Loss or Mislocalization of Aquaporin-4 Affects Diffusion Properties and Intermediary Metabolism in Gray Matter of Mice

Neurochemical Research

Volumn 42, Issue 1, 2017, Pages 77-91

  Pavlin, T ^a,b   Nagelhus, E A ^c   Brekken, C ^a   Eyjolfsson, E M ^a   Thoren, A ^c   Haraldseth, O ^a   Sonnewald, U ^a,d   Ottersen, O P ^c   Haberg A K ^a,e  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF BERGEN   (Norway)

^c UNIVERSITY OF OSLO   (Norway)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

13C MRS; Cortex; Diffusion weighted MRI; Glucose; Glutamate; Membrane permeability

Indexed keywords

4 AMINOBUTYRIC ACID; ALANINE; ALPHA SYNTROPHIN; AMINO ACID RECEPTOR AFFECTING AGENT; AQUAPORIN 4; ASPARTIC ACID; CREATINE; GLUTAMIC ACID; GLUTAMINE; LACTIC ACID; N ACETYLASPARTIC ACID; SYNTROPHIN; TAURINE; UNCLASSIFIED DRUG; ALPHA SYNUCLEIN; AQP4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CARBON NUCLEAR MAGNETIC RESONANCE; CONTROLLED STUDY; DIFFUSION COEFFICIENT; DIFFUSION WEIGHTED IMAGING; EXTRACELLULAR SPACE; FEMALE; GLUCOSE METABOLISM; GRAY MATTER; IN VIVO STUDY; LIGHT DARK CYCLE; MALE; MEMBRANE PERMEABILITY; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; PROTEIN METABOLISM; STEADY STATE; WATER FLOW; WATER PERMEABILITY; ANIMAL; BRAIN CORTEX; C57BL MOUSE; CHEMISTRY; DIFFUSION; KNOCKOUT MOUSE; METABOLISM;

ALPHA-SYNUCLEIN; ANIMALS; AQUAPORIN 4; CEREBRAL CORTEX; DIFFUSION; FEMALE; GRAY MATTER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

EID: 85007417980     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-016-2139-y     Document Type: Article

References (63)

