Absence of Aquaporin-4 in skeletal muscle alters proteins involved in bioenergetic pathways and calcium handling

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Basco, Davide ^a   Nicchia, Grazia Paola ^a   D'Alessandro, Angelo ^b   Zolla, Lello ^b   Svelto, Maria ^a   Frigeri, Antonio ^a  

^a UNIVERSITY OF BARI   (Italy)

^b UNIVERSITY OF TUSCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLOSUCCINATE SYNTHASE; ANAZOLENE SODIUM; AQUAPORIN 4; CALPHOBINDIN II; COLLAGEN TYPE 6; CREATINE KINASE; DYSTROPHIN; EUKARYOTIC TRANSLATION ELONGATION FACTOR 1 ALPHA 2; GENE PRODUCT; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOGEN PHOSPHORYLASE; GLYCOPROTEIN; LAMININ ALPHA2; MUSCLE GLYCOGEN PHOSPHORYLASE; MUSCLE PROTEIN; MYOSIN BINDING PROTEIN C; OXOGLUTARATE DEHYDROGENASE; PARVALBUMIN; PGM2 PROTEIN; PHOSPHOGLYCERATE MUTASE; PHOSPHOGLYCERATE MUTASE 2; PROTEOME; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 1; UNCLASSIFIED DRUG; VALOSIN CONTAINING PROTEIN; CALCIUM; SCLEROPROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; ELECTROSPRAY MASS SPECTROMETRY; ENERGY METABOLISM; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE TEST; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUADRICEPS FEMORIS MUSCLE; SARCOLEMMA; SKELETAL MUSCLE; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION; WESTERN BLOTTING; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; MALE; MASS SPECTROMETRY; METABOLISM; PROTEIN ANALYSIS; PROTEOMICS;

MUS;

ANIMALS; AQUAPORIN 4; CALCIUM; DYSTROPHIN; ENERGY METABOLISM; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; MALE; MASS SPECTROMETRY; MICE; MUSCLE, SKELETAL; PROTEIN INTERACTION MAPPING; PROTEOMICS; QUADRICEPS MUSCLE; SARCOLEMMA;

EID: 79955723731     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0019225     Document Type: Article

References (47)

