When the brain goes diving: glial oxidative metabolism may confer hypoxia tolerance to the seal brain

Neuroscience

Volumn 163, Issue 2, 2009, Pages 552-560

  Mitz, S A ^a,b   Reuss, S ^b   Folkow, L P ^c   Blix, A S ^c   Ramirez, J M ^d   Hankeln, T ^e   Burmester, T ^a  

^a UNIVERSITY OF HAMBURG   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

^c UNIVERSITY OF TROMSØ   (Norway)

^d SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

astrocytes; cytochrome c; deep diving; lactate shuttle; neuroglobin; seal

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYTOCHROME C; NEUROGLOBIN; REACTIVE OXYGEN METABOLITE;

ADAPTATION; AEROBIC METABOLISM; AMINO ACID SUBSTITUTION; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN CORTEX; BRAIN METABOLISM; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIVING; ENERGY METABOLISM; GLIA CELL; HYPOXIA; MOUSE; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYGEN AFFINITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SEAL;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; ASTROCYTES; BRAIN; CEREBELLUM; CYTOCHROMES C; FEMALE; GLOBINS; HYPOXIA, BRAIN; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROGLIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; SEALS, EARLESS; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY;

EID: 69249208538     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.06.058     Document Type: Article

References (48)

1. Bentmann A., Schmidt M., Reuss S., Wolfrum U., Hankeln T., and Burmester T. Divergent distribution in vascular and avascular mammalian retinae links neuroglobin to cellular respiration. J Biol Chem 280 (2005) 20660-20665
2. Blix A.S., and Folkow B. Cardiovascular adjustments to diving in mammals and birds. In: Shepherd J.T., and Abboud F.M. (Eds). Handbook of physiology-the cardiovascular system III (1983), American Physiological Society, Bethesda 917-945
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
4. Burmester T., Haberkamp M., Mitz S., Roesner A., Schmidt M., Ebner B., Gerlach F., Fuchs C., and Hankeln T. Neuroglobin and cytoglobin: genes, proteins and evolution. IUBMB Life 56 (2004) 703-707
5. Burmester T., and Hankeln T. Neuroglobin and other nerve globins. In: Bolognesi M., et al. (Ed). Protein reviews Vol. 9 (2008), Springer Verlag Italia, Milan 211-222
6. Burmester T., and Hankeln T. What is the function of neuroglobin?. J Exp Biol 212 (2009) 1423-1428
7. Burmester T., Weich B., Reinhardt S., and Hankeln T. A vertebrate globin expressed in the brain. Nature 407 (2000) 520-523
8. Butler P.J. Metabolic regulation in diving birds and mammals. Respir Physiol Neurobiol 141 (2004) 297-315
9. Butler P.J., and Jones D.R. Physiology of diving of birds and mammals. Physiol Rev 77 (1997) 837-899
10. Choi D.W. Cerebral hypoxia: some new approaches and unanswered questions. J Neurosci 10 (1990) 2493-2501
11. Dewilde S., Kiger L., Burmester T., Hankeln T., Baudin-Creuza V., Aerts T., Marden M.C., Caubergs R., and Moens L. Biochemical characterization and ligand binding properties of neuroglobin, a novel member of the globin family. J Biol Chem 276 (2001) 38949-38955
12. Folkow L.P., and Blix A.S. Diving behaviour of hooded seals (Cystophora cristata) in the Greenland and Norwegian Seas. Polar Biol 22 (1999) 61-74
13. Folkow L.P., Ramirez J.M., Ludvigsen S., Ramirez N., and Blix A.S. Remarkable neuronal hypoxia tolerance in the deep-diving adult hooded seal (Cystophora cristata). Neurosci Lett 446 (2008) 147-150
14. Halliwell B. Oxidative stress and neurodegeneration: where are we now?. J Neurochem 97 (2006) 1634-1658
15. Hankeln T., Ebner B., Fuchs C., Gerlach F., Haberkamp M., Laufs T.L., Roesner A., Schmidt M., Weich B., Wystub S., Saaler-Reinhardt S., Reuss S., Bolognesi M., De Sanctis D., Marden M.C., Kiger L., Moens L., Dewilde S., Nevo E., Avivi A., Weber R.E., Fago A., and Burmester T. Neuroglobin and cytoglobin in search of their role in the vertebrate globin family. J Inorg Biochem 99 (2005) 110-119
16. Hankeln T., Wystub S., Laufs T., Schmidt M., Gerlach F., Saaler-Reinhardt S., Reuss S., and Burmester T. The cellular and subcellular localization of neuroglobin and cytoglobin-a clue to their function?. IUBMB Life 56 (2004) 671-679
17. Herold S., Fago A., Weber R.E., Dewilde S., and Moens L. Reactivity studies of the Fe(III) and Fe(II)NO forms of human neuroglobin reveal a potential role against oxidative stress. J Biol Chem 279 (2004) 22841-22847
18. Itoh Y., Esaki T., Shimoji K., Cook M., Law M.J., Kaufman E., and Sokoloff L. Dichloroacetate effects on glucose and lactate oxidation by neurons and astroglia in vitro and on glucose utilization by brain in vivo. Proc Natl Acad Sci U S A 100 (2003) 4879-4884
19. Katsura K., Kristian T., and Siesjo B.K. Energy metabolism, ion homeostasis, and cell damage in the brain. Biochem Soc Trans 22 (1994) 991-996