1. Nielsen S, Nagelhus EA, Amiry-Moghaddam M, Bourque C, Agre P, Ottersen OP (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J Neurosci 17(1):171–180
2. Nagelhus EA, Ottersen OP (2013) Physiological roles of aquaporin-4 in brain. Physiol Rev 93(4):1543–1562
3. Amiry-Moghaddam M, Frydenlund DS, Ottersen OP (2004) Anchoring of aquaporin-4 in brain: molecular mechanisms and implications for the physiology and pathophysiology of water transport. Neuroscience 129(4):999–1010
4. Neely JD, Amiry-Moghaddam M, Ottersen OP, Froehner SC, Agre P, Adams ME (2001) Syntrophin-dependent expression and localization of aquaporin-4 water channel protein. Proc Natl Acad Sci USA 98(24):14108–14113
5. Iliff JJ, Wang M, Liao Y, Plogg BA, Peng W, Gundersen GA, Benveniste H, Vates GE, Deane R, Goldman SA et al (2012) A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid β. Sci Transl Med 4(147):147ra111
6. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O’Donnell J, Christensen DJ, Nicholson C, Iliff JJ et al (2013) Sleep drives metabolite clearance from the adult brain. Science 342(6156):373–377
7. Papadopoulos MC, Verkman AS (2013) Aquaporin water channels in the nervous system. Nat Rev Neurosci 14(4):265–277
8. Eid T, Lee TS, Thomas MJ, Amiry-Moghaddam M, Bjørnsen LP, Spencer DD, Agre P, Ottersen OP, de Lanerolle NC (2005) Loss of perivascular aquaporin 4 may underlie deficient water and K + homeostasis in the human epileptogenic hippocampus. Proc Natl Acad Sci USA 102(4):1193–1198
9. Binder DK, Yao X, Zador Z, Sick TJ, Verkman AS, Manley GT (2006) Increased seizure duration and slowed potassium kinetics in mice lacking aquaporin-4 water channels. Glia 53(6):631–636
10. Alvestad S, Hammer J, Hoddevik EH, Skare Ø, Sonnewald U, Amiry-Moghaddam M, Ottersen OP (2013) Mislocalization of AQP4 precedes chronic seizures in the kainate model of temporal lobe epilepsy. Epilepsy Res 105(1–2):30–41
11. Hinson SR, Lennon VA, Pittock SJ (2016) Autoimmune AQP4 channelopathies and neuromyelitis optica spectrum disorders. Handb Clin Neurol 133:377–403
12. Yang J, Lunde LK, Nuntagij P, Oguchi T, Camassa LM, Nilsson LN, Lannfelt L, Xu Y, Amiry-Moghaddam M, Ottersen OP et al (2011) Loss of astrocyte polarization in the tg-ArcSwe mouse model of Alzheimer’s disease. J Alzheimers Dis 27(4):711–722
13. Verkman AS, Wong KR (1987) Proton nuclear magnetic resonance measurement of diffusional water permeability in suspended renal proximal tubules. Biophys J 51(5):717–723
14. Benga G, Matei H, Borza T, Poruţiu D, Lupşe C (1993) Comparative nuclear magnetic resonance studies on water diffusional permeability of red blood cells from mice and rats. Comp Biochem Physiol Comp Physiol 104(3):491–495
15. Lahajnar G, Macek P, Zupancic I (2000) Suppression of red cell diffusional water permeability by lipophilic solutes. Bioelectrochemistry 52(2):179–185
16. Ibata K, Takimoto S, Morisaku T, Miyawaki A, Yasui M (2011) Analysis of aquaporin-mediated diffusional water permeability by coherent anti-stokes Raman scattering microscopy. Biophys J 101(9):2277–2283
17. Aslund I, Nowacka A, Nilsson M, Topgaard D (2009) Filter-exchange PGSE NMR determination of cell membrane permeability. J Magn Reson 200(2):291–295
18. Meng S, Qiao M, Lin L, Del Bigio MR, Tomanek B, Tuor UI (2004) Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur J Neurosci 19(8):2261–2269
19. Tourdias T, Dragonu I, Fushimi Y, Deloire MS, Boiziau C, Brochet B, Moonen C, Petry KG, Dousset V (2009) Aquaporin 4 correlates with apparent diffusion coefficient and hydrocephalus severity in the rat brain: a combined MRI-histological study. Neuroimage 47(2):659–666
20. Badaut J, Ashwal S, Adami A, Tone B, Recker R, Spagnoli D, Ternon B, Obenaus A (2011) Brain water mobility decreases after astrocytic aquaporin-4 inhibition using RNA interference. J Cereb Blood Flow Metab 31(3):819–831
