Pisani F, Mastrototaro M, Rossi A, Nicchia GP, Tortorella C, et al. (2011) Identification of two major conformational aquaporin-4 epitopes for neuromyelitis optica autoantibody binding. J Biol Chem 286: 9216-9224.