20. Kerem D., and Elsner R. Cerebral tolerance to asphyxial hypoxia in the harbor seal. Respir Physiol 19 (1973) 188-200
21. Khan A.A., Wang Y., Sun Y., Mao X.O., Xie L., Miles E., Graboski J., Chen S., Ellerby L.M., Jin K., and Greenberg D.A. Neuroglobin-overexpressing transgenic mice are resistant to cerebral and myocardial ischemia. Proc Natl Acad Sci U S A 103 (2006) 17944-17948
22. Kraus D.W., and Colacino J.M. Extended oxygen delivery from the nerve hemoglobin of Tellina alternata (Bivalvia). Science 232 (1986) 90-92
23. Laufs T.L., Wystub S., Reuss S., Burmester T., Saaler-Reinhardt S., and Hankeln T. Neuron-specific expression of neuroglobin in mammals. Neurosci Lett 362 (2004) 83-86
24. Lenfant C., Johansen K., and Torrance J.D. Gas transport and oxygen storage capacity in some pinnipeds and the sea otter. Respir Physiol 9 (1970) 277-286
25. Lutz P.L., and Nilsson G.E. Vertebrate brains at the pilot light. Respir Physiol Neurobiol 141 (2004) 285-296
26. Magistretti P.J. Neuron-glia metabolic coupling and plasticity. J Exp Biol 209 (2006) 2304-2311
27. Odden A., Folkow L.P., Caputa M., Hotvedt R., and Blix A.S. Brain cooling in diving seals. Acta Physiol Scand 166 (1999) 77-78
28. Pellerin L. How astrocytes feed hungry neurons. Mol Neurobiol 32 (2005) 59-72
29. Pellerin L. Brain energetics (thought needs food). Curr Opin Clin Nutr Metab Care 11 (2008) 701-705
30. Peng L., Arystarkhova E., and Sweadner K.J. Plasticity of Na,K-ATPase isoform expression in cultures of flat astrocytes: species differences in gene expression. Glia 24 (1998) 257-271
31. Pesce A., Dewilde S., Nardini M., Moens L., Ascenzi P., Hankeln T., Burmester T., and Bolognesi M. Human brain neuroglobin structure reveals a distinct mode of controlling oxygen affinity. Structure 11 (2003) 1087-1095
32. Polasek L.K., and Davis R.W. Heterogeneity of myoglobin distribution in the locomotory muscles of five cetacean species. J Exp Biol 204 (2001) 209-215
33. Porollo A., and Meller J. Versatile annotation and publication quality visualization of protein complexes using POLYVIEW-3D. BMC Bioinformatics 8 (2007) 316
34. Qvist J., Hill R., Schneider R., Falke K., Liggins G., Guppy M., Elliot R., Hochachka P., and Zapol W. Hemoglobin concentrations and blood gas tensions of free-diving Weddell seals. J Appl Physiol 61 (1986) 1560-1569
35. Ramirez J.M., Folkow L.P., and Blix A.S. Hypoxia tolerance in mammals and birds: from the wilderness to the clinic. Annu Rev Physiol 69 (2007) 113-143
36. Reuss S., Saaler-Reinhardt S., Weich B., Wystub S., Reuss M.H., Burmester T., and Hankeln T. Expression analysis of neuroglobin mRNA in rodent tissues. Neuroscience 115 (2002) 645-656
37. Schmidt M., Gerlach F., Avivi A., Laufs T., Wystub S., Simpson J.C., Nevo E., Saaler-Reinhardt S., Reuss S., Hankeln T., and Burmester T. Cytoglobin is a respiratory protein in connective tissue and neurons, which is up-regulated by hypoxia. J Biol Chem 279 (2004) 8063-8069
38. Schmidt M., Giessl A., Laufs T., Hankeln T., Wolfrum U., and Burmester T. How does the eye breathe?. Evidence for neuroglobin-mediated oxygen supply in the mammalian retina. J Biol Chem 278 (2003) 1932-1935
39. Scholander P.F. Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets Skrifter 22 (1940) 1-131
40. Snyder G.K. Respiratory adaptations in diving mammals. Respir Physiol 54 (1983) 269-294
41. Sun Y., Jin K., Mao X.O., Zhu Y., and Greenberg D.A. Neuroglobin is up-regulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci U S A 98 (2001) 15306-15311
42. Sun Y., Jin K., Peel A., Mao X.O., Xie L., and Greenberg D.A. Neuroglobin protects the brain from experimental stroke in vivo. Proc Natl Acad Sci U S A 100 (2003) 3497-3500
43. Wang X., Liu J., Zhu H., Tejima E., Tsuji K., Murata Y., Atochin D.N., Huang P.L., Zhang C., and Lo E.H. Effects of neuroglobin overexpression on acute brain injury and long-term outcomes after focal cerebral ischemia. Stroke 39 (2008) 1869-1874
44. Williams T.M., Zavanelli M., Miller M.A., Goldbeck R.A., Morledge M., Casper D., Pabst D.A., McLellan W., Cantin L.P., and Kliger D.S. Running, swimming and diving modifies neuroprotecting globins in the mammalian brain. Proc Biol Sci 275 (2008) 751-758
45. Wittenberg J.B. Functions of cytoplasmatic hemoglobins and myohemerythrin. Adv Comp Environ Physiol 13 (1992) 60-85
46. Wong-Riley M.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12 (1989) 94-101
47. Wystub S., Ebner B., Fuchs C., Weich B., Burmester T., and Hankeln T. Interspecies comparison of neuroglobin, cytoglobin and myoglobin: sequence evolution and candidate regulatory elements. Cytogenet Genome Res 105 (2004) 65-78
48. Wystub S., Laufs T., Schmidt M., Burmester T., Maas U., Saaler-Reinhardt S., Hankeln T., and Reuss S. Localization of neuroglobin protein in the mouse brain. Neurosci Lett 346 (2003) 114-116