21. Mitra PP, Sen PN, Schwartz LM (1993) Short-time behavior of the diffusion coefficient as a geometrical probe of porous media. Phys Rev B Condens Matter 47(14):8565–8574
22. Latour LL, Svoboda K, Mitra PP, Sotak CH (1994) Time-dependent diffusion of water in a biological model system. Proc Natl Acad Sci USA 91(4):1229–1233
23. Novikov DS, Fieremans E, Jensen JH, Helpern JA (2011) Random walk with barriers. Nat Phys 7(6):508–514
24. Novikov DS, Jensen JH, Helpern JA, Fieremans E (2014) Revealing mesoscopic structural universality with diffusion. Proc Natl Acad Sci USA 111(14):5088–5093
25. Burcaw LM, Fieremans E, Novikov DS (2015) Mesoscopic structure of neuronal tracts from time-dependent diffusion. Neuroimage 114:18–37
26. Dmytrenko L, Cicanic M, Anderova M, Vorisek I, Ottersen OP, Sykova E, Vargova L (2013) The impact of alpha-syntrophin deletion on the changes in tissue structure and extracellular diffusion associated with cell swelling under physiological and pathological conditions. PLoS One 8(7):e68044
27. Amiry-Moghaddam M, Williamson A, Palomba M, Eid T, de Lanerolle NC, Nagelhus EA, Adams ME, Froehner SC, Agre P, Ottersen OP (2003) Delayed K + clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice. Proc Natl Acad Sci USA 100(23):13615–13620
28. Cruz NF, Ball KK, Froehner SC, Adams ME, Dienel GA (2013) Regional registration of [6-(14)C]glucose metabolism during brain activation of α-syntrophin knockout mice. J Neurochem 125(2):247–259
29. Haberg A, Qu H, Sonnewald U (2006) Glutamate and GABA metabolism in transient and permanent middle cerebral artery occlusion in rat: importance of astrocytes for neuronal survival. Neurochem Int 48(6–7):531–540
30. 13C NMR Spectroscopy as a Toolin Neurobiology. In: Choi IY (ed) Neural metabolism in vivo. edn. Springer
31. Sonnewald U, Gribbestad IS, Westergaard N, Nilsen G, Unsgard G, Schousboe A, Petersen SB (1994) Nuclear magnetic resonance spectroscopy: biochemical evaluation of brain function in vivo and in vitro. Neurotoxicology 15(3):579–590
32. Sonnewald U, Kondziella D (2003) Neuronal glial interaction in different neurological diseases studied by ex vivo 13 C NMR spectroscopy. Nmr Biomed 16(6–7):424–429
33. Öz G, DiNuzzo M, Kumar A, Moheet A, Seaquist ER (2015) Revisiting Glycogen Content in the Human Brain. Neurochem Res 40(12):2473–2481
34. Roig ES, Magill AW, Donati G, Meyerspeer M, Xin L, Ipek O, Gruetter R (2015) A double-quadrature radiofrequency coil design for proton-decoupled carbon-13 magnetic resonance spectroscopy in humans at 7 T. Magn Reson Med 73(2):894–900
35. Thrane AS, Rappold PM, Fujita T, Torres A, Bekar LK, Takano T, Peng W, Wang F, Rangroo Thrane V, Enger R et al (2011) Critical role of aquaporin-4 (AQP4) in astrocytic Ca2 + signaling events elicited by cerebral edema. Proc Natl Acad Sci USA 108(2):846–851
36. Adams ME, Kramarcy N, Krall SP, Rossi SG, Rotundo RL, Sealock R, Froehner SC (2000) Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J Cell Biol 150(6):1385–1398
37. Parisi M, Dorr RA, Ozu M, Toriano R (2007) From membrane pores to aquaporins: 50 years measuring water fluxes. J Biol Phys 33(5–6):331–343
38. Solenov E, Watanabe H, Manley GT, Verkman AS (2004) Sevenfold-reduced osmotic water permeability in primary astrocyte cultures from AQP-4-deficient mice, measured by a fluorescence quenching method. Am J Physiol Cell Physiol 286(2):C426–C432
39. Verkman AS (2000) Water permeability measurement in living cells and complex tissues. J Membr Biol 173(2):73–87
40. Andrasko J (1976) Water diffusion permeability of human erythrocytes studied by a pulsed gradient NMR technique. Biochim Biophys Acta 428(2):304–311
41. Krager J (1969) Zur bestimmung der diffusion in einem zweibereichsystem mit hilfe von gepulsten feldgradienten. Ann Phys 479:1–4