1. 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 Sci 108 (Pt 9): 2993-3002.
2. 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.
3. Greenleaf JE, Van BW, 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-R214.
4. 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.
5. 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-R1906.
6. 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.
7. 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.
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. Vajda Z, Pedersen M, Doczi T, Sulyok E, Nielsen S, (2004) Studies of mdx mice. Neuroscience 129: 993-998.
13. 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.
14. Adams ME, Mueller HA, Froehner SC, (2001) In vivo requirement of the alpha-syntrophin PDZ domain for the sarcolemmal localization of nNOS and aquaporin-4. J Cell Biol 155: 113-122.
15. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, et al. (2001) Syntrophin-dependent expression and localization of Aquaporin-4 water channel protein. Proc Natl Acad Sci U S A 98: 14108-14113.
16. 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.
17. Fan Y, Kong H, Shi X, Sun X, Ding J, et al. (2008) Hypersensitivity of aquaporin 4-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine and astrocytic modulation. Neurobiol Aging 29: 1226-1236.
18. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, et al. (2007) Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 34: 34-39.
19. Zhou J, Kong H, Hua X, Xiao M, Ding J, et al. (2008) Altered blood-brain barrier integrity in adult aquaporin-4 knockout mice. Neuroreport 19: 1-5.
20. Kong H, Fan Y, Xie J, Ding J, Sha L, et al. (2008) AQP4 knockout impairs proliferation, migration and neuronal differentiation of adult neural stem cells. J Cell Sci 121: 4029-4036.
21. Menke A, Jockusch H, (1991) Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse. Nature 349: 69-71.
22. Weller B, Karpati G, Carpenter S, (1990) Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. J Neurol Sci 100: 9-13.
23. Straub V, Rafael JA, Chamberlain JS, Campbell KP, (1997) Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J Cell Biol 139: 375-385.
24. Halawani D, Latterich M, (2006) p97: The cell's molecular purgatory? Mol Cell 22: 713-717.
25. van Gestel RA, van Solinge WW, van der Toorn HW, Rijksen G, Heck AJ, et al. (2010) Quantitative erythrocyte membrane proteome analysis with Blue-native/SDS PAGE. J Proteomics 73: 456-465.
26. Lewis SF, Haller RG, (1989) Skeletal muscle disorders and associated factors that limit exercise performance. Exerc Sport Sci Rev 17: 67-113.
27. Kell R, Pierce H, Swoap SJ, (1999) PGAM-M expression is regulated pretranslationally in hindlimb muscles and under altered loading conditions. J Appl Physiol 86: 236-242.
28. Cros N, Muller J, Bouju S, Pietu G, Jacquet C, et al. (1999) Upregulation of M-creatine kinase and glyceraldehyde3-phosphate dehydrogenase: two markers of muscle disuse. Am J Physiol 276: R308-R316.
29. Basco D, Mastrototaro M, Sparaneo A, Nicchia GP, Svelto M, et al. (2010) Strongly impaired muscle activity in mice lacking Aquaporin-4 water channel. Neuromuscular Disorders 20/9-10: 680 doi:10.1016/j.nmd.2010.07.267.
30. Diaz-Munoz M, Hamilton SL, Kaetzel MA, Hazarika P, Dedman JR, (1990) Modulation of Ca2+ release channel activity from sarcoplasmic reticulum by annexin VI (67-kDa calcimedin). J Biol Chem 265: 15894-15899.
31. Thrane AS, Rappold PM, Fujita T, Torres A, Bekar LK, et al. (2010) Critical role of aquaporin-4 (AQP4) in astrocytic Ca2+ signaling events elicited by cerebral edema. Proc Natl Acad Sci U S A 108: 846-851.
32. Miura P, Coriati A, Belanger G, De RY, Lee J, et al. (2010) The utrophin A 5′-UTR drives cap-independent translation exclusively in skeletal muscles of transgenic mice and interacts with eEF1A2. Hum Mol Genet 19: 1211-1220.
33. Mansilla F, Dominguez CA, Yeadon JE, Corydon TJ, Burden SJ, et al. (2008) Translation elongation factor eEF1A binds to a novel myosin binding protein-C-like protein. J Cell Biochem 105: 847-858.
34. Hetzer M, Meyer HH, Walther TC, Bilbao-Cortes D, Warren G, et al. (2001) Distinct AAA-ATPase p97 complexes function in discrete steps of nuclear assembly. Nat Cell Biol 3: 1086-1091.
35. Jarosch E, Geiss-Friedlander R, Meusser B, Walter J, Sommer T, (2002) Protein dislocation from the endoplasmic reticulum-pulling out the suspect. Traffic 3: 530-536.
36. Rabinovich E, Kerem A, Frohlich KU, Diamant N, Bar-Nun S, (2002) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol Cell Biol 22: 626-634.
37. Rabouille C, Kondo H, Newman R, Hui N, Freemont P, et al. (1998) Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell 92: 603-610.
38. Weihl CC, Pestronk A, Kimonis VE, (2009) Valosin-containing protein disease: Inclusion body myopathy with Paget's disease of the bone and fronto-temporal dementia. Neuromuscular Disorders 19: 308-315.
39. Shaw CE, (2010) Capturing VCP: another molecular piece in the ALS jigsaw puzzle. Neuron 68: 812-814.
40. Blake DJ, Tinsley JM, Davies KE, (1996) Utrophin: a structural and functional comparison to dystrophin. Brain Pathol 6: 37-47.
41. Schagger H, Cramer WA, von JG, (1994) Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein complexes by two-dimensional native electrophoresis. Anal Biochem 217: 220-230.
42. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333.
43. Shevchenko A, Wilm M, Vorm O, Mann M, (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
44. Murgiano L, D'Alessandro A, Egidi MG, Crisa A, Prosperini G, et al. (2010) Proteomics and transcriptomics investigation on longissimus muscles in Large White and Casertana pig breeds. J Proteome Res 9: 6450-6466.
45. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, et al. (2009) STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37: D412-D416.
46. D'Alessandro A, Righetti PG, Zolla L, (2010) The red blood cell proteome and interactome: an update. J Proteome Res 9: 144-163.
47. Medina I, Carbonell J, Pulido L, Madeira SC, Goetz S, et al. (2010) Babelomics: an integrative platform for the analysis of transcriptomics, proteomics and genomic data with advanced functional profiling. Nucleic Acids Res 38: W210-W213.