42. Yao X, Hrabetová S, Nicholson C, Manley GT (2008) Aquaporin-4-deficient mice have increased extracellular space without tortuosity change. J Neurosci 28(21):5460–5464
43. Crick F (1970) Diffusion in embryogenesis. Nature 225(5231):420–422
44. Håberg A, Qu H, Haraldseth O, Unsgård G, Sonnewald U (1998) In vivo injection of [1-13C]glucose and [1,2-13C]acetate combined with ex vivo 13 C nuclear magnetic resonance spectroscopy: a novel approach to the study of middle cerebral artery occlusion in the rat. J Cereb Blood Flow Metab 18(11):1223–1232
45. Hassel B, Bachelard H, Jones P, Fonnum F, Sonnewald U (1997) Trafficking of amino acids between neurons and glia in vivo. Effects of inhibition of glial metabolism by fluoroacetate. J Cereb Blood Flow Metab 17(11):1230–1238
46. Lundgaard I, Li B, Xie L, Kang H, Sanggaard S, Haswell JD, Sun W, Goldman S, Blekot S, Nielsen M et al (2015) Direct neuronal glucose uptake Heralds activity-dependent increases in cerebral metabolism. Nat Commun 6:6807
47. Qu H, Haberg A, Haraldseth O, Unsgard G, Sonnewald U (2000) (13)C MR spectroscopy study of lactate as substrate for rat brain. Dev Neurosci 22(5–6):429–436
48. Sonnewald U, Westergaard N, Schousboe A, Svendsen JS, Unsgård G, Petersen SB (1993) Direct demonstration by [13C]NMR spectroscopy that glutamine from astrocytes is a precursor for GABA synthesis in neurons. Neurochem Int 22(1):19–29
49. Nehlig A, Coles JA (2007) Cellular pathways of energy metabolism in the brain: is glucose used by neurons or astrocytes? Glia 55(12):1238–1250
50. Qu H, Håberg A, Haraldseth O, Unsgård G, Sonnewald U (2000) (13)C MR spectroscopy study of lactate as substrate for rat brain. Dev Neurosci 22(5–6):429–436
51. Ottersen OP (1989) Postembedding immunogold labelling of fixed glutamate: an electron microscopic analysis of the relationship between gold particle density and antigen concentration. J Chem Neuroanat 2(1):57–66
52. Patel MS (1974) The relative significance of CO2-fixing enzymes in the metabolism of rat brain. J Neurochem 22(5):717–724
53. Yu AC, Drejer J, Hertz L, Schousboe A (1983) Pyruvate carboxylase activity in primary cultures of astrocytes and neurons. J Neurochem 41(5):1484–1487
54. Norenberg MD, Martinez-Hernandez A (1979) Fine structural localization of glutamine synthetase in astrocytes of rat brain. Brain Res 161(2):303–310
55. Ottersen OP, Zhang N, Walberg F (1992) Metabolic compartmentation of glutamate and glutamine: morphological evidence obtained by quantitative immunocytochemistry in rat cerebellum. Neuroscience 46(3):519–534
56. Kvamme E, Torgner IA, Roberg B (2001) Kinetics and localization of brain phosphate activated glutaminase. J Neurosci Res 66(5):951–958
57. Taylor A, McLean M, Morris P, Bachelard H (1996) Approaches to studies on neuronal/glial relationships by 13 C-MRS analysis. Dev Neurosci 18(5–6):434–442
58. Sullivan GM, Feinn R (2012) Using Effect Size-or Why the P Value Is Not Enough. J Grad Med Educ 4(3):279–282
59. Nilsson M, van Westen D, Ståhlberg F, Sundgren PC, Lätt J (2013) The role of tissue microstructure and water exchange in biophysical modelling of diffusion in white matter. MAGMA 26(4):345–370
60. Barry PH, Diamond JM (1984) Effects of unstirred layers on membrane phenomena. Physiol Rev 64(3):763–872
61. Sen P (2003) Time-dependent diffusion coefficient as a probe of the permeability of the pore wall. J Chem Phys 119(18):9871–9876
62. Amiry-Moghaddam M, Otsuka T, Hurn PD, Traystman RJ, Haug FM, Froehner SC, Adams ME, Neely JD, Agre P, Ottersen OP et al (2003) An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain. Proc Natl Acad Sci USA 100(4):2106–2111
63. Gandhi GK, Cruz NF, Ball KK, Dienel GA (2009) Astrocytes are poised for lactate trafficking and release from activated brain and for supply of glucose to neurons. J Neurochem 111(2):